19th-century idealistic morphologists such natural-theological assumptions about a per- gram as one not dominated by a typological

as Carl F. Kielmeyer and3/30/09

0403NewsFocus.qxp J. F. Meckel 5:23 that
PM Page sonified
29 God who had created a perfectly and linear-recapitulationist mindset but
retained their teleology, their typological adapted nature. Bronn’s translation, though it rather as continuing to wrestle with the need
emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehen- to account for variability and unpredictable
tionism. This story, emphasizing the long per- sible to a German academic audience, was not change in terms of mechanistic laws of
sistence of a German transcendental approach a conservative throwback. It represented the nature—among which Haeckel included, at
to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolo- the top of his list, natural selection. Haeckel’s ORIGINS
Introduction

Contents
history of biology. gist who had also long been working on many Darwinism thus shows continuity with early-

Gliboff challenges this history
Stockholm. “When we started, right from of the questions Darwin claimed as his own— 19th-century concerns, mediated through
2 Darwin’s Inspiration, Darwin’s Legacy
the beginning. theThe
search ascription
profile was of simple
bigger, linear a critical yet generous equal, who saw himself Bronn. But those concerns were always more
Andrew Sugden
recapitulationism
a magnolia to the[flower],”
views of Romantic
she as moving science forward through the modi- flexible than has been acknowledged, and
embryologists, recalls.
he notes,But 30 owesyears ago,toshe
much a carica- fications he made to Darwin’s flawed theory. their articulation changed over time. Of
ture developed and by othersKarldiscovered
Ernst vontiny Baer in a Bronn’s death in 1862 afforded him little course Haeckel’s Darwinism was not
ancient flowers by sieving
polemical context, then adopted uncritically by chance to steer the conversation further.
Articles
Darwin’s own, but it was not an aberration or
through sand and clay sedi-
influential historians
ments. With suchthis as E. S.
technique, a distortion 3 ofOn the Origin
some true theory, of Life anyonmore
Earth
Russell and theyStephen
have now Jay collected
Gould. hun- than any otherCarl post-Darwinian
Zimmer additions or
Gliboff’s fresh reading
dreds of of the orig-
millimeter-size adjustments were.
ScienceIt was science
9 January moving
2009 on.
323: 198-199
inal sources flowers,
interpretssome Kielmeyer
preserved in Gliboff ’s overall picture of scientific
and Meckelthree as far dimensions,
less rigidly from Por- advance, in5 contrastOn the to Origin
Richards’s of Art and Symbolism
emphasis on
typological intugal
theirand other locations
orientation and with charisma andMichael passion, is one of scientists
Balter
Cretaceous deposits 70 mil-
much more lion attentive to nature’s
to 120 million years old.
building and innovating
Science 6 February
incrementally,2009 323: 709-711
work-
variability thanThis has fossil
been seen diversity ing with what their predecessors have handed
before. Bothshows
for these 8 On the Origin of Photosynthesis
that early-19th-
angiosperms were them and sculpting it into something new yet
century naturalists and for their
understandable Mitch
to Leslie
those around them. His sen-
thriving, with several groups
Science 6 March 2009 323: 1286-1287
intellectual heirs, Gliboff argues,
well-established, by 100 mil- sitive reading allows Out us of tothe seepast.post-1859
lion years ago.
the critical issue was to understand In some, the page 10 German evolutionists as Tinyrational
Amborellaactorssits rather
flower parts are whorled 10 On theatOrigin of Flowering Plants
nature’s manifold variety while like than irrationally stuck the
inbottom
someof early-19th-
the

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

those of modern flowers; in Elizabeth Pennisi
angiosperm family tree.
seeking out underlying strict natu- century moment with unmodern commit-
others they are spiraled, con- Science 3 April 2009 324: 28-31
ral laws to account for it.
sidered by some researchers ments. By challenging the very foundations of
This provides
as the amore newprimitive
starting arrangement. Some the standard
from one 14 of the narrative
Alexander
nonflowering of von
German Humboldt
seed morphol-
plants and the General Physics
prescribed numbers of “We are realizing that this or

CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE, UC SANTA CRUZ; PHOTO BY JENNIFER SVITKO, COURTESY OF WILLIAM L. CREPET, CORNELL UNIVERSITY
point for analyzing Darwin’s
flower fossils havefirst ogy, this careful,
gymnosperms, compelling
whose
of the Earth heyday account
was 200 does at
translator, the prominent
petals, anotherpaleon-
modern feature, whereas in
huge diversity is probably million least asyears
much

ago. Modern gymnosperms
as Richards’s
Stephen T. Jackson to undermine the
tologist H. G.others
Bronn—a the petal count
figure lit-varies. include conifers,
association of ginkgoes, andGerman the cycads,
Science 1 May 2009 324:Darwin-
19th-century 596-597
tle attended toInin1998, standardgeologist Ge Sun of the result of one innova-
the Chinese with their astout
ism with trunks and
dangerously large fronds.
exceptional view of
Jilin University in Changchun, China, came Before angiosperms came along, these
story but the lynchpin of Gli-
across what seemed to be a much older tion piled on top of
nature. But
plants were 16 themuch two books
Making more
offer
Germandiverse
very different
Evolution:
and Translation and Tragedy
boff’s. Intriguingly
flower. The andfossil,
plausibly,
called Archaefructus, was reads. Is cycadlike
included scientific
Lynn K. progress
Nyhartsuch
species, a matter
as theof per-
Gliboff argues that Bronn’s
an aquatic plant that uselooked to be 144 mil- another innovation.” sonal anguish
extinct and triumph,
Science
Bennettitales, 27
and or ofwoody
February
many intellectual
2009 323: 1170-1171
REPORTS
of terms likelion“vervollkommnet”
years old. By 2002, Sun and David chuggingcalled
plants along?Gnetales,
Our conceptofof which it should be
presence
(perfect) as Dilcher
translations of of
thetwo lineages
Florida
for that co-occur
Dar- Museum —Petersites
in the ad- 6.2% divergence). In contrast,
of Natural Crane,
located acapacious
few 18
population Darwin’s
expansion
representatives,
enough (23)Originality
to include areboth.
including found the in the
jacent refugia.
History
win’s “improved” or(FLMNH) In all species,
“favored”
average nethad
in Gainesville nucle- outside (south of)University
the refugiaofare
Chicago unstable
genetically joint firs, area for H.today
survive albomarginatus
Peter J. Bowler(see family and H. faber,
tree,
otide differences
described an entire across from
plant, localities
roots (22)
to reflects more similar to each other, although to a lesser p. as
flow- well
31). as incommon
Also the Bahia in refugium
the area for were
Jurassic H. faber
were not abouthigh dragging Darwin within refugia (2.6 to extent in H. faber (0.1 to 1.6%). Signatures of andReferences Science
H. semilineatus.
and Notes 9 January
The of 2009
lack gone; 323: 223-226
signature
geographic
ers, entombed on astructure
slab of rock unearthed in These fossils often spark debate because seed ferns,
1. E. Haeckel,a group
Generellenow long
Morphologie their of
der Organismen
backward into a German teleo-
Liaoning in northeastern China. page 16
specimens tend to be imperfectly preserved most(Georg famous member
Reimer, is Caytonia, which
Berlin, 1866).
logical view of nature (asArchaefructus
has in putative 22 The Red Queenpress and the Court Jester: Species Diversity
In one
Fig. 2. sense,
Genetic diversity wasn’t much and leave room for interpretation. To help seems 2. Theto have
reviewer precarpel-like
previously served as astructures.
reader for both
been claimedtoby those who
look at.(stable)
refugial have
“It’s versus
a flowering
unstableplant
A B books
at
Cthe and the
manuscript
areas before remedy that, Friis and her colleagues have These g roups’ perceived relevance to Role
stage. of Biotic and Abiotic Factors Through Time
paid attention intowere
there Bronn
the at all).
flowers,”
Brazilian Dilcher
Atlantic notes. It
rainforest. lacked begun to examine flowers using synchro-
A painter, too. Haeckel’s oil landscape of highlands in Java, from flower
evolution Michael
and J. Benton
their relationships to
Instead, Gliboff (Top)
petals Species-specific
and
asserts, sepals,
Bronn’sbut stability maps;have an tron radiation to generate a 3D image of angiosperms
it did
Wanderbilder (1905). Science
have 6 February
ping-ponged 2009 323: 728-732
between
10.1126/science.1169621
modeledcarpel.
enclosed refugiaWhenin black.
Kevin (A)Nixon
H. and their inner structures, allowing the fossil to camps, depending on how the evolutionary Pernambuco
albomarginatus, (B) H. semilineatus, refugium
colleagues at Cornell University compared remain intact while Friis peers inside it trees were26 Evidence
constructed. for Ecological Speciation and Its Alternative
(C) H. faber. Note the absence
its stable
traits regions
with those same
of large
www.sciencemag.org
traits in 173 living from SCIENCE
many angles VOL 323
(Science, 7 27 FEBRUARY
December In2009
the
mid-1980s,
Dolph Peter Crane,
Schluter now
Bahia at
refugium 1171
in the southern portion
plants, Archaefructus came out
of the forest (south of the Bahia and as a sister to *2007, p. 1546). “We can get fantastic reso- the University of Chicago in Illinois, pro-
* Science 6 February 2009 323: 737-741
living
São angiosperms
Paulo refugia)and closerto tothe
relative the com- lution,” says Friis. “It’s really exciting.” But posed a solution, the anthophyte hypothesis.
mon ancestor than even Amborella. so far, the flowers Friis finds are Using several
30 lines
The of evidenceSpecies
Bacterial and noting
Sã o Paulo refugium Challenge: Making Sense of Genetic
central and northern areas. Asterisks
Archaefructus’s
denote refugia inferreddistinction
beyond was the short- too diverse to trace back to a that both Bennettitales and
lived, however.
current ranges Within months,
of the target better dat- particular
species. ancestor. “From
Gnetales
and Ecological Diversity
organize their male
5.4%
ingSymbols
of the indicate
sediments localities sampled
in which for found these fossils, we cannot
it was and Christophe
female organs Eric J. Alm, Martin F. Polz, et al.
Fraser, together
molecular analysis. Scale bar, 400 km.
yielded younger dates, putting this f irst say what is the basic Science 6 February
in what could be 2009 323: 741-746
con-
(Bottom)
flower The 50%with
squarely majority-rule
other earlycon- fossil form,” she says. strued as a preflower,
sensus Bayesian phylogenetic trees,
flower parts, about 125 million years old. 7% 36 Stability Predicts Genetic
he considered
7.8% them, Diversity in the Brazilian Atlantic
rooted with sequences from the oth-
Also, a 2009 phylogenetic
er two congeneric species studied analysis of Before flowers Forest
along Hotspot
with angiosperms,
67 (root
taxanot
by shown).
Doyle Thick
and Peter Endress
internodes de- of thepage Although
36 they have yet
5.3 –
as comprising
Ana a single
Carolina Carnaval, Michael J. Hickerson, Célio F. B. Haddad, et al.
University
note cladesofwithZurich, Switzerland,
posterior probability placed to find the oldest fossil Larger than 5.8%
life. Although merely angiosperm
Science entity
6 February
4% 2009called
323: 785-789
thegreater
fossilthan
in with
90%.water liliesindicate
Percentages rather than at flowers, researchers 2.2 millimeters in diameter, this 3D anthophytes. For the next
Around the world, governments turn to AAAS as an objective, multidisciplinary scientific authority to theTamura-Nei
base of the angiosperms,
corrected although this assume that the ances-
distances between fossil flower shows that grasses date decade, most family trees
Science funding conclusion
clades (20).is contested. tral angiosperm evolved back to 94 million years ago. based image:
Cover on morphology sup-
©Tui De Roy/Minden Pictures/FLPA
educate public officials and judicial figures on today’s most pressing issues. Our goal is to promote 5.6%
Inset: George Richmond/Bridgeman Art Library, London (Superstock)
Climate regulation informed policy decisions that benefit society. And this is just one of the ways that AAAS is committed to
www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009 29
Human rights advancing science to support a healthy and prosperous world. Join
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 NEWSFOCUS
and proteins. Later, RNA-based life may have
Introduction On the Origin of
of evolved the ability to assemble amino acids into
proteins. It’s a small step, biochemically, for

Darwin’s Inspiration, Darwin’s Legacy Life on Earth

DNA to evolve from RNA.
In modern cells, RNA is remarkably versa-
tile. It can sense the levels of various com-
pounds inside a cell and switch genes on and
off to adjust these concentrations, for example.
The day has passed delightfully. Delight itself, however, is a weak term to express in some warm little pond, with all sorts of It can also join together amino acids, the build-
ammonia and phosphoric salts, light, heat, elec- ing blocks of proteins. Thus, the first cells
the feeling of a naturalist who, for the first time, has wandered by himself in a tricity, etc., present, that a protein compound might have tapped RNA for all the tasks on
Brazilian forest. The elegance of the grasses, the novelty of the parasitical plants, was chemically formed ready to undergo still which life depends.
the beauty of the flowers, the glossy green of the foliage, but above all the general more complex changes, at the present day such For 60 years, researchers have been honing
matter would be instantly devoured or theories about the sources of the amino acids
luxuriance of the vegetation, filled me with admiration. A most paradoxical mixture absorbed, which would not have been the case and RNA’s building blocks. Over time, they
of sound and silence pervades the shady parts of the wood. The noise from the before living creatures were formed.” have had to refine their ideas to take into
Scientists today who study the origin of life account an ever-clearer understanding of what
insects is so loud, that it may be heard even in a vessel anchored several hundred
do not share Darwin’s pessimism about our early Earth was like.
yards from the shore; yet within the recesses of the forest a universal silence appears ability to reconstruct those early moments. In an iconic experiment in 1953, Stanley
to reign. To a person fond of natural history, such a day as this brings with it a “Now is a good time to be doing this research, Miller, then at the University of Chicago,
because the prospects for success are greater ignited a spark that zapped through a chamber
deeper pleasure than he can ever hope to experience again. than they have ever been,” says John filled with ammonia, methane, and other
—Charles Darwin, The Voyage of the Beagle, Feb 29th [1832] Sutherland, a chemist at the University of Man- gases. The spark created a goo rich in amino
chester in the United Kingdom. He and others acids, and, based on his results, Miller sug-
are addressing each of the steps involved in the gested that lightning on the early Earth could

L
transition to life: where the raw materials came have created many compounds that would
ike many other scientists raised in temperate latitudes, Charles examines the extent to which biotic and abiotic factors have shaped from, how complex organic molecules such as later be assembled into living things.
Darwin was enthralled by his first glimpse of the tropical rain species diversity in the fossil record. Dolph Schluter reviews how RNA formed, and how the first cells arose. In By the 1990s, however, the accumulated
forest. His Beagle diary entry conveyed those immediate and research on speciation has shifted in focus from morphological AN AMAZON OF WORDS FLOWED FROM doing so, they are inching their way toward evidence indicated that the early Earth was
Charles Darwin’s pen. His books covered the making life from scratch. “When I was in grad- dominated by carbon dioxide, with a pinch of
thrilling first impressions, but the encounter with the Brazilian Atlan- evolution to reproductive isolation, tracing the links between Dar-
gamut from barnacles to orchids, from geol- uate school, people thought investigating the nitrogen—two gases not found in Miller’s
tic Forest had an enduring influence on the development of his ideas win’s ideas and current thinking. Christophe Fraser and colleagues
ogy to domestication. At the same time, he origin of life was something old scientists did at flask. When scientists tried to replicate Miller’s
over the following decades, with resounding echoes even today in discuss the contentious area of microbial species formation, an is-

CREDITS (TOP TO BOTTOM): KATHARINE SUTLIFF/SCIENCE; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)
filled notebooks with his ruminations and the end of their career, when they could sit in an experiments with carbon dioxide in the mix,
21st century evolutionary science. sue that would surely have vexed Darwin horribly had the bewil- scribbled thousands of letters packed with armchair and speculate,” says Henderson their sparks seemed to make almost no amino
dering diversity of microbes been known in his day. observations and speculations on nature. Yet James Cleaves of the Carnegie Institution for acids. The raw materials for life would have
The collection reprinted here is a sample of the articles published Darwin dedicated only a few words of his great Science in Washington, D.C. “Now making an had to come from elsewhere, they concluded.
in 2009 by Science magazine in celebration of the Darwin bicen- Finally, with a focus on conservation, a Report by Ana Carnaval et verbal flood to one of the biggest questions in artificial cell doesn’t sound like science fiction In 2008, however, lightning began to look
tenary. We start with four of the essays from our “On the Origin al., who model evolutionary processes in endemic tree-frog spe- all of biology: how life began. any more. It’s a reasonable pursuit.” promising once again. Cleaves and his col-
of” series, prepared by Science’s news writers; further essays in this cies in the Brazilian Atlantic Forest, the very biodiversity hotspot The only words he published in a book leagues suspected that the failed experiments
series are appearing monthly in Science throughout the year. A Per- that so inspired Darwin on his South American landfall, and that is appeared near the end of On the Origin of Raw ingredients were flawed because the sparks might have pro-
spective by Stephen Jackson then considers the legacy of Alexander now reduced to a collection of small fragments scattered along the Species: “Probably all the organic beings which Life—or at least life as we know it—appears to duced nitrogen compounds that destroyed any
have ever lived on this earth have descended have emerged on Earth only once. Just about all newly formed amino acids. When they added
von Humboldt, for whom, like Darwin, the South American tropics coast. Darwin returned to the Brazilian coast on his final homeward
from some one primordial form, into which life organisms use double-stranded DNA to encode buffering chemicals that could take up these
were a critical inspiration, and who died 150 years ago in the year leg, more than four years after his first landfall there. His enthusi-
was first breathed,” Darwin wrote. genetic information, for example. They copy nitrogen compounds, the experiments gener-
of the publication of Darwin’s Origin. (Humboldt’s Personal Nar- asm for the tropical forested landscape was undiminished. Darwin believed that life likely emerged their genes into RNA and then translate RNA ated hundreds of times more amino acids than
rative of his tropical explorations was acknowledged by Darwin as spontaneously from the chemicals into proteins. The genetic code scientists had previously found.
‘far exceed[ing] in merit anything I have read’ on the subject.) A In my last walk I stopped again and again to gaze on these beau- it is made of today, such as carbon, THE YEAR OF they use to translate DNA into pro- Cleaves suspects that lightning was only
book review by Lynn Nyhart explores two recent volumes on Ernst ties, and endeavoured to fix in my mind for ever, an impression nitrogen, and phosphorus. But he The English teins is identical, whether they are one of several ways in which organic com-
Haeckel’s work, his interpretations of Darwin and his contributions which at the time I knew sooner or later must fail … they will leave, did not publish these musings. DARWIN
naturalist had
emus or bread mold. The simplest pounds built up on Earth. Meteorites that fall to
to evolutionary thought. like a tale heard in childhood, a picture full of indistinct, but most The English naturalist had built explanation for this shared biology Earth contain amino acids and organic carbon
beautiful figures. his argument for evolution, in built his argu- is that all living things inherited it molecules such as formaldehyde. Hydro-
In the first of four Review articles reprinted here, Peter Bowler ana- —Charles Darwin, The Voyage of the Beagle, August 1836 large part, on the processes he from a common ancestor— thermal vents spew out other compounds that
could observe around him. He did
ment for evo- namely, DNA-based microbes that could have been incorporated into the first life
lyzes the originality of Darwin’s contribution to the understanding of
CREDIT: KATHARINE SUTLIFF/SCIENCE

the diversity and diversification of the living world. Michael Benton Andrew Sugden, Deputy Editor
not think it would be possible to lution, in large lived more than 3.5 billion years forms. Raw materials were not an issue, he
see life originating now because ago. That common ancestor was says: “The real hurdle is how you put together
part, on the
the life that’s already here would already fairly complex, and many organic compounds into a living system.”
prevent it from emerging. processes he scientists have wondered how it
In 1871, he outlined the prob- This could
essay isobserve
the first might have evolved from a simpler Step 1: Make RNA
lem in a letter to his friend, botanist in a monthly series, with predecessor. Some now argue that An RNA molecule is a chain of linked
Joseph Hooker: “But if (and Oh! roots around
more him.
on evolutionary
online at blogs.
. membrane-bound cells with only nucleotides. Each nucleotide in turn consists
what a big if!) we could conceive sciencemag.org/origins RNA inside predated both DNA of three parts: a base (which functions as a

2 198 9 JANUARY 2009 VOL 323 SCIENCE www.sciencemag.org 3

 EVOLUTIONARY ROOTS EVOLUTIONARY ROOTS
ORIGINS
On the Origin of
of
“letter” in a gene’s recipe), a sugar molecule, soup. “We’ve got the molecules in our RNA, producing the first protocells. “The goal “letter” in a gene’s recipe), a sugar molecule, soup. “We’ve got the molecules in our RNA, producingVenus, the firstphallus,
protocells. or“The
pebble? goal
and a cluster of phosphorus and oxygen sights,” he says. is to have something that can replicate by itself, and a cluster of phosphorus and oxygen sights,” he says. is to have something thatknow
“I don’t can replicate
much about by itself,
Art, but I know what
atoms, which link one sugar to the next. For Sutherland can’t say for sure where these using just chemistry,” says Szostak. atoms, which link one sugar to the next. For Sutherland can’t say for sure where these using just chemistry,” I like,” says Szostak.the humorist and art critic
quipped

Art and Symbolism

years, researchers have tried in vain to synthe- reactions took place on the early Earth, but he After 2 decades, he and his colleagues years, researchers have tried in vain to synthe- reactions took place on the early Earth, but he After 2 decades, Geletthe and hisback
Burgess colleagues
in 1906. For archaeo-
size RNA by producing sugars and bases, notes that they work well at the temperatures have come up with RNA molecules that can size RNA by producing sugars and bases, notes that they work well at the temperatures have come up with RNA
logists, molecules that
distinguishing art can
from nonart is still
joining them together, and then adding phos- and pH levels found in ponds. If those ponds build copies of other short RNA molecules. joining them together, and then adding phos- and pH levels found in ponds. If those ponds build copies of quite otherashort RNA Take
challenge. molecules.
the 6-centimeter-long
phates. “It just doesn’t work,” says Sutherland. dried up temporarily, They have been able to phates. “It just doesn’t work,” says Sutherland. dried up temporarily, piece They have been
of quartzite knownable toas the Venus of
This failure has led scientists to consider
two other hypotheses about how RNA came to
they would concentrate
the nucleotides, making
“Now making an mix RNA and fatty
acids together in such a
This failure has led scientists to consider they would concentrate
two other hypotheses about how RNA came to the nucleotides, communicate making
“Now making an
meaning, whether they be the rich trove
Tan-Tan. mix
acidsof
RNA
Found
together
in and
Morocco
stone intools
fattyin 1999 next to a
suchestimated
a to be
be. Cleaves and others think RNA-based life conditions for life even artificial cell doesn’t way that the RNA gets be. Cleaves and others think RNA-based life conditions for life wordseventhat makeartificial
up our
may have evolved from organisms that used a more favorable. cal sounds that convey emotion, or the dra- resembles
cell
languages, doesn’t
the musi- between way that
300,000
trapped
the RNA
and
in vesicles.
gets
500,000 years old, it
may have evolved from organisms that used a more favorable. trapped in vesicles. The a human figureThe with stubby arms
different genetic material—one no longer Were these Darwin’s sound like science vesicles are able to add different genetic material—one no longer Were these Darwin’s
matic paintings sound that, 30,000like science
years after their and legs. vesicles
Robert areBednarik,
able to addan independent
found in nature. Chemists have been able to warm little ponds? “It fatty acids to their found in nature. Chemists have been able to warm little ponds? “It caused the discoverers of the Chau- archaeologist
creation, fatty acids based to intheir
Caulf ield South,
use other compounds to build backbones for might just be that he fiction any more. It’s membranes and grow. use other compounds to build backbones for might just be vet thatCave fiction any more. It’s
he to break down in tears. Australia,membranes insists and
that grow.
an ancient human
nucleotides (Science, 17 November 2000, wasn’t too far off,” says In July 2008, Szostak nucleotides (Science, 17 November 2000, wasn’t too far off,” While says sites like Chauvet might be vivid deliberately In Julymodified
2008, Szostak the stone to
p. 1306). They’re now investigating whether Sutherland. a reasonable pursuit.” reported that he had p. 1306). They’re now investigating whether Sutherland. examples ofa what reasonable
some researchers pursuit.”
still make itreported look morethat likehe had
a person.
these humanmade genetic molecules, called figured out how proto- these humanmade genetic molecules, called consider a “creative explosion” that began If so, this figured
objetout d’art how proto-
is so old
PNA and TNA, could have emerged on their Step 2: The cell —HENDERSON JAMES CLEAVES, cells could “eat” and PNA and TNA, could have emerged on their Step 2: The cell when modern humans —HENDERSON colonized Europe JAMES CLEAVES, cellscreated
that it was couldnot “eat”
by ourand
own on the early Earth more easily than RNA. If life did start out with CARNEGIE INSTITUTION FOR SCIENCE bring in nucleotides to own on the early Earth more easily than RNA. If life did start out aboutwith40,000 years ago, an increasing
CARNEGIE INSTITUTIONnum-FOR SCIENCE bring inwhich
own species, nucleotides first to
According to this hypothesis, RNA evolved RNA alone, that RNA build the RNA. According to this hypothesis, RNA evolved RNA alone, that berRNAof prehistorians are tracing our sym- appears build the RNA.
in Africa nearly
later and replaced the earlier molecule. would need to make copies of itself without All living cells depend on complicated later and replaced the earlier molecule. would need to make copiesmuch
bolic roots of itself without
further All living cells
back in time—and 200,000depend yearsonago, complicated
but
But it could also be that RNA wasn’t put help from proteins. Online in Science this channels to draw nucleotides across their But it could also be that RNA wasn’t put help from proteins. in some Online
cases,intoScience
speciesthisancestralchannels
to Homo to draw by onenucleotides
of our ances- across their
together the way scientists have thought. “If week (www.sciencemag.org/cgi/content/ membranes, raising the question of how a together the way scientists have thought. “If week (www.sciencemag.org/cgi/content/
sapiens. Like modern humans themselves, membranes, raising tors, the perhapsquestion theof how a
you want to get from Boston to New York, abstract/1167856), Tracey Lincoln and Ger- primitive protocell membrane brought in these you want to get from Boston to New York, abstract/1167856), Traceybehavior
symbolic Lincolnseems and Ger- to have primitive
its originsprotocell membrane brought
large-brained H. in these
there is an obvious way to go. But if you can’t ald Joyce of the Scripps Research Institute in molecules. By experimenting with different there is an obvious way to go. But if you can’t ald Joyce of theinScripps Africa.Research
Recent Institute
excavations in have
molecules.
turnedBy experimenting
heidelbergensis, with different
get there that way, there are other ways you San Diego, California, have shown how that recipes for membranes, Szostak and his col- get there that way, there are other ways you San Diego, California, up elaboratehave shown how that
stone tools, beads,recipes for membranes,
and ochre thought by Szostak
someand his col-
could go,” says Sutherland. He and his col- might have been possible. They designed a leagues have come up with protocells leaky could go,” says Sutherland. He and his col- might have been possible.
dating backThey designed
100,000 or morea leagues
years ago, have come up with protocells
anthropologists to leaky

PROJECT; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)

leagues have been trying to build RNA from pair of RNA molecules that join together and enough to let nucleic acids slip inside, where leagues have been trying to build RNA from pair of RNA molecules although thatresearchers
join togetherare andstillenough
debatingto let nucleic
be theacids common slip inside, where
simple organic compounds, such as formalde- assemble loose nucleotides to match their they could be assembled into RNA, but not so simple organic compounds, such as formalde-
Since their discovery by Frenchassemble
spelunkers loosewhich
nucleotides
of these to fmatch their demonstrate
inds really they could be assembledancestor into RNA, but not so
of mod-
hyde, that existed on Earth before life began. partner. Once the replication is complete, old porous that the large RNA could slip out. hyde, that existedin on Earth
1994, thebefore life began.
magnificent lions, partner.
horses, Once
and the replication
symbolic is complete,But
expression. old there’s
porouswide-
that the large RNA could
ern humans and slip out.
They find they make better progress toward and new RNA molecules separate and join Their experiments also show that these They find they rhinos
make better progress
that seem toward
to leap andwalls
from the new RNA molecules
of spread separatethat
agreement andthejoinbuildingTheir blocksexperiments
Neandertals. also showThat that these
producing RNA if they combine the compo- with new partners to form new RNA. In 30 vesicles survive over a 100°C range. At high producing RNAChauvetif they combine
Cave inthesouthern
compo- France
with new havepartners to form newpreceded
of symbolism RNA. In 30 vesicles art.
full-blown survivewould over a 100°C
mean that range. At high
nents of sugars and the components of bases hours, Lincoln and Joyce found, a population temperatures, protocells take in nucleotides nents of sugars reigned
and the components
as the world’s of bases hours,paint-
oldest cave Lincoln and“When Joyce wefound, a population
talk about beads andtemperatures,
art, we are protocells take in nucleotides
art is an extremely
together instead of separately making com- of RNA molecules could grow 100 million quickly, and at lower temperatures, Szostak together insteadings.
of separately
Expertly making
composed com-
in redofochre
RNA and molecules could
actually growabout
talking 100 million quickly, and at ancient
material technologies lower temperatures,
part of the Homo Szostak
plete sugars and bases first. times bigger. found, they build RNA molecules faster. plete sugars andblack
bases charcoal,
first. the vivid drawings timesdemon-
bigger. for symbolic expression that certainly found, they
post-buildrepertoire.
RNA molecules “Ignoring faster.
the Symmetry in stone.
Over the past few years, they have docu- Lincoln and Joyce kept their RNA mole- He speculates that regular temperature Over the past few years,
strate they
that the have docu-
artistic Lincoln
gift stretches backanddate Joycethe kept their RNA
origins mole- thought
of symbolic He speculates
and fewthat regularwe
specimens temperature
have Some stone tools
mented almost an entire route from prebiotic cules in beakers. On the early Earth, however, cycles could have helped simple protocells sur- mented almost an moreentire
thanroute from years.
30,000 prebiotic
Thesecules in beakers.communication,
paintings On the early Earth, however,by acycles
potentially verycould
wide have ofhelped
very earlysimplepaleoart,
protocells sur- require a mental
molecules to RNA and are preparing to pub- replicating RNA might have been packed in the vive on the early Earth. They could draw in molecules to RNA and aresure
are almost preparing to pub- replicating
to be mentioned in any arti- RNAmargin,”
might have been
says packed in the Dietrich
archaeologist vive onStoutthe early Earth. They
explaining them couldaway, drawimagein to create.
lish even more details of their success. Dis- first cells. Jack Szostak and his colleagues at nucleotides when they were warm and then use lish even more cle details of their
or paper success.
about Dis- art.
the earliest first
Butcells.
whatJack ofSzostak and his
University colleagues
College London.at nucleotides when orthey were warm
rejecting them andout then use
covering these new reactions makes Suther- Harvard Medical School in Boston have been them to build RNA when the temperature covering these new reactions
do they reallymakes
tell usSuther-
about theHarvard
originsMedical
of School in Boston of
The evolution have been them
symbolism wastooncebuild RNA of hand when doesthe nottemperature
serve this discipline well,”
land suspect it wouldn’t have been that hard investigating how fatty acids and other mole- dropped. In Szostak’s protocells, nucleotides land suspect it wouldn’t have been that hard investigating how
artistic expression? fatty acids
thought to have andbeen
other asmole-
rapid as dropped.
“flicking In on Szostak’s
Bednarik protocells,
wrote in nucleotides
a 2003 analysis of the
for RNA to emerge directly from an organic cules on the early Earth might have trapped are arranged along a template of RNA. Strands for RNA to emergeThe directly from anhumans
prehistoric organicwhocules on the early
decorated Earth
a light mightashave
switch,” trapped Clive
archaeologist are arranged
Gamble along Venusa template
of Tan-Tan of RNA. StrandsAnthropology.
in Current
of RNA tend to stick together at low tempera- Chauvet’s walls by torchlight arrived at the of the Royal Holloway, University of RNA tend to stick
of Lon- Yettogether at low tempera- are skeptical,
many archaeologists

PROJECT
tures. When the protocell warmed up again, the cave with their artistic genius already in full don, put it some years ago. Buttures. given When
newthe protocell
arguing warmed that theup again, resemblance
stone’s the to a
heat might cause the two strands to pull apart, flower. And so, most researchers agree that evidence that symbolic behavior heatappears
might causehuman the two strands
figure might to pullbe apart,
coincidence. Indeed,

BOXGROVE
BOXGROVE
allowing the new RNA molecule to function. the origins of art cannot simply long before cave allowing paintings, the newthe RNAdebatemolecule
over the to Tan-Tan
function.“figurine” is rem-
Now Szostak is running experiments to be pegged to the latest discovery THE YEAR OF Gamble now says that his Now Szostak
much- is running
iniscent of aexperiments
similar controversy to over a
Recent cited comment needsbring to behis protocells closer to life. He is devel-

THE
bring his protocells closer to life. He is devel- of ancient paintings or sculp- mod- smaller stone discovered in 1981 at the site of
DARWIN

THE
ified: “It’s a dimmer oping switchnew now,forms of RNARam that mayin thebeIsraeli-occupied
able to

SUTLIFF/SCIENCE;
oping new forms of RNA that may be able to ture. Some of the earliest art excavations Berekhat Golan

SUTLIFF/SCIENCE;
replicate longer molecules faster. For him, likely perished over the ages; a stuttering candle.” replicate longerHeights. molecules Tofaster.
someFor him,
archaeologists, this
the true test of his experiments will be much remains to be found; and have turned As they more precisely the truepin- test of his experiments
250,000-year-old object will be
resembles a woman,
whether his protocells not only grow and archaeologists don’t always up elaborate point when symbolic whether
behavior his protocells
but othersnot argueonly thatgrowit wasand shaped by natural
reproduce, but evolve. agree on how to interpret what is
KATHARINE
RIGHT): KATHERINE
stone tools, began, scientists are reproduce,
hoping they but evolve.
forces, and, in any case, looks more like a
“To me, the origin of life and the origin of unearthed. As a result, instead of might one day crack the “To me, the penguin
tough- origin ofor life and the origin
a phallus. Even afterof an exhaustive
Darwinian evolution are essentially the same chasing after art’s first appear- beads, and est question of all: What Darwinian
was itsevolution are essentially
microscopic studytheconcluded
same that the
TOBOTTOM):

thing,” says Szostak. And if Darwin was alive ance, many researchers seek to ochre dating evolutionary advantage thing,” says toSzostak.
BerekhatAndRam if Darwin
objectwas hadalive
indeed been etched
CREDIT: JANET IWASA

today, he mightwith wellabe willing to write what a lot some consider

CREDIT: JANET IWASA

Protocell. Researchers at today, he might well be willing to write a lot understand its symbolic roots. back 100,000Protocell. humans? Didatsymbols,
Researchers as many tool to emphasize
After all, art is an aesthetic This essay continuesHarvard more about how life began.
(LEFTTO

Harvard are trying to make more about how life began. our researchers
are trying to makesuspect, serve as a its “head” and “arms,” many researchers have
expression of something more monthlyorseries. more
CREDITS (TOP

simple life forms, shown –CARL ZIMMER See more

simplesocial glue
life forms, that helped tribes of rejected it as a–CARL
shown work of ZIMMER
art. For some, proof of
on humans’ evolutionary
CREDITS

years here in aearly

computer image. to survive
fundamental: the cognitive abil- journey onlineago. humans and
here in a computer image. Carl Zimmer is the author of Microcosm: E. coli and the Carl Zimmer is the symbolic behaviorE.requires
author of Microcosm: coli and the evidence that the
at blogs.
New Science of Life. ity to construct symbols that sciencemag.org/origins. reproduce? New Science of Life.symbols had a commonly understood mean-

4 www.sciencemag.org SCIENCE VOL 323 9 JANUARY 2009 199 www.sciencemag.org SCIENCE VOL
www.sciencemag.org 323 9 JANUARY
SCIENCE VOL 323 2009
6 FEBRUARY 2009 199 5
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ORIGINS ORIGINS

tools, which Wynn and many others argue are Late Acheulean tools. Both methods turned ated with human burials. Some researchers
A roaring start. Researchers agree that Chauvet Cave’s clear examples of an imposed form based on a on visual and motor areas of the brain. But argue that this represents an early case of
magnificent paintings, including these lions, are full-blown art. mental template. Some have even argued that only Late Acheulean knapping turned on cir- “color symbolism,” citing the universal
these skillfully crafted hand axes had symbolic cuits also linked to language, the team importance of red in historical cultures
meanings, for example to display prestige or reported last year. worldwide and the apparently great lengths
even attract members of the opposite sex. to which early humans went to gather red
The half-million-year mark also heralded Color me red ochre. ”There is very strong circumstantial
the arrival of H. heidelbergensis, which had At Twin Rivers, it’s not just the tools that hint evidence for the very great antiquity of the
a much larger brain than H. erectus. Not at incipient symbolic behavior. Early humans color red as a symbolic category,” says
long afterward, our African ancestors began there also left behind at least 300 lumps of anthropologist Sally McBrearty of the
to create a wide variety of finely crafted ochre and other pigments in a rainbow of col- University of Connecticut, Storrs.
blades and projectile points, which allowed ors: yellow, red, pink, brown, purple, and These finds of colorful ochre, fancy
them to exploit their environment in more blue-black, some of which were gathered far tools, and beads have convinced many
sophisticated ways, and so presumably from the site. Excavator Lawrence Barham researchers that the building blocks of
enhance their survival and reproduction. of the University of Liverpool in the United symbolism had emerged by at least
Archaeologists refer to these tools as Middle Kingdom thinks they used the ochre to 100,000 years ago and possibly
Stone Age technology and agree that they paint their bodies, though there’s little much earlier. But why? What
did require mental templates. “The tools tell hard evidence for this. Most archaeolo- selective advantages did using
us that the hominid world was changing,” gists agree that body painting, as well symbols confer on our ancestors?

CREDITS (TOP TO BOTTOM): FRENCH MINISTRY OF CULTURE AND COMMUNICATION/DRAC RHONE-ALPES/DEPARTMENT OF ARCHAEOLOGY; CHRIS HENSHILWOOD AND FRANCESCO D’ERRICO
says Wynn. as the wearing of personal orna- To some scientists, the ques-
ing and were shared within groups of people. ity to hold an abstract concept in one’s head— As one moves forward in time, humans ments such as bead necklaces, tion is a no-brainer, especially
For example, the hundreds of bone and stone and, in the case of the tool, to “impose” a pre- appear able to imagine and create even more was a key way that early humans when it is focused on the most
“Venus figurines” found at sites across Eura- determined form on raw material based on an elaborate tools, sharpening their evolution- symbolically communicated sophisticated form of symbolic
sia beginning about 30,000 years ago were abstract mental template. That kind of ability ary edge in the battle for survival. By social identity such as member- communication: language. The
skillfully carved and follow a common motif. was probably not needed to make the earliest 260,000 years ago, for example, ancient ship in a particular group, much ability to communicate detailed,
They are widely regarded not only as sym- known tools, say Wynn and other researchers. humans at Twin Rivers in what is now Zambia as people today declare social concrete information as well as
bolic expression, but full-fledged art. These implements, which date back 2.6 mil- could envision a complex finished tool and allegiances and individual person- abstract concepts allowed early
Thus many researchers are reluctant to lion years, consist mostly of rocks that have put it together in steps from different compo- alities by their clothing and jewelry. humans to cooperate and plan for the
accept rare, one-off discoveries like the Tan- been split in two and then sharpened to make nents. They left behind finely made blades Yet while the Twin Rivers evidence is future in ways unique to our species,
Tan or Berekhat Ram objects as signs of simple chopping and scraping implements. and other tools that had been modified— suggestive, it’s hard to be sure how the ochre thus enhancing their survival during
symbolic behavior. “You can imagine [an Then, about 1.7 million years ago, large, usually by blunting or “backing” one edge— was actually used. There’s little sign that it was rough times and boosting their repro-
ancient human] recognizing a resemblance teardrop-shaped tools called Acheulean hand to be hafted onto handles, presumably made ground into powder, as needed for decoration, ductive success in good times. “What
but [the object] still hav[ing] no symbolic axes appeared in Africa. Likely created by of wood. These so-called backed tools have says Ian Watts, an independent ochre expert in aspects of human social organization and
meaning at all,” says Philip Chase, an anthro- H. erectus and probably used to cut plants and been widely regarded as evidence of sym- Athens. And even ground ochre could have adaptation wouldn’t benefit from the evolu-
pologist at the University of Pennsylvania. butcher animals, these hand-held tools vary bolic behavior when found at much younger had utilitarian uses, says archaeologist Lyn tion of language?” asked Terrence Deacon, a
Thomas Wynn, an anthropologist at the greatly in shape, and archaeologists have sites. “This flexibility in stone tool manufac- Wadley of the University of Witwatersrand biological anthropologist at the University
University of Colorado, Colorado Springs, debated whether creating the earliest ones ture [indicates] symbolic capabilities,” says in Johannesburg, South Africa. Modern-day of California, Berkeley, in his influential
agrees: “If it’s a one-off, I don’t think it required an abstract mental template. But by archaeologist Sarah Wurz of the Iziko Muse- experiments have shown that ground ochre book The Symbolic Species: The Coevolu-
counts. It’s not sending a message to anyone.” about 500,000 years ago, ancient humans were ums of Cape Town in South Africa. can be used to tan animal hides, help stone tion of Language and the Brain. Deacon
creating more symmetrical Late Acheulean Similar cognitive abilities were possibly tools adhere to bone or wooden handles, and Eye of the beholder. Archaeologists debate whether went on to list just some of the advantages:
Tools of the imagination required to make the famous even protect skin against mosquito bites. this modified stone was meant to represent a woman. organizing hunts, sharing food, teaching
Given how difficult it is to detect 400,000-year-old wooden spears “We simply don’t know how ancient peo- toolmaking, sharing past experiences, and
the earliest symbolic messages in “If it’s a one-off, I don’t think from Schöningen, Germany. One ple used ochre 300,000 years ago,” Wadley consider diagnostic elements of symbolic raising children. Indeed, many researchers
the archaeological record, some recent study concludes that these says. And since at that date the ochre users behavior came together. And in work now have argued that symbolic communication is
researchers look instead for proxy
it counts. It’s not sending a spears’ creators—probably mem- were not modern humans but our archaic in press, the Blombos team reports finding what held groups of early humans together
behaviors that might have
required similar cognitive abili-
message to anyone.” bers of H. heidelbergensis—car-
ried out at least eight preplanned
ancestors, some experts are leery of assign- engraved ochre in levels dating back to
ing them symbolic savvy. 100,000 years ago (Science,
as they explored new environments and
endured climatic shifts.
ties, such as toolmaking. Charles
Darwin himself saw an evolu-
—THOMAS WYNN, UNIVERSITY OF COLORADO,
COLORADO SPRINGS
steps spanning several days,
including chopping tree branches
Yet many archaeologists are
willing to grant that our species, Online 30 January, p. 569).
There are other hints that the
As for art and other nonlinguistic forms
of symbolic behavior, they may also have
tionary parallel between tool- with hand axes and shaping the H. sapiens, was creating and sciencemag.org modern humans who ventured been key to cementing these bonds, by

CREDIT: FRANCESCO D’ERRICO AND APRIL NOWELL

making and language, probably spears with stone flakes. using certain kinds of symbols Hear author out of Africa around this time expressing meanings that are difficult or
Michael Balter
the most sophisticated form of The idea that sophisticated by 75,000 years ago and per- discuss the roots of art at might also have engaged in sym- impossible to put into words. In that way,
symbolic behavior. “To chip a toolmaking and symbolic haps much earlier. At sites such www.sciencemag.org/ bolic behavior. At the Skhul rock artistic expression, including music, may
flint into the rudest tool,” Darwin thought require similar cognitive as Blombos Cave on South darwin. shelter in Israel, humans left have helped ensure the survival of the
wrote in The Descent of Man, skills also gets some support Africa’s southern Cape, people 100,000-year-old shell beads fittest. This may also explain why great art
demands a “perfect hand” as well from a surprising quarter: brain- left sophisticated tools, including elabo- considered by some to be personal orna- has such emotional force, because the most
adapted to that task as the “vocal imaging studies. Stout’s team ran rately crafted bone points, as well as perfo- ments (Science, 23 June 2006, p. 1731). At effective symbols are those that convey
organs” are to speaking. positron emission tomography rated beads made from snail shells and the 92,000-year-old Qafzeh Cave site their messages the most powerfully—
To many researchers, making scans on three archaeologists— pieces of red ochre engraved with what nearby, modern humans apparently strongly something the artists at Chauvet Cave seem
sophisticated tools and using Symbolic start. Some scientists argue that this 77,000-year-old engraved ochre all skillful stone knappers—as appear to be abstract designs. At this single preferred the color red: Excavators have to have understood very well.
symbols both require the capac- shows symbolic capacity. they made pre-Acheulean and site, a number of what many archaeologists studied 71 pieces of bright red ochre associ- –MICHAEL BALTER

6 7
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 ORIGINS
On the Origin of
of live in habitats such as scalding hot springs,
don’t generate oxygen. Their photosynthetic
proteins huddle in relatively simple “reaction
Allen (no relation to John Allen)
and JoAnn Williams of Arizona
State University, Tempe, and col-
Catching rays. Long before plants got
in on the act, photosynthetic cyano-
bacteria living in pools like this one in

Photosynthesis centers” that may have been the predecessors leagues are working out how a Yellowstone National Park were chang-
of the two photosystems. bacterial reaction center could ing the composition of the atmosphere.
Envisioning the steps that led to this have evolved photosystem II’s
complex biochemistry is mind-boggling. appetite for electrons. says astrobiologist Roger Buick
Similarities between proteins in photo- Taking a hands-on approach, of the University of Washington,
piece together how and when organisms first synthetic and nonphotosynthetic bacteria they have been tinkering with the Seattle. These hints could push
began to harness light’s energy. Although suggest that early microbes co-opted some reaction center of the purple bac- the origin back 600 million
most modern photosynthesizers make oxygen photosynthesis genes from other metabolic terium Rhodobacter sphaeroides years or more.
from water, the earliest solar-powered bacteria pathways. But protophotosynthesizers to determine if they can make One line of evidence is oil
relied on different ingredients, perhaps hydro- might also have helped each other piece it more like photosystem II. biomarkers that researchers
gen sulfide. Over time, the photosynthetic these pathways together by swapping First they targeted bacterio- think are the remains of cyano-
machinery became more sophisticated, even- genes. Biochemist Robert Blankenship of chlorophyll, the bacterial version bacteria. They’ve turned up in
tually leading to the green, well-oxygenated Washington University in St. Louis, Mis- of chlorophyll that’s at the core rocks that are up to 2.7 billion
world that surrounds us today. In the lab, some souri, and colleagues say they’ve uncovered of the reaction center, and years old. And in western Aus-
biochemists are recapitulating the chemical traces of these lateral gene transfers by altered the number of hydrogen tralia, thick shale deposits that
steps that led to this increased complexity. comparing complete bacterial genomes. bonds. Adding hydrogen bonds are 3.2 billion years old hold
Other researchers are locked in debates over For example, their 2002 study of more than hiked the molecule’s greed for rich bacterial remains but no
just when this transition happened, 2.4 billion 60 photosynthetic and nonphotosynthetic electrons, they found. traces of sulfur or other possible
years ago or much earlier. bacteria (Science, 22 November 2002, The water-cleaving portion electron sources, suggesting that
Looking so far into the past is difficult. p. 1616) suggested that bugs had passed of photosystem II sports four the microbes were using water
The geological record for that time is around several photosynthesis genes, manganese atoms that become to make energy.
skimpy and tricky to interpret. Eons of evo- including some involved in synthesizing the oxidized, or lose electrons. So Geologist Euan Nisbet of
lution have blurred the molecular vestiges bacterial version of chlorophyll. the team equipped the bacterial Royal Holloway, University of
of the early events that remain in living Gene-sharing might also explain the puz- reaction center with one atom London, and colleagues found
organisms. But “it’s a terribly important zling distribution of the photosystems, of the metal. In this modif ied additional support for an early
problem,” says biochemist Carl Bauer of Blankenship says. A cell needs both photo- version, the added manganese origin when they went search-
Indiana University, Bloomington, one well systems to carry out oxygenic photosynthesis. also underwent oxidation, the ing for traces of RuBisCO, a
Try to picture the world without photo- worth the travails. Yet modern nonoxygenic bacteria have the researchers reported in 2005. key photosynthetic enzyme.
synthesis. Obviously, you’d have to strip presumptive predecessor either of photo- James Allen says that their cre- RuBisCO feeds carbon dioxide
away the greenery—not just the redwoods To catch a photon system I or of photosystem II, never both. To ations aren’t powerful enough to into the reactions that yield sug-
and sunflowers, but also the humble algae Over more than 200 years, researchers have explain how the two protein complexes split water. But eventually, they ars. The enzyme version found
and the light-capturing bacteria that nourish ironed out most of the molecular details of wound up together, Blankenship favors “a
many of the world’s ecosystems. Gone, too, how organisms turn carbon dioxide and large-scale lateral [gene] transfer” or even a
hope to engineer a reaction center
that can oxidize less possessive
Oxygenic photosynthesis “was the in oxygenic photosynthesizers
plays favorites: It prefers carbon
would be everything that depends on photo-
synthetic organisms, directly or indirectly,
water into food. Chlorophyll pigment and
about 100 other proteins team up to put light
fusion of organisms carrying each photo-
system. However, other researchers remain
molecules, such as hydrogen
peroxide, that would have been
last of the great inventions of micro- dioxide that contains the carbon-
12 isotope over the bulkier car-
for sustenance—from leaf-munching bee-
tles to meat-eating lions. Even corals, which
to work. Plants, some protists, and cyano-
bacteria embed their chlorophyll in two
skeptical, arguing that one photosystem
evolved from the other, possibly through the
present on the early Earth. Even bial metabolism, and it changed the bon-13. In 2007, Nisbet and
if the researchers never replicate his colleagues found dispropor-
play host to algal partners, would lose their large protein clusters, photosystem I and duplication of genes, creating an ancient cell photosystem II, “if we def ine planetary environment forever.” tionately low carbon-13 values
main food source. photosystem II. And they need both systems with both. No one knows for sure. the intermediate stages, we’ve indicative of RuBisCO activity
Photosynthesis makes Earth congenial for to use water as an electron source. Light accomplished a lot,” he says. —Paul Falkowski, Rutgers University when they analyzed organic
life in other ways, too. Early photosynthesizers jump-starts an electrical circuit in which The electron thief matter in rocks from three sites
pumped up atmospheric oxygen concentra- electrons flow from the photosystems Either way, it took some fancy fiddling to Something in the air about 2.4 billion years ago, geologists see in Zimbabwe and Canada that are between
tions, making way for complex multicellular through protein chains that convert the primitive reaction How the photosystems got their start is cru- the first unmistakable signs of significant, 2.7 billion and 2.9 billion years old. Nisbet
life, including us. And water-dwellers were make the energy-rich molecules THE YEAR OF centers to oxygen-generating cial for understanding the origin of photo- sustained levels of atmospheric oxygen. concludes that oxygen-making photo-
able to colonize the land only because the ATP and NADPH. These mole- Given its photosystems. Oxygenic photo- synthesis. But the question that’s drawn the These signs include red beds, or layers synthesis began at least 2.9 billion years ago.
oxygen helped create the ozone layer that
shields against the sun’s ultraviolet radiation.
cules then power the synthesis
of the sugars that organisms
DARWIN
importance in synthesis was a huge upgrade,
leading to a land of plenty, says
most attention—and provoked the most tinged by oxidized iron, i.e., rust. Further The early-origin case isn’t ironclad. For
making and wrangling—is when photosynthesis began. support that the GOE marks an atmospheric example, a 2008 paper that has some
Oxygen-producing, or oxygenic, photo- depend on to grow and multiply. biochemist John Allen of Queen Most researchers accept that nonoxygenic revolution comes from a technique that researchers fuming claims that the oil bio-
synthesis “was the last of the great inventions Photosystem II—the strongest keeping earth Mary, University of London. photosynthesis arose first, probably shortly detects skewed abundances of sulfur iso- markers are contaminants that seeped in
of microbial metabolism, and it changed the naturally occurring oxidant— lush, photo- “Water is everywhere, so the CREDIT: NEALE CLARK/GETTY IMAGES
after life originated more than 3.8 billion topes that occur if the air lacks oxygen. from younger rocks. Advocates also have to
planetary environment forever,” says geo- regains its lost electrons by organisms never ran out of elec- years ago. “Life needs an energy source, and These imbalances persisted until the GOE, explain why it took hundreds of millions of
biologist Paul Falkowski of Rutgers Univer- swiping them from water, gener- synthesis ranks trons. They were unstoppable.” the sun is the only ubiquitous and reliable when they vanished. years for oxygen to build up in the air.
CREDIT: K. SUTLIFF/SCIENCE

sity in New Brunswick, New Jersey. ating oxygen as a waste product. high on the But water clings to its elec- energy source,” says Blankenship. Hard-liners construe these data to mean Although the last word on the origins of
Given its importance in making and keep- However, some bacteria trons. With its oxidizing power, The sharpest disputes revolve around that oxygenic photosynthesis could not have oxygen-making photosynthesis isn’t in,
ing Earth lush, photosynthesis ranks high on
top- 10 list of
don’t rely on water as an elec- This essay is the third photosystem II can wrench them when organisms shifted to oxygenic photo- emerged until shortly before the GOE. But researchers say they are making progress. One
the top-10 list of evolutionary milestones. By tron source, using hydrogen sul- in aevolutionary
monthly series. More away, but the reaction centers in synthesis. At issue is how to interpret a other scientists disagree. “We are finding thing is for certain, however: Without this
on evolution online at
delving into ancient rocks and poring over fide or other alternatives. These blogs.sciencemag.org/
milestones. nonoxygenic photosynthesizers watershed in the fossil record known as the more and more hints that oxygenic photo- innovation, Earth would look a lot like Mars.
DNA sequences, researchers are now trying to nonconformists, which today origins. cannot. Biochemists James great oxidation event (GOE). In rocks from synthesis goes deeper into the fossil record,” –MITCH LESLIE

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 NEWSFOCUS ORIGINS
embryo that serves as its food supply. Stockholm. “When we started,
On the Origin of
of Darwin was perplexed by the diversity of
flowering plants; they were too numerous
the search profile was bigger,
a magnolia [flower],” she

Flowering Plants
and too varied, and there were too few fos- recalls. But 30 years ago, she
sils to sort out which were more primitive. and others discovered tiny
Throughout much of the 20th century, mag- ancient flowers by sieving
nolia relatives with relatively large flowers through sand and clay sedi-
were leading candidates for the most primi- ments. With this technique,
how flowers got started—and from which tive living flowers, although a few they have now collected hun-
ancestor. Today, researchers have analytical researchers looked to small herbs instead. dreds of millimeter-size
tools, fossils, genomic data, and insights that In the late 1990s, molecular systematics flowers, some preserved in

GARDENS, KEW; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)

Darwin could never have imagined, all of came to the rescue, with several reports pre- three dimensions, from Por-
which make these mysteries less abom- senting a fairly consistent picture of the tugal and other locations with
inable. Over the past 40 years, techniques lower branches of the angiosperm tree. An Cretaceous deposits 70 mil-
for assessing the relationships between obscure shrub found only in New Caledonia lion to 120 million years old.
organisms have greatly improved, and gene emerged as a crucial window to the past. This fossil diversity
sequences, as well as morphology, now help Amborella trichopoda, with its 6-millimeter shows that angiosperms were
researchers sort out which angiosperms greenish-yellow flowers, lives deep in the thriving, with several groups
arose early and which arose late. New fossil cloud forests there. In multiple gene-based well-established, by 100 mil- Out of the past.
finds and new ways to study them—with assessments, including an analysis in 2007 lion years ago. In some, the Tiny Amborella sits
synchrotron radiation, for example—pro- of 81 genes from chloroplast genomes flower parts are whorled like at the bottom of the
vide a clearer view of the detailed anatomy belonging to 64 species, Amborella sits those of modern flowers; in angiosperm family tree.
of ancient plants. And researchers from var- at the base of the angiosperm family tree, others they are spiraled, con-
ious fields are figuring out genomic changes the sister group of all the rest of the sidered by some researchers
that might explain the amazing success of angiosperms. as the more primitive arrangement. Some from one of the nonflowering seed plants
“We are realizing that this

CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE, UC SANTA CRUZ; PHOTO BY JENNIFER SVITKO, COURTESY OF WILLIAM L. CREPET, CORNELL UNIVERSITY
this fast-evolving group. Given that placement, Amborella’s tiny flower fossils have prescribed numbers of or gymnosperms, whose heyday was 200
These approaches have given researchers flowers may hint at what early blossoms petals, another modern feature, whereas in million years ago. Modern gymnosperms
a much better sense of what early flowers were like. It’s one of “the most similar living others the petal count varies.
huge diversity is probably include conifers, ginkgoes, and the cycads,
were like and the relationships among them. flower[s]” to the world’s first flower, says
IN 1879, CHARLES DARWIN PENNED A LETTER
to British botanist Joseph Dalton Hooker, But one of Darwin’s mysteries remains: the James Doyle of the University of Califor-
In 1998, Chinese geologist Ge Sun of
Jilin University in Changchun, China, came
the result of one innova- with their stout trunks and large fronds.
Before angiosperms came along, these
lamenting an “abominable mystery” that nature and identity of the angiosperm ances- nia, Davis. The petals and sepals of its sin- across what seemed to be a much older tion piled on top of plants were much more diverse and

ROYAL BOTANIC
threw a wrench into his theory of evolution: tor itself. When flowering plants show up in gle-sex flowers are indistinguishable and flower. The fossil, called Archaefructus, was included cycadlike species, such as the

KEW
How did flowering plants diversify and the fossil record, they appear with a bang, vary in number; so too do the numbers of an aquatic plant that looked to be 144 mil- another innovation.” extinct Bennettitales, and many woody

GARDENS,
spread so rapidly across the globe? From with no obvious series of intermediates, as seed-producing carpels on female flowers lion years old. By 2002, Sun and David plants called Gnetales, of which
rice paddies to orange groves, alpine mead- Darwin noted. Researchers still don’t know and pollen-generating stamens on male —Peter Crane, a few representatives, including the

TRUSTEES,
Dilcher of the Florida Museum of Natural

BOTANIC
ows to formal gardens, prairies to oak- which seed- and pollen-bearing flowers. The organs are spirally History (FLMNH) in Gainesville had University of Chicago joint firs, survive today (see family tree,
hickory forests, the 300,000 species of organs eventually evolved into THE YEAR OF arranged, and carpels, rather described an entire plant, from roots to flow- p. 31). Also common in the Jurassic were

OF
ROYAL
angiosperms alive today shape most terres- the comparable flower parts. than being closed by fused tis-
DARWIN ers, entombed on a slab of rock unearthed in These fossils often spark debate because seed ferns, a group now long gone; their

THE BOARD
trial landscapes and much of human life “We’re a bit mystif ied,” says For more on sue as in roses and almost all Liaoning in northeastern China. specimens tend to be imperfectly preserved most famous member is Caytonia, which

TRUSTEES,
and culture. Their blooms color and scent botanist Michael Donoghue of flower origins, familiar flowers, are sealed by a In one sense, Archaefructus wasn’t much and leave room for interpretation. To help seems to have precarpel-like structures.

BOARD OFAND
our world; their fruits, roots, and seeds feed Yale University. “It doesn’t secretion. to look at. “It’s a flowering plant before remedy that, Friis and her colleagues have These g roups’ perceived relevance to
us; and their biomass provides clothing, appear that we can locate a close listen to a Most genetic analyses showed

THE DIRECTOR
there were flowers,” Dilcher notes. It lacked begun to examine flowers using synchro- flower evolution and their relationships to
building materials, and fuel. And yet this relative of the flowering plants.” podcast by that water lilies were the next petals and sepals, but it did have an tron radiation to generate a 3D image of angiosperms have ping-ponged between
takeover, which took place about 100 mil- branch up the angiosperm tree, enclosed carpel. When Kevin Nixon and their inner structures, allowing the fossil to camps, depending on how the evolutionary

OF THE
lion years ago, apparently happened in a Seeking the first flower author Elizabeth followed by a group represented colleagues at Cornell University compared remain intact while Friis peers inside it trees were constructed.

DIRECTOR AND
blink of geological time, just a few tens of One of two major living groups by star anise, which also has a its traits with those same traits in 173 living from many angles (Science, 7 December In the mid-1980s, Peter Crane, now at
THEPERMISSION
Pennisi at
millions of years. of seed plants, angiosperms have primitive look about it, says plants, Archaefructus came out as a sister to 2007, p. 1546). “We can get fantastic reso- the University of Chicago in Illinois, pro-
The father of evolution couldn’t quite “covered” seeds that develop This essay www.
is the fourth Doyle, “though each of these living angiosperms and closer to the com- lution,” says Friis. “It’s really exciting.” But posed a solution, the anthophyte hypothesis.
encased in a protective tissue in a monthly series.
KIND

fathom it. Darwin had an “abhorrence that has deviations from the ances- mon ancestor than even Amborella. so far, the flowers Friis finds are Using several lines of evidence and noting
sciencemag.
For more on evolutionary
OF

evolution could be both rapid and poten- called a carpel (picture a bean topics tral type.” Archaefructus’s distinction was short- too diverse to trace back to a that both Bennettitales and
WITH THE

online, see the

KIND PERMISSION

tially even saltational,” writes William pod). That’s in contrast to the Origins blog org/ at lived, however. Within months, better dat- particular ancestor. “From Gnetales organize their male
Friedman in the January American Journal nonflowering gymnosperms, blogs.sciencemag.org/ Fossil records ing of the sediments in which it was found these fossils, we cannot and female organs together
REPRODUCED

origins. For more on

multimedia/
of Botany, which is devoted to this such as conifers, which bear flower origins, listen Although some fossil pollen yielded younger dates, putting this f irst say what is the basic in what could be con-
“abominable mystery.” Throughout his life, naked seeds on scales. An to a podcast by author
podcast. dates back 135 million years, no flower squarely with other early fossil form,” she says. strued as a preflower,
Elizabeth Pennisi at
WITH THE

Darwin pestered botanists for their angiosperm’s carpel sits at the www.sciencemag.org/ credible earlier fossil evidence flower parts, about 125 million years old. he considered them,
(TOP TO BOTTOM):

thoughts on the matter, but they couldn’t center of the flower, typically multimedia/podcast. exists. In Darwin’s day, and for Also, a 2009 phylogenetic analysis of Before flowers along with angiosperms,
give him much help. surrounded by pollen-laden sta- many decades afterward, pale-
CREDITSREPRODUCED

67 taxa by Doyle and Peter Endress of the Although they have yet as comprising a single
Now, 130 years later, evolutionary biol- mens. In most flowers, the carpel and stamens obotanists primarily found leaves or pollen University of Zurich, Switzerland, placed to find the oldest fossil Larger than life. Although merely angiosperm entity called
ogists are still pestering botanists for clues are surrounded by petals and an outer row of but almost no fossil flowers. They had the the fossil in with water lilies rather than at flowers, researchers 2.2 millimeters in diameter, this 3D anthophytes. For the next
about what has made this plant group so leaflike sepals. Seeds have a double coating wrong search image, says Else Marie Friis of the base of the angiosperms, although this assume that the ances- decade, most family trees
CREDIT:

fossil flower shows that grasses date

successful, as well as when, where, and as well as endosperm, tissue surrounding the the Swedish Museum of Natural History in conclusion is contested. tral angiosperm evolved back to 94 million years ago. based on morphology sup-
10 11
28 3 APRIL 2009 VOL 324 SCIENCE www.sciencemag.org www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009 29
ORIGINS ORIGINS

such a causal relationship is not set-

tled. Later, animals that ate fruit and SEED PLANT Paleozoic seed ferns
dispersed seeds likely helped evolv-
ing species expand quickly into new
PHYLOGENY
territory. Some think the answer lies Asterids »
Eudicots
in genes: duplications that gave the
angiosperm genome opportunities to
Rosids
try out new floral shapes, new chem-
ical attractants, and so forth. This
flexibility enabled angiosperms to Monocots
exploit new niches and set them up

Angiosperms
for long-term evolutionary success.
“My own view is that in the past, we
Magnolias »
have looked for one feature,” says
Crane. Now, “we are realizing that Water lilies
this huge diversity is probably the
result of one innovation piled on top
?
of another innovation.” Archaefructus »
The latest insights into diversifica-
tion come from gene studies. From
2001 to 2006, Pamela Soltis of the Amborella
FLMNH and Claude dePamphilis
of Pennsylvania State University, ?
Caytonia
University Park, participated in
fuel. Darwin
Flowers, food, fuel. Darwin marveled
marveled at
at the
the diversity
diversityofofangiosperms.
angiosperms.Given mainstays
Given that of both our
they represent welfare
nine in 10and
landsense of beauty.
plants, Clockwisethat
it’s no surprise fromthey
left:serve
aspens,
as the Floral Genome Project, which ?
that they represent
mainstays ninewelfare
of both our in 10 land
and plants,
sense ofit’sbeauty.
no surprise that they
Clockwise fromserve as aspens,
top left: orchids,orchids,
grasses,grasses,
sunflowers, tulips, apples,
sunflowers, tulips,walnuts.
apples, walnuts. searched for genes in 15 angiosperms. Bennettitales
Now as a follow-up, the Ancestral
ported this idea. Crane and others carefully work points you in another direction,” out. Today, almost nine in 10 land plants Angiosperm Genome Project looks
dissected and described fossils of these Crane says. are angiosperms. at gene activity in five early angio- Cycads
groups, looking for the precursors to And if the molecular work is correct, The exact timing of the angiosperms’ sperms and a cycad, a gymnosperm.

gymnosperms
carpels, the seed’s double coat, and other then the field doesn’t know in which direc- explosion and expansion is under debate, as is DePamphilis and his colleagues
distinctive angiosperm traits. tion to turn, because in most analyses the matched all the genes in each Ginkgoes »
the cause. At least one estimate based on the

Living
But they have run into problems. “We do genetic data don’t place any living plant rate at which gene sequences change—that species against one another to deter-
not really know how to compare them close to angiosperms. The angiosperms is, the ticking of the molecular clock— mine the number of duplicates. They ? Gnetales
because the structures are very different- group together, the living gymnosperms pushes angiosperm evolution back to 215 then looked at the number of differ-
looking; figuring out what’s homologous is group together, and there’s nothing in million years ago. “There appears to be a ences in the sequences of each gene
quite a difficult thing,” says Crane. He and between. “The nonangiosperm ancestor just gap in the fossil record,” says Donoghue, pair to get a sense of how long ago Conifers »
his colleagues argue, for example, that the isn’t there,” says paleobotanist William who also notes that molecular dating meth- the duplication occurred. In most Extinct taxa
seeds in the Bennettitales have two cover- Crepet of Cornell. “I’m starting to worry ods “are still in their infancy” and, thus, early angiosperms, including water
ings, which may be a link to angiosperms. that we will never know, that it transformed could be misleading. He and others think lilies and magnolias, they saw many Shifting branches. As this simplified family tree shows, gene studies have helped clarify the relationships of many
But in the January American Journal of without intermediates.” that flowering plants lingered in obscurity simultaneous duplications—but not living angiosperms, but fitting in extinct species is still a challenge, and some nodes are hotly debated.
Botany, Gar Rothwell of Ohio University, for tens of millions of years before radiating in Amborella, they reported in the

CREDITS: (ARCHAEFRUCTUS IMAGE) DAVID DILCHER; (ALL OTHER IMAGES) PHOTOS.COM

Athens, and two colleagues disagree, say- Seeds of success toward their current diversity. January 2009 American Journal of Botany, The Floral Genome Project also looked are not as well-defined as they are in Ara-
ing that what Crane calls the outer layer is The angiosperm’s ancestor may be missing, Whatever the timing, there was some- confirming earlier reports. The data suggest to see whether the genetic programs guiding bidopsis. This sloppiness may have made
the only layer, and f ind but what is very clear—and was quite thing special about the angiosperm radia- that a key genome duplication happened flower development were consistent development flexible enough to undergo
fault with the hypothesis annoying to Darwin—is that the angio- tion. During the 1980s and again in 1997, after the lineage leading to Amborella split throughout the angiosperms. “We found that many small changes in expression patterns
in general. sperm prototype so readily proved a Cornell’s Karl Niklas compiled a database off but before water lilies evolved. “We’re there are fundamental aspects that are con- and functions that helped yield the great
To make matters winner. Seed ferns and showing the first and last occurrences of
FRIIS
MARIE FRIIS
beginning to get the idea that polyploidiza- served in the earliest lineages,” says Soltis. diversity in floral forms.
worse for anthophyte other gymnosperms fossil plants. When he and Crepet used that tion may have been a driving force in creat- “But there are differences in how the genes In his letter to Hooker, Darwin wrote
ELSE MARIE

proponents, gene- arose about 370 and more recent information to look at ing many new genes that drive floral devel- are deployed.” that he would like “to see this whole prob-
based evolutionary million years ago species’ appearances and disappearances, opment,” dePamphilis says. Take the avocado, a species on the lower lem solved.” A decade ago, Crepet thought
PHOTOS.COM; ELSE

trees break up this and dominated the they found that new angiosperms appeared Others have noted that a duplication branches of the angiosperm tree. In most Darwin would have gotten his wish by now.
BOTTOM): PHOTOS.COM;

grouping, pulling the planet for 250 mil- in bursts through time, whereas other plants, occurred in the evolution of grasses, and the angiosperms, the flower parts are arranged in That hasn’t happened, but Crepet is opti-
Gnetales off any lion years. Then in a such as gymnosperms, radiated rapidly only Floral Genome Project confirms that yet concentric circles, or whorls, around the mistic that he and his colleagues are on the
angiosperm branch few tens of millions at first. Moreover, angiosperms proved less another duplication paved the way for eudi- carpels, with stamens innermost, then petals, right track, as analyses of various kinds of
TO BOTTOM):

and placing them of years, angio- likely to disappear, somehow resisting cots, the group that includes apples, roses, and finally sepals. Each tissue has its own data become more sophisticated. “We are
among or next to the sperms edged them extinction, says Crepet. beans, tomatoes, and sunflowers. “There are distinct pattern of gene expression, but not less likely to go around in circles in the next
other gymnosperms. Once the angiosperms arrived, how did some real ‘hot spots’ in angiosperm evolu- in the avocado. Genes that in Arabidopsis 10 years,” he says. “I believe a solution to
(TOP TO
CREDITS (TOP

“The molecular work Inside and out. Synchrotron radiation helped pro- they diversify and spread so quickly? Darwin tionary history,” says dePamphilis, who is are active only in, say, the developing petals the problem is within reach. … The mystery
working to fully sequence the genome of spill over in avocado to the sepals. Thus in is solvable.”
CREDITS

points in one direc- duce a 3D rendering (gold) of this fossil male flower suspected that coevolution with insect polli-
tion; the paleobotanical (right) and insights into its internal structure. nators helped drive diversification, though Amborella with his colleagues. the more primitive plants, petals and sepals –ELIZABETH PENNISI

12
30 3 APRIL 2009 VOL 324 SCIENCE www.sciencemag.org www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009 13
31
TIVES
PERSPECTIVES
E HISTORY
HISTORY OF
HISTORY OF SCIENCE
OF SCIENCE
SCIENCE atmospheric, oceanic, geological, ecological, typically producing detailed descriptive reports Global environmental change may be the

vonAlexander
Humboldt von Humboldt and
and In and cultural phenomena across the globe. Hum- with little integration within or among the com- greatest challenge faced by human societies
In the
In the early 19th century,
In the
the early
early 19th
Alexander
early 19th century,
19th century, Alexander
von
century, Alexander von
Alexander von
von
Humboldt laid the foundations boldt’s obsession with geographically refer- ponent entities. However, for a few intellectu- since the advent of agriculture. Humboldt ad-
Humboldt
Humboldt laid
Humboldt laid the foundations laid
for the
the foundations for
foundations
today’s for today’s
for today’s
today’s enced measurements and collections was central ally nimble participants—including Charles vocated for science that spoke to human needs
the General Physics
Earthof the Earth
Earth
Earth system
Earth system sciences.
system sciences.
sciences.

l Physics of the
Earth system sciences. to his vision. He recognized that spatial arrays Darwin, T. H. Huxley, Matthew Maury, Asa and concerns (5). It is fitting that on the 150th
of observations could be aggregated to reveal Gray, C. Hart Merriam, and Peter Kropotkin— anniversary of his death, we recognize his role
patterns that would in turn reveal underlying these explorations provided data and experience in fostering the sciences that speak to the most
Stephen
Stephen T.
Stephen T. Jackson
T. Jackson
Jackson processes—such as the distribution of incident that spurred the development of biogeography, profound human concerns—sustainability of

A
radiation, the transport of heat and materials in ecology, oceanography, and other environmen- human societies and the ecosystems on which
sss scientists
scientists are
scientists are celebrating
are celebrating the
celebrating the 200th
the 200th
200th winds and ocean currents, the influence of tem- tal sciences (11). they depend.
anniversary
anniversary of
anniversary of Charles
of Charles Darwin’s
Charles Darwin’sDarwin’s birth birth
birth
rating the 200thand perature on plant form, and the effect of latitude Unfortunately, the conceptual unification
and the
and the 150th
the 150th anniversary
150th anniversary of
anniversary of the
of the pub-
the pub-
pub- and continentality on mountain snowline. among the sciences of the Earth that Humboldt References and Notes
s Darwin’s birthof
lication
lication
lication of his
of his On
his On the
On the Origin
the Origin of
Origin of Species,
of Species,
Species, He expanded this vision in the succeeding sought never developed in the century follow- 1. P. J. Bowler, Science 323, 223 (2009).[Abstract/
Darwin’s
rsary of the pub- ideas
Darwin’s
Darwin’s ideas continue
ideas continue to
continue to shape
to shape and
shape and enrich
and enrich
enrich years, establishing international cooperative ing his death. Disciplinary specialization played Free Full Text]
the sciences (1). 6 May 2009 marks 2. A. de Humboldt, Essai sur la géographie des
the sciences
gin of Species,
the sciences (1). (1). 66 MayMay 2009 2009 marks marks the the 150th
the 150th
150th networks of meteorological and geomagnetic a large role in eclipsing Humboldt’s integration, plantes (Levrault, Schell & Co., Paris, 1807).
anniversary
anniversary
anniversary of
of
of the
the
the death
death
death of
of
of another
another
another 19th-cen-
19th-cen-
19th-cen- measurement stations, inventing isotherms and as did 20th-century trends toward reductionism,
hape andtury enrich 3. An English translation of (2) is currently in
tury figure—Alexander
tury figure—Alexander von
figure—Alexander von Humboldt—
von Humboldt—
Humboldt— other graphical devices to portray spatial pat- experimentalism, and fine-scale processes in press at the University of Chicago Press, Chi-
marks thewhose150th
whose
whose scientific
scientific legacy
scientific legacy also
legacy also flourishes
also flourishes in
flourishes in the
in the
the terns, and noting that plant form is often better many disciplines. cago.
nother 19th-cen-
21st century.
21st century.
21st century. Humboldt Humboldt
Humboldt helped helped
helped create create
create the the
the predicted by local environment than by taxo- A new incarnation of Humboldt’s general 4. A. de Humboldt, Personal Narrative of Trav-
intellectual els to the Equinoctial Regions of the New
n Humboldt—intellectual world
intellectual world Darwin
world Darwin inhabited,
Darwin inhabited, and
inhabited, and his
and his
his nomic affinity (a paradox resolved by Darwin). physics of the Earth began to emerge with the Continent, During the Years 1799–1804, by
writings
in the inspired Darwin to embark on
writings
flourisheswritings inspired
inspired Darwin
Darwin to
to embark
embark on
on Humboldt’s genius lay in his geographical vi- plate tectonics revolution in the 1960s. Draw- Alexander de Humboldt and Aime Bonpland;
H.M.S.
H.M.S.
H.M.S. Beagle.
Beagle.
Beagle. More
More
More pertinent
pertinent
pertinent to
to
to our
our
our time,
time,
time, sion, and in his intuition that Earth’s land sur- ing on Humboldtian spatial arrays of observa- with Maps, Plans, &c. (Longman, Hurst, Rees,
lped create
Humboldt the
Humboldt established
Humboldt established the
established the foundation
the foundation for
foundation for the
for the
the face, oceans, atmosphere, and inhabitants form tions, this theory provided a unified explanatory Orme, & Brown, London, 1814 to 1829), vols.
habited, Earth
and his
system
Earth system
Earth sciences:
system sciences:
sciences: the the integrated
the integrated
integrated system system
system an integrated whole, with linkages among the framework for disparate geophysical, geologi- 1 to 7.
5. A. von Humboldt, Cosmos: A Sketch of the
to embarkof
of on
of knowledge
knowledge
knowledge on
on which
on which human
which human society
human society may
society may
may various components (4, 5). Humboldt’s general cal, paleontological, and biogeographic phe- Physical Description of the Universe (Johns
ent to ourdependtime,in
depend
depend inin the
the face
the face of
face of global
of global climate
global climate change.
climate change.
change. physics of the Earth envisioned climate as a nomena. Hopkins Univ. Press, Baltimore, 1997), vol. 1.
undationmajorforLike
Like
the
Like
voyage
Darwin,
Darwin, Humboldt
Darwin,
that
Humboldt undertook
Humboldt
would shape
undertook aaa
undertook major control of Earth-surface phenomena, with Today, a second, even broader manifestation 6. M. Nicolson, Hist. Sci. 25, 167 (1987). [ISI]
7. M. Nicolson, in Romanticism and the Sciences,
major voyage
voyage that that would
would shape shape his his ideas ideas vegetation serving as both an index of climate of Humboldt’s vision aspires to understand the
tegrated major
andsystem his ideas A. Cunningham, N. Jardine, Eds. (Cambridge
and thinking. Humboldt spent 5 years (1799
and thinking.
thinking. Humboldt
Humboldt spent
spent 55 years
years (1799
(1799 and a proximal control of microclimate, animal interactions and feedbacks among the compo-
Univ. Press, Cambridge, 1990), p. 169.
man societyto
to
maywith
to 1804)
1804)
1804) with botanist
with botanistAimé
botanist Aimé Bonpland
Aimé Bonpland explor-
Bonpland explor-
explor- habitat, and cultural practices (6–8). nents of the Earth system, encompassing the 8. M. Dettelbach, in Cultures of Natural History,
limate change.
ing Venezuela,
ing Venezuela,
ing Venezuela, the the northern
northern Andes,
the northern Andes, and
Andes, and cen-
and cen-
cen- Humboldt’s dream of systematic observa- lithosphere, atmosphere, hydrosphere, cryo- N. Jardine, et al., Eds. (Cambridge Univ. Press,
tral
dt undertooktral Mexico,
tral a with
Mexico,
Mexico, with visits
with visits to
visits to Tenerife,
to Tenerife, Cuba,
Tenerife, Cuba, and
Cuba, and
and tional arrays across the globe took hold in the sphere, and biosphere as well as human societies Cambridge, 1996), p. 287.
the United 19th century. Throughout the century, countless and economies. This effort is often referred to as 9. S. F. Cannon, Science in Culture: The Early
hape histhe United States.
theideas
United States. They
States. They collected
They collected botanical,
collected botanical,
botanical, Victorian Period (Dawson, New York, 1978).
zoological,
zoological, geological,
geological, and and ethnological
ethnological spec- spec- Humboldt-inspired explorations were launched, Earth system science, but it could just as well be
nt 5 yearszoological,
(1799
imens,
imens, mademade
geological,
extensive
made extensive
and ethnological
atmospheric
atmospheric and
extensive atmospheric
spec-
and geo-geo- Intellectual each involving systematic measurement and designated “general physics of the Earth,” using
10. W. H. Goetzmann, New Lands, New Men:
imens, and geo- Intellectual riches.
riches. The The central
central portionportion of of Humboldt’s
Humboldt’s Physical
Physical Tableau
Tableau of of the
the Andes
Andes and and Neighboring
Neighboring America and the Second Great Age of Discov-
Bonplandphysical
explor- measurements,
physical
physical measurements, and
measurements, and recorded
and recorded the
recorded
Intellectual
the Countries,
the
riches.
published
The
as part
central
of (2,
portion
3), shows
of Humboldt’s
Chimborazo in
Physical
profile,
Tableau
with
of
vegetation
the Andes
zones,
and
plant
Neighboring
species, mapping of physical, biological, and often cul- the early-19th century definition of physics as ery (Viking, New York, 1986).
Countries,
Countries, published
published as
as part
part of
of (2,
(2, 3),
3), shows
shows Chimborazo
Chimborazo in
in profile,
profile, with
with vegetation
vegetation zones,
zones, plant
plant species, and
species, and
and tural features of landscapes and oceans (8–10). the study of the material world and its phenom-
Andes, and geographic
cen- location
geographic location of of their
their thousands
thousands of of snowline 11. P. J. Bowler, The Norton History of the Envi-
geographic location of their thousands of snowline depicted
snowline depicted at
depicted at appropriate
at appropriate elevations.
appropriate elevations. In
elevations. In the
In the original,
the original, the
original, the profile
the profile is
profile isis flanked
flanked on
flanked on both
on both sides
both sides by
sides by tables
by tables
tables ronmental Sciences (Norton, New York, 1993).
specimens These surveys were relentlessly inductive, ena (which we now call science).
erife, Cuba, and and
specimens
specimens and tens
and tens of
tens of thousands
of thousands of
thousands of measure-
of measure- describing
measure- describing elevational
describing elevational patterns
elevational patterns in
patterns in temperature,
in temperature, humidity,
temperature, humidity, light
humidity, light refraction
light refraction and
refraction and intensity,
and intensity, agriculture,
intensity, agriculture, fauna,
agriculture, fauna, and
fauna, and
and
ments.
ments.
ments. Humboldt
Humboldt
Humboldt spent
spent
spent the
the
the next
next
next 22
22
22 years
years
years and
and
and other
other physical,
physical, chemical,
chemical, and
and biological
biological features.
features.
ected botanical,
most
other physical, chemical, and biological features.
most of
most of his
of his inherited
his inherited fortune
inherited fortune in
fortune in Paris,
in Paris, pre-
Paris, pre-
pre-
hnologicalparingspec-
paring and
and publishing
publishing 45
45 volumes
volumes of
of aaa never-
never- distribution
distribution of of incident
incident radiation,
radiation, the the transport
transport serving serving as as both
both anan indexindex of of climate
climate and and aaa prox-
prox-
paring and publishing 45 volumes of never- distribution of incident radiation, the transport serving as both an index of climate and prox-
spheric and geo-report
finished on his travels. of heat and materials in winds and ocean cur- imal control of microclimate, animal habitat,

PARIS
finished report on his travels. of heat and materials in winds and ocean cur- imal control of microclimate, animal habitat,

PARIS
finished report on his
Intellectual travels. riches. The portion of
centralofportionheat and materials
of Humboldt’s in winds
Physical TableauPhysical and ocean
Tableau cur- imal
of the Andes control of microclimate,
andpublished
Neighboring animal habitat,

PARIS
Intellectual riches. The central Humboldt’s of the Andes and Neighboring Countries, as part
d recordedOf these
Ofthethese volumes,
volumes, the first
thepublished
first was
was aaa as slim
slim work
work rents,
rents, the
the influence
influence of
of temperature
temperature on
on plant
plant and cultural
andatzones,
cultural practices
practices (6–8).
(6–8).

MUSEUM,
Of these volumes,
of
Countries, the
(2, 3), shows first was
Chimborazo slim in work
profile,
part of rents,
with
(2, the
vegetation
3), shows influence
zones, plant
Chimborazo of temperature
species,
in on
and snowline
profile, with plant and
depicted
vegetation cultural
appropriate practices
plant elevations.
species, (6–8).
and

MUSEUM,
MUSEUM,
entitled
ir thousandsentitled
entitled ofEssay
Essay
Essay In theon
on the
the Geography
onoriginal,
the the profile of
Geography
Geography of
of Plants
is flanked
Plantson both
Plants form,
form,
form, and
sides
and
and bythe
the
the effect
tables
effect
effect of
of latitude
describing
of latitude
latitude and
elevational continen-
patterns in temperature,
andprofile
and continen-
continen- Humboldt’s
Humboldt’s
Humboldt’s dream
humidity,
dream
dream lightof
of
of systematic
systematic observa-
systematic observa-
observa-
(2, snowline depicted at appropriate elevations. In the original, the is flanked on both sides by tables
(2,
nds of measure- 3). The
(2, 3).
3). The modest
The modest title
refraction
modest title belies
title
and
belies the
intensity,
belies the intellectual
the intellectual tality
agriculture,
intellectual tality on
fauna, and
tality on mountain
other
on mountain snowline.
physical,
mountain
chemical,
snowline.
snowline.
and biological features. tional
tional arrays
tional arrays across
arrays across the
across the globe
the globe took
globe took hold
took hold in
hold in the
in the
the

HISTORY
describing elevational patterns in temperature, humidity, light refraction and intensity,century. agriculture, fauna,the and

HISTORY
HISTORY
richness
richness within.
richness within. In
within. In the
In the text
the text and
text and accompanying
and accompanying
accompanying He
He expanded
He expanded this
expanded this vision
this vision in
vision in the
in the succeeding
the succeeding 19th
succeeding 19th century.Throughout
19thcentury. Throughoutthe
Throughout thecentury,
century,countless
century, countless
countless
ext 22 years and
color
color plate
color plate (see
plate (see
(see
other
the
the
physical,
the figure),
figure),
figure),
chemical,
Humboldt
Humboldt
Humboldt laysand
lays
lays outbiological
out
out years, features.
years,
years, establishing
establishing international
establishing international cooperative
international cooperative Humboldt-inspired
cooperative Humboldt-inspiredexplorations
Humboldt-inspired explorationswere
explorations werelaunched,
were launched,
launched, In the early 19th century, Alexander von

A
NATURAL
NATURAL
e in Paris, pre-
aaa vision
visionsof
vision of a comprehensive
ofscientists
aa comprehensive
comprehensive “general
“general
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physics
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meteorological
meteorological and
and
and geomagnetic
geomagnetic
geomagnetic each
each
each involving
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and
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NATURAL

arenothing
celebrating the a200th inhabited, and his writings inspired isotherms
Darwin to atmospheric and geophysical measurements,
umes of aof of the
never-
the Earth”
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distribution
aimed
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anniversary
at
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Charlesless
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Darwin’s
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the
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on H.M.S.
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serving
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Beagle.inventingMore pertinentas both
isotherms
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to our and
mapping
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of physical,
and
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biological,
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and often
often
and often
location
cul-
cul-
cul-
of their
Humboldt laid the foundations for today’s
THE
THE

thesis
thesis of atmospheric, oceanic, geological, and other graphical devices to portray spatial tural
tural features of
of landscapes and oceans (8–10).
THE

ofand atmospheric,
of150th oceanic,
heat anniversary
and materials geological,
thein windstime,and
and other
ocean graphical
cur- devices
imalthe tocontrol
portray spatial
of microclimate, features ofanimal landscapes
habitat, and oceans (8–10).
RIGINAL COPY IN THE NATURAL HISTORY MUSEUM, PARIS

thesis of atmospheric,
the oceanic, geological,
of publi- and other
Humboldtgraphical devices
established to portray
foundation spatial tural
for thousands features of landscapes
specimens andand tensoceans (8–10).
of thousands
ININ

ecological, and cultural phenomena across the patterns, and noting that plant form is often These surveys were relentlessly inductive, typ-
IN

ecological, and cultural phenomena across the patterns, and noting that plant form is often
COPY

was a slimecological,
cationwork of his On and cultural
the Origin
rents, phenomena across
of Species, Darwin’s
the influence the
of temperature patterns,
the Earth on and
system noting
plant sciences:that
and plant
thecultural form is
integratedpracticesoften
system of(6–8).These
These surveys
surveys were
were relentlessly
measurements. Humboldt spent the nexttyp-
relentlessly inductive,
inductive, typ-
22
COPY
COPY

globe.
globe. Humboldt’s
globe.continue
Humboldt’s
Humboldt’s obsession
obsession
obsession with
withthe
with geographi-
geographi-
geographi- better
better
better predicted
predicted
predicted by
by
by local
local
local environment
environment
environment than
thande-
than by ically
by years
by icallyand
ically producing
producing
producing detailed
detailed
detailed descriptive
descriptive
descriptive reports
reports
reports
ideas to shape and enrich sciences of knowledge on which human society may most of his inherited fortune in Paris,
ORIGINAL

raphy ofcallyPlants form, and the effect of latitude and continen- Humboldt’s dream of systematic observa-
Earth system sciences.
ORIGINAL
ORIGINAL

cally
cally referenced
referenced
referenced measurements
measurements
measurements and
and collec-
and collec-
collec- taxonomic
taxonomic
taxonomic affinity
affinity
affinity (a
(a paradox
(a paradox
paradox resolved
resolved by
resolved with
with little
by preparing
by with little integration
little integration
integration within
within
within or
or among
amongof the
theacom-
com-
(1). 6 May 2009 marks the 150th anniversary of pend in the face of global climate change. and publishing 45 or among
volumes the com-
nev-
s the intellectual
tions
tions
tions was
was
was tality
central
central
central to
to
to on
his
his
his mountain
vision.
vision.
vision.
the death of another 19th-century figure—Alex-
He
He
He snowline.
recognized
recognized
recognized Darwin).
Darwin).
Darwin). Humboldt’s
Humboldt’s
Humboldt’s tional
genius
genius
genius arrays
lay
lay
lay in
in
in his
his
hisacross
geo-
geo-
geo-
Like Darwin, Humboldt undertook a major er-finished report on his travels.
the globe
ponent
ponent
ponent took
entities.
entities.
entities. hold
However,
However,
However, in the
for
for
for aaa few
few
few intellectu-
intellectu-
intellectu-
AN

that
that spatial
d accompanying arrays Heof observations
ofexpanded this couldvision be graphical
be invoyage
the succeeding vision, and
and19th in
in his intuition
century. that
that ally
Throughout nimble
allyOfthe participants—including
century, countless Charles
AN
AN

that
ander spatial
spatial arrays
arrays
von Humboldt—whose of observations
observations scientific could
could legacy be graphical
graphical vision,
thatvision,
would shape and in
his his
his
ideas intuition
intuition
and thinking. that ally nimble
nimble
these participants—including
participants—including
volumes, the first was a slim Charles
Charles
work
FROM
FROM

aggregated to reveal patterns that would in Earth’s land surface, oceans, atmosphere, and Darwin, T. H. Huxley, Matthew Maury, Asa
FROM

umboldt alsoaggregated
lays out
aggregated
flourishes to
to reveal
years,
reveal
in patterns
the establishing
patterns
21st century. thatHumboldt
that would
international
would in Humboldt
in Earth’s
Earth’s land
cooperative
land surface,
surface,
spent 5 years oceans,
oceans, (1799 atmosphere,
Humboldt-inspired
atmosphere,
to 1804) with and explorations
and Darwin,Essay
Darwin,
entitled T. H.
T. H.
wereHuxley,
Huxley,
on launched,
the Matthewof
Matthew
Geography Maury,
Maury,
PlantsAsaAsa(2,
turn reveal underlying processes—such as the inhabitants form an integrated whole, with Gray, C. Hart Merriam, and Peter Kropotkin—
REPRODUCED

turn reveal underlying processes—such as the inhabitants form an integrated whole, with Gray,
3). C. Hart Merriam, and Peter Kropotkin—
REPRODUCED

helped
turn revealcreate the
underlying intellectual
processes—such world Darwin
as the botanist
inhabitants Aimé formBonpland
an exploring
integrated Venezuela,
whole, with Gray, The C. modest
Hart title
Merriam, beliesand the
Peterintellectual
Kropotkin— rich-
REPRODUCED

“general physics networks of meteorological and geomagnetic

linkages among the each components
various involving systematic (4, these measurement
explorations provided anddata and experi-
linkages
the northern
linkages among
amongAndes, theand
the various
central
various components
Mexico, with
components (4, ness
(4, thesewithin.
these explorations
In the text
explorations provided data and
and accompanying
provided data and experi-
experi-
color
g less than a syn- measurement stations, inventing 5).
5).
visits
5). to
isotherms
Humboldt’s
Humboldt’s
Tenerife,
Humboldt’s general
general
Cuba,
general
mapping
physics
and physics
physics the of
ofof
United
of the
the
the
physical,
Earth
Earth
States.
Earth
biological,
ence
ence
plate
ence that
that
(see
that the
and
spurred
spurred
spurredfigure),
often
the
the
the
cul-
development
development
Humboldt
development of
of
lays
of biogeog-
biogeog-
out a vi-
biogeog-
Botany Department
Botany Department
Department and and Program
and Program
Program in in Ecology,
in Ecology, University
Ecology, University
University of of
of
nic, geological,
Botany and other graphical devices toThey
portray
envisioned
envisioned spatial
climate
climate astural
as aaa major features
major control
control of landscapes
of raphy,
of sion
raphy, aand
of ecology,
ecology, oceans (8–10).
oceanography,
oceanography, and
and other
otherof envi-
envi-
CREDIT:

Wyoming,
Wyoming, Laramie,
Laramie, WY WY 82071,
82071, USA. USA. E-mail:
E-mail: jackson@ collected
envisioned botanical,
climate as zoological,
major geological,
control of raphy, comprehensive
ecology, oceanography, “general andphysics
other the
envi-
CREDIT:

jackson@
CREDIT:

Wyoming, Laramie, WY 82071, USA. E-mail: jackson@

omena acrossuwyo.edu
uwyo.edu
uwyo.edu the patterns, and noting that plant Earth-surface
and form
Earth-surface is often
ethnological
Earth-surface phenomena,
phenomena, Thesewith
specimens,
phenomena, made
with vegetation
surveys
with vegetation
extensive
vegetation ronmental
were relentlessly
ronmental
Earth”
ronmental aimed sciences
inductive,
sciences
at nothing
sciences (11). typ-
(11).less
(11). than a synthesis of
with geographi- better predicted by local environment than by ically producing detailed descriptive reports
14 15
ents596
596
and collec-
596 taxonomic affinity (a 1
11 MAY
MAY
MAY 2009
paradox VOL 324 bySCIENCE
VOL 324
2009 resolved
2009 VOL 324 www.sciencemag.org
with little
SCIENCE
SCIENCE integration within or among the com-
www.sciencemag.org
www.sciencemag.org
 BOOKS ET AL. BOOKS ETAL.

HISTORY OF SCIENCE mer students who challenged ing the translation of Origin of Species into translations involved an attempt to recast exist- And so, finally, we come to Haeckel.
The Tragic Sense of Life his ideas as they gained in- German, and (more intriguingly) diachroni- ing German terms in a newer, more up-to-date Gliboff ’s key insight here is that Haeckel
Making German Evolution: Ernst Haeckel and
the Struggle over
tellectual independence, and
debated the pro-evolution
cally, as scientists reworked older words such mode that encompassed selection yet tamed
as “perfection” and “type” to lend them new Darwin’s emphasis on unpredictability to meet
originally read Bronn’s translation of Darwin,
not Darwin in the original. Gliboff shows
Translation and Tragedy Evolutionary Thought (but anti-Haeckel) Jesuit priest
and entomologist Erich Was-
meanings. Gliboff’s own clear, crisp prose is the more rigorous requirements of a German
key to the success of this analysis, as he deftly academic scientist’s understanding of a “law”
Haeckel as both echoing and responding to
Bronn’s concerns, rather than either reflect-
by Robert J. Richards
Lynn K. Nyhart mann—the list could go on leads his reader through dense philosophical of organic nature. Simultaneously, Bronn ing directly on Darwin’s original writing or
University of Chicago
Press, Chicago, 2008.
and on. These were not iso- and terminological thickets with nary a thorn sought to translate Darwin’s ideas about selec- reaching directly back to the Romantic

I
n this year of Darwin anniversaries (the duced important books. Robert 579 pp. $39, £27. lated episodes but rather scratch. This is some of the best close reading tion into a language without an exact equiva- embryologists. (Although Gliboff acknowl-
200th year of his birth and the 150th J. Richards, the director of the ISBN 9780226712147. moments in a lifelong cam- I have seen. It also represents a profound chal- lent for the term, and for an academic audience edges the centrality of monism to Haeckel’s
anniversary of On the Origin of Species), University of Chicago’s Fish- paign to advance his philoso- lenge to our standard picture of 19th-century lacking the gentlemanly traditions of breeding thought, he focuses on the working evolution-
The Tragic Sense of Life and H. G. Bronn, bein Center for the History of phy, which was accompanied German biology. pigeons and dogs so central to Darwin’s expo- ary theorist, not the popular ideologue.) Like
Ernst Haeckel, and the Origins of German Science and Medicine and a H. G. Bronn, by a bitter hostility to orga- The old story, crudely put, is that Haeckel’s sition. The selection metaphor was further Bronn himself, Haeckel made further amend-
Darwinism remind us that the history of evo- much-published author on Darwin Ernst Haeckel, and nized religion. version of evolution was a Darwinism in name fraught with an anthropomorphism foreign to ments both terminological and intellectual,
lutionary thought in the 19th century extended and German Romantic biology, the Origins of Richards does not neg- only, best understood as an update on early- Germans, who were not brought up on British and Gliboff rereads Haeckel’s research pro-
well beyond Darwin himself. Darwin did not has written a biography of Haec- German Darwinism lect Haeckel’s science pro- 19th-century idealistic morphologists such natural-theological assumptions about a per- gram as one not dominated by a typological
launch his theory onto an unprepared public kel. Sander Gliboff, a professor A Study in Translation per, treating us to fascinat- as Carl F. Kielmeyer and J. F. Meckel that sonified God who had created a perfectly and linear-recapitulationist mindset but
and scientific community, nor was the evolu- in Indiana University’s Depart- and Transformation ing and original discussions retained their teleology, their typological adapted nature. Bronn’s translation, though it rather as continuing to wrestle with the need
tionism that developed after 1859 a mere ment of History and Philosophy by Sander Gliboff of his pathbreaking system- emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehen- to account for variability and unpredictable
extension of his views—it was not even one of Science, places Haeckel at the atic and phylogenetic work tionism. This story, emphasizing the long per- sible to a German academic audience, was not change in terms of mechanistic laws of
MIT Press, Cambridge, MA,
thing. How, then, should we think about the end of a study that examines the on radiolaria and other marine sistence of a German transcendental approach a conservative throwback. It represented the nature—among which Haeckel included, at
2008. 271 pp. $35, £22.95.
history of evolution in the 19th century? What larger process through which ISBN 9780262072939.
organisms, the importance to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolo- the top of his list, natural selection. Haeckel’s
sorts of accounts best help us understand the Darwin’s words were translated, of linguistic analysis to his history of biology. gist who had also long been working on many Darwinism thus shows continuity with early-
reception of Darwin’s theory, its relations to and his ideas modified, in the phylogenetic trees of the Gliboff challenges this history right from of the questions Darwin claimed as his own— 19th-century concerns, mediated through
earlier ideas about nature, the directions that context of German biology. Both illuminate races of humans, and his remarkable experi- the beginning. The ascription of simple linear a critical yet generous equal, who saw himself Bronn. But those concerns were always more
evolutionary investigation subsequently took, the twists and turns that evolutionary thought mental work with siphonophores. These con- recapitulationism to the views of Romantic as moving science forward through the modi- flexible than has been acknowledged, and
and the relations of all of these to the broader took in Germany, but they do so in dramati- stitute important contributions to our under- embryologists, he notes, owes much to a carica- fications he made to Darwin’s flawed theory. their articulation changed over time. Of
social, cultural, and religious concerns scien- cally different ways. standing of the technical development of ture developed by Karl Ernst von Baer in a Bronn’s death in 1862 afforded him little course Haeckel’s Darwinism was not
tists shared with their contemporaries? Richards’s book, though over twice as long evolutionary biology. polemical context, then adopted uncritically by chance to steer the conversation further. Darwin’s own, but it was not an aberration or
These questions become especially pointed as Gliboff’s, is the more entertaining read of The big picture here, however, is an argu- influential historians such as E. S. a distortion of some true theory, any more
when one considers German Darwinism, and the two. In his characteristically rich and ment about the power of personality—at least Russell and Stephen Jay Gould. than any other post-Darwinian additions or
especially Germany’s best-known follower of rolling prose, Richards weaves a compelling one personality—to shape the course of sci- Gliboff’s fresh reading of the orig- adjustments were. It was science moving on.
Darwin, Ernst Haeckel. Most often remem- story of a life marked by tragedy and of an ence. In Richards’s presentation, German evo- inal sources interprets Kielmeyer Gliboff ’s overall picture of scientific
bered by biologists as the author of the bio- intense, larger-than-life figure whose passions lutionism was profoundly shaped by both and Meckel as far less rigidly advance, in contrast to Richards’s emphasis on
genetic law (“ontogeny recapitulates phy- drove his scientific research and philosophy. In Haeckel’s charisma and his combativeness. typological in their orientation and charisma and passion, is one of scientists
logeny”), Haeckel has also been accused of Richards’s rendering, the scientific Haeckel Perhaps the late-19th-century opposition of much more attentive to nature’s building and innovating incrementally, work-
promoting European fascism via his monistic cannot be understood separately from the evolutionary science to Christianity would not variability than has been seen ing with what their predecessors have handed
philosophy and of presenting a eugenic, bio- man’s personality and private circumstances. have been so fiery, he suggests, had Haeckel before. Both for these early-19th- them and sculpting it into something new yet
logically determinist vision of humanity that His love of nature was surpassed only by his not continually fanned its flames. And century naturalists and for their understandable to those around them. His sen-
led to Hitler’s “final solution.” Can one scien- love for his first wife, Anna Sethe, who died in although Richards absolves Haeckel of per- intellectual heirs, Gliboff argues, sitive reading allows us to see post-1859
tist be responsible for so much? Most histori- abdominal agony on his 30th birthday. Over sonal responsibility for fascism and Nazism, the critical issue was to understand German evolutionists as rational actors rather
ans would say no, arguing that it takes a com- the next year, he wrote his way through the in part by situating him firmly in his time and nature’s manifold variety while than irrationally stuck in some early-19th-

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

munity, rather than an individual, to make a despair that enveloped him, producing his place, he does show how the scientist’s ardent seeking out underlying strict natu- century moment with unmodern commit-
movement; that single-cause explanations are foundational work, Generelle Morphologie temperament led him to the occasional intem- ral laws to account for it. ments. By challenging the very foundations of
insufficient to account for something as broad (1). Although he remarried, the union was not perate statement that could be taken up by This provides a new starting the standard narrative of German morphol-
as fascism; and that an individual cannot be happy, and passionate love would elude him extreme thinkers. One cannot leave this book point for analyzing Darwin’s first ogy, this careful, compelling account does at
held responsible for the ways in which others until his sixties, when he had a secret affair that without a deep appreciation for Haeckel as a translator, the prominent paleon- least as much as Richards’s to undermine the
(such as Hitler) took up his ideas and molded ended tragically with the death of his lover. tragic figure and for the force of personality in tologist H. G. Bronn—a figure lit- association of 19th-century German Darwin-
them to new agendas after his death. But that Science remained his salvation and refuge. shaping the direction science may take. tle attended to in the standard ism with a dangerously exceptional view of
still leaves open the questions of how to write His professional life was also filled with Gliboff’s account is of a completely differ- story but the lynchpin of Gli- nature. But the two books offer very different
responsibly about what Haeckel actually drama, much of which centered on his philos- ent order. His is not a story of personalities or boff’s. Intriguingly and plausibly, reads. Is scientific progress a matter of per-
believed and how we should situate him in the ophy of evolutionary monism—a science- private lives (although he mentions salient Gliboff argues that Bronn’s use sonal anguish and triumph, or of intellectual
history of evolutionary thought. centered faith that became one of the most details), but of German academics seeking to of terms like “vervollkommnet” chugging along? Our concept of it should be
The historians under consideration here successful alternatives to the Judeo-Christian live up to the highest (if changing) ideals of (perfect) as translations for Dar- capacious enough to include both.
have chosen two radically different strategies religion among those searching for a secular Wissenschaft and of the ways in which win’s “improved” or “favored”
to understanding Haeckel’s place within spirituality. Haeckel could not turn down a Darwin’s theory was translated into this envi- were not about dragging Darwin References and Notes
1. E. Haeckel, Generelle Morphologie der Organismen
German evolutionism, and both have pro- fight: He battled the physician-statesman ronment. He thus situates Haeckel at the end backward into a German teleo- (Georg Reimer, Berlin, 1866).
Rudolf Virchow over the role of evolution in of a revised intellectual history of 19th- logical view of nature (as has 2. The reviewer previously served as a press reader for both
the schools (Haeckel argued that it should century German evolutionism. Central to his been claimed by those who have books at the manuscript stage.
The reviewer is at the Department of the History of Science,
University of Wisconsin, Madison, WI 53706–1393, USA. replace religious education), sparred with reli- account is the idea of translation, which he paid attention to Bronn at all). A painter, too. Haeckel’s oil landscape of highlands in Java, from
E-mail: lknyhart@wisc.edu giously conservative scientists and with for- uses both synchronically, especially in treat- Instead, Gliboff asserts, Bronn’s Wanderbilder (1905). 10.1126/science.1169621

16
1170 27 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org www.sciencemag.org SCIENCE VOL 323 27 FEBRUARY 2009
17
1171
 REVIEW shaped by something
by the organisms’ (later identified as genetic(the
own activities muta- so- vancing through a predetermined sequence of ulation became divided
direction stages within each family, driven by force derived dependent acts of migration
up, in explaining
science, this case bypresent in- distribu-
opments that would push other naturalists toward called tions), but it was effect),
Lamarckian not aimed butinthis anytoo onepermitted tions into terms oceanicofislands. past migrations,
REVIEW REVIEW
an evolutionary vision during the years he worked
opments that would push other naturalists toward
in isolation. By the late 1850s, the idea of pro-
and, thus,
multiple vectors left adaptive
of change.
ended. He allowed a limited role for variation
depicted as a branching
evolution
tree
Evolution
in which
essentially hadopen-
each
to be from individual development.
act of
Here, Darwin followed
REVIEW Lyell in seeing
extinctions
geography must become a historical
for Lyell)
and (for
evolutionary
that Darwin
bio- but not
adaptations.
Darwin’s Originality of the individual variants in a population was the relations among species. Several
an evolutionary vision during the years he worked
gressive
proposals
of isolation.
in progressive
evolutionhiswastheory
Byevolution
widelytorecognized,
the late 1850s, was widely predict
the
andorderly
an
recognized,
idea of pro-
the pattern of of the
shaped by the organisms’ own activities (the so-
branching
called was thevariants
individual
Lamarckian result
effect), ofin
buta amore tooorpermitted
population
this less was un-
science, explaining present distribu-
tions in Populations
It has been ofargued
terms pastdivided that Darwin’s
migrations, by geographical move
Darwin’s Originality essentially undirected ruled out any possibility available in the 1830s deflected attention
Peter J. Bowler that evolution could be shaped by a predeter- from the model of the branching
positive
opments
gressive
articulated
an
was
evolutionary
tree
positivebeing
role
that
away
(11).
role
of individual
would
by thinkers
vision
articulated
of individual
push
relations.
and the positive role of individual competition
evolution was
Itby
widely
hassuch
during
competition
other
been
thinkers
naturalists
recognized,
as argued
the
competition
Herbert
years was
such asthat
was
and
he Spencer
being
toward
worked
Herbert
being
the
Darwin’s move to a
predictable
tion.depicted
At the same
ity that evolution
migration
essentially undirected ruled out any possibil-
multiple vectors of of
time, Darwin’s
as a branching could be
organisms
change. Evolution
intheory
treeshaped
to
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a new
had
undermined
each
toloca-
act of
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push
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for
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Lyell)the
German
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naturalists
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extinctions and
asevolutionary
each
years
(forwillDarwin
adapts
romanticismhe worked
develop
toward but independently
was inspired
to its new environ-
adaptations.
[e.g. (12)], but a
mined developmental trend. There was no ob- William Sharp Macleay’s quinary (Fig.
in or 1). But
isolation.
circular keymore
By aspects
the late of the viewpoint
1850s,
historical Darwinian
the idea of vision
was pro-inspired by German the old
branching idea that
was species
the result were
of a idealized
more or lesstypes,
un- Populations ment dividedin itsby own way, and the pos-
geographical
Darwin’s Originality
Peter J. Bowler
Charles Darwin’svious
contributions todid
theory
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goal of natural
toward selection
science. an
produce
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When orderly
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hailed
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and as it one
1859, however,
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gressive
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Herbert
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Darwinian
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(12)],
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Wallace
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Darwin’s
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a new order.
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of
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gressive evolution wasthe
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Charles Darwin’s theory of natural selection has been hailed as one of the most innovative occurred
were trulytooriginal
any comparison:
other andnaturalist
would not at the
have time. Here,
occurred it did not produce anspecies
orderlywere pattern of relations positive role of individual
Beagle competition
voyage was
(1831–36). being The Galapagos
by his contemporaries, even by those who accepted the general idea of evolution. This article provides
articulated a good
by thinkers such Heas too moved
Herbert toward
Spencer the old idea that idealized types, ment in its own
ingHerbert way,
process Spencer and the pos-
of evolution that Darwin
Peter J. Bowler
contributions to between
modern science. species. When The accusation
first proposed that the theory however,
in 1859, rangeditinwas a circle;
widely each family five genera,
rejected to any and
Wallace other provides
insights
sonaturalist
a good
gained
at the time. onHere,
comparison:
the BeagleWallace
He
voyagePeter
too J. Bowlering
(1831–36).
between
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species. inThe
fixed elements accusation that the theo- articulated by thinkers such provided
species
sibility that
as
barriersthe can most obvious example
be crossed
identifies those depended
by his contemporaries,
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even “random”by those who
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indicated
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on of revolutionary
through
evolution. the taxonomictheory, hierarchy.provides
This article
the
(Fig. idea
1). aBut
Chambers’s of branching
good keycomparison:
aspects
The evolution
Galapagosof He the too drivenprovided
Darwinian
species
moved
by local
vision
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Darwinian in vision
the late 1830s. It was
including
Charles Darwin’s his studiestheory of biogeography and animal breeding, and his recognition of the role played moved
adaptation, toward but the
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did branching
not share evolution
Darwin’s ry depended
Species hadon to be “random”
treated as variation
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allows forwithin
the aproblem
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identifies cerns
those aspects ofofof natural
hisDarwin’s
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work onthatthishas been
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develop as one ofrevolutionary
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example would
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rangeas one of the most innovative were truly original andingwould byofapproaching
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contributions to for
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insight
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The concerns
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athe insight that the work of the As of possible
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who accepted as geneticthe generalmuta- idea vancing of evolution.
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up,
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science and in Western culture. Yet there of how process certainly wise and benevolent God. There a wider
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ing
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evolutionism the
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publication
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the Origin.
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ment
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in its own of
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Historians have quarried Darwin’s notebooks Latin evolutio refers to the unrolling of a scroll.) assumption
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variation. is still preserved in the very term “evolution”;
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NICHOLSON/CORBIS

appreciate just how new and how radical it ended, divergent evolution. Wallace One
overover innovation
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NICHOLSON/CORBIS

TheThe image of
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CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY

to anyone embedded in a vision of nature as a diversity.
MICHAEL NICHOLSON/CORBIS

and was proposed independently by Wallace in

CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY

was perhaps the first to realize that if adaptation (modern Indonesia). might be natural processes
in 1855. adapting species that itto predictable,
models could have beengoverned
proposed by to account for Thisery promptedwas so his move that toward evolutionism

CREDIT (LEFT TO RIGHT): STAPLETON COLLECTION/CORBIS; HULTON-DEUTSCH COLLECTION/CORBIS; MICHAEL NICHOLSON/CORBIS

a paper published Both realized orderly system a divine model radical many late
MICHAEL

a paper published
changes in their in 1855. Both realized that predictable,
it plan. orderly system governed byproposals
a divine (13). This modelmany was so radical thatargued many that late
to the local environment was the only mechanism Adrian Desmond and James explained whyenvironment.
naturalists were But able Darwin
to arrange was the relations
Such a world among
view species. Severalto
made it difficult ac- 19th-century Because
evolutionists were unableslaveholders to accept
of evolution, there would be major implications Moore have recently proposed that explained
perhaps why
theinto first naturalists
to realize were able
that if adaptation to arrange
using descentto cept plan. Such a world
that theinhistory
available the 1830s view made
of lifedeflected it difficult
on earth attention
might be away to ac- 19th-century
theErnst
black evolutionists
raceargued was separately were unable
created to accept
of from the
MICHAEL

species groups within groups, it in full. Mayr that the theory

speciesfrominto groups ancestor withinwasgroups, onlyusing the descent cept that the history ofbranching
life on earth mightWil- it in
be white, full. Ernstonewanted
Mayr argued that that the theory of
COLLECTION/CORBIS;

for the whole system by which species are clas- Darwin’s hatred of slavery prompted the local aenvironment
common the
to explain mechanism under- essentiallyfrom theirregular
model of the
and unpredictable, tree (11).
dependant common descent Darwin
was of Darwin’s to show greatest all races
sified into groups. Darwin’s mentor in geology, his move toward evolutionism (13). from
of a common
evolution,
lying thereancestor
similarities. would
Closely be to explain
major
related thehave
implications
species under- di- onliamessentially
hazardsirregular
the Sharp Macleay’s andquinary
of migration, unpredictable,
isolation,or circular dependant
and local system
common descent
share aincommon
achievements, was
addition ancestry, one of
to natural and
Darwin’s
selection greatest
he realized that
COLLECTION/CORBIS;

Because many slaveholders argued lyingverged

similarities.
recently Closely related ancestor,
species whereas have di- on the hazards Darwinofwas migration, isolation, and local achievements,
itself (14). So it was, but in addition
I think Mayr to natural over- selection
Charles Lyell, had shown how his uniformitarian for the whole system from a common
by which species are clas- adaptation.of classification led toward
supposed his alterna-
that every genus con- this claim could be defended by extending the
theory would allow the biogeographer to re- that the black race was separately verged the recently
ancestry of from more distantly related
a common ancestor, forms must tive
whereas model in Darwin
adaptation. part because was he ledwas more his
toward inter- estimated
alterna- the (14).
itself rapidity Sowith whichbut
it was, otherI natural-
think Mayr over-
Fig. 1. Charles construct Darwin, Alfred Russel Wallace, and on Herbert Spencer. sified be into groups. Darwin’s mentor in geology, tained five species that could be arranged inistsa were idea throughout
converted thethe animal kingdom. As a ba-
the migrations of species an ever- created from the white, Darwin the ancestry traced offurther
moreback distantlydown the family
related forms tree mustto ested tiveinmodel
adaptation thanbecause
in part cosmic teleology,
he was thanks more inter- estimated theto rapidity theory. with Many which of the other natural-
COLLECTION/CORBIS;

Charlesfind Lyell,
the common had shown point of how
origin. his uniformitar- tocircle; the each family
influence of five genera,
William Paley’s and so on
natural through
the- sis for his
non-Darwinian thinking,
theories of this thesis
evolution is sure to gener-
proposed
Fig. 1. Charles changing
Darwin, earth.Russel
Alfred Populations
Wallace,ofcould andand sometimes
Herbert Spencer. wanted to show that all races share be traced further back down the family tree to ested in adaptation than cosmic teleology, thanks ists were converted to the theory. Many of the
ferences But
position. Darwin thehad created the outlines letters to establishhis thetheory
complex process by term “evolution”; the Latinchallenged evolutio refers to the ian theory would allow the biogeographer
now seems soto ology. the taxonomic hierarchy. Chambers’s Vestigesduring
of the much controversy,
ate“eclipse but if late accepted it would
HULTON-DEUTSCH

which theory of natural selection thisancestry,

vision find theThe idea of point
common descent to theNatural selection replaced divine benev- of Darwinism”theoriesinoftheevolution 19th proposed
between become ways
divided in by which he and barriers,
geographical sohethat developed (6–9). Darwin a common and he realized common of origin. influence of William Paley’s natural the- non-Darwinian
the theory 20 years earlier, and there were sig- which he developed his theory (6–9). Darwin unrolling of a scroll.) The explanatory framework reconstruct
obvious the
that migrations
we might of
wonder species what on an
alternativeever- the
olence Natural
as an History
explanation of Creation
of adaptation. depicted
Unlike evolu-
century emphasize
were introduced the crucial
with the role
aim played
of subvert- by his move
HULTON-DEUTSCH

Wallace formulated their ideas. Insingle

this essay, I wassplit a highly creative thinker who synthesized a of nature as an orderly patternthat of relations.
thisthis claim could be defended The idea of common descent now seemsforso Macleay ology. Natural selection replacednotdivine benev- during the “eclipse of Darwinism” in the late 19th
ferences
nificant betweenwhat
differences the was
ways
between
once in awhich
the ways
species
inhewhich and could which
was heinto
a highly developedcreative his theorywho
thinker (6–9). Darwin theory
synthesized centered of on natural
the selection
theory challenged
of natural selection vision
chal- changing
models earth. could have Populations
been proposed could sometimes
to account tion in terms of parallel
and Chambers, lines did
Darwin advancing expect throughing the toward
implicationsa model of the of branching
principle evolution
of common based on
argue1.that
Fig. Darwin
Charles was
Darwin,
multiple truly
Alfred originalRussel in his think-
Wallace, and number
Herbert of key
Spencer. insights, some derived from his Darwin’s world view was byprofoundly differ-
extending the idea Fig. 1. Charles obvious
throughout Darwin, that Alfred weRusselmight Wallace, wonder what and Herbert alternative Spencer. olence as an explanation of adaptation. Unlike century were introduced with the aim of subvert-
Wallace
he and formulated
Wallace formulatedtheir branches
ideas.
their In adapting
ideas. thisInessay,
this
to Iseparate
es- was
a aenviron-
number highly of creative
key insights, thinker some whoderivedsynthesized
from a of
his naturethis
lenged as vision
an orderly of pattern
nature as of
an relations.
orderly pattern become divided by geographical barriers, so a predetermined sequence of stages within each geographical diversity.
ing, and I support ments this(10).claim by addressing
Evolution the scientific work and others from currents circulat- ent because he argued that thethe adaptation
animal kingdom. of pop- As a basis for models could have been proposed to account for Macleay and Chambers, Darwin did not expect ing the implications of the principle of common
argue
say, I that
argue Darwin
that was truly
Darwin was original
truly in would
originalhis think-
inand
become
his number
a divergent
scientific ofworkkey insights,
and others some from derived
currents from circu- Darwin’s world view was profoundly
his of relations. differ- that what was once a single species could split family, driven323 by force from individual
derived www.sciencemag.org This model was so radical that many late
HULTON-DEUTSCH
COLLECTION/CORBIS;

related
ferences issue of defining
between the
process, just
wayswith why
insome the
which theoryhe
branches was splittinging over
which in his he cultural
anddeveloped environment.
his theory Few (6–9).would Darwinnow ent ulationsoftonatural
theory
because heworld
their local
selection
arguedview
environment
that the challenged
his was this
thinking, the solethesisferences
vision
this is sure to
between224 the ways in which he and which 9 JANUARY he developed 2009 his VOL theory (6–9). SCIENCE Darwin theory of natural selection challenged this vision
ing, and Iand
thinking,
so disturbing
Wallace
support
I support
to
formulated his
this claimthisideas.
contemporaries.
their
by addressing
claim In bythis addressing
essay,
the scientific
I lating
accept
was a inthe
highly
work
hisclaim and others
cultural
creative that
from currents
environment.
evolution
thinker who by Few circulat-
natural
synthesized would se-a cause
of Darwin’s
nature of transmutation.
as an orderly pattern wasadaptation
Many of profoundly
people
relations.
of pop-
found dif-it into multiple branches adapting to separate en- development. 19th-century evolutionists were unable to accept
over again, whereas others was came toinga in dead his end generate wasmuch controversy, butformulated
if their ideas. In this essay, I was a highly creative thinker who synthesized a of nature as an orderly pattern of relations.
COLLECTION/CORBIS;

related issueissue of defining just why the theory cultural environment.

Fig. 2. Tree ofFewLife,wouldfrom now ulations
Darwin’s notebooks to their (22). local environment the sole Wallace
the Darwin
argue related
that Darwin of
wasthrough defining
certainly
was truly notjustthe
original
extinction. why inthe
first histotheorysug- number
think- now
lection acceptwas
of claimthe
key claim
in insights,
the air.thatDarwin
someevolution approached
derived byfrom
natural the cause
his ferent tobecause
hardDarwin’s see natural he
world argued
selection
viewMany that
was the agent
asaccepted
the adaptation
profoundly itofdiffer-
either
would of emphasize the224 vironments (10). Evolution would become 9 JANUARY a 2009These rigidly
VOL 323 structuredSCIENCEmodels ofwww.sciencemag.org
taxonomic it in full. Ernst Mayr argued that the theory of
so disturbing to his contemporaries. accept the that evolution by natural se- of transmutation. people found it argue that Darwin was truly original in his think- number of key insights, some derived from his Darwin’s world view was profoundly differ-
was
gest sothedisturbing
idea of to his
evolution contemporaries.
as an alternative to selection
subject in was
a wayin the
that air.
was Darwin approached
significantly differentthe populations
divine
ent because benevolence to their
he argued local
or of
that a
roletheenvironment
rationally
adaptation was
structured the divergent process, with some branches splitting relations and evolution made good sense to any- common descent was one of Darwin’s greatest
ing,Darwin
and I supportwas certainly this
Theclaim imagenotby of addressing
the the
firsttreetoofsug- life scientific
the hadlectionappeared was work
inin and the othersThese
air. from
Darwin rigidlycurrents circulat-
structured
approached themodelshard of
to seetaxo- natural crucial
selection asplayed
the agent by his ofofeither
pop- toward
move ing,a andmodel I support this claim by addressing the scientific work and others from currents circulat- ent because he argued that the adaptation of pop-
theDarwin was certainly not the first to sug- subject in cultural
a2)way that was significantly different sole cause of transmutation. Many people found over and over again, whereas others came to a one embedded in a vision of nature as a predict- achievements, in addition to natural selection it-
COLLECTION/CORBIS;

relatedcreation
issue of defining
species
Darwin’s byjust God. why
notebooks J.theB. Lamarck’s
theory
of the was
late fromin(Fig.
ing
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other efforts
environment.
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Few
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ulations
good teleology.
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local environment
branching adaptedevolution species
was the
basedto
sole anon geographical
related issue of defining just why the theory was ing in his cultural environment. Few would now ulations to their local environment was the sole
gest the idea of evolution as an alternative to subject in a way that was significantly different divine benevolence or of a rationally structured
gest
theory, thepublished
idea ofhis evolution
incontemporaries.
1809,proposed as an
had been alternative
widely dis- to acceptfrom
plain any
the ofclaim
thehistory the other
ofthatlifeefforts
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had to ex-
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ever-changing see natural
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didtheso by agent killing of so disturbing to dead end through extinction. accept the claimable, thatorderly system by governed
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STAPLETON

so disturbing
creation oftospecies and was by God. J. B.independently Lamarck’s by Wallace ofin the to anyone evolution
embedded bymade natural tovision cause
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CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY

the from any other efforts being ex- teleology. Selection adapted species his contemporaries. evolution transmutation. people
the creation
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theory, publisheda in paper
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STAPLETON

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the
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RIGHT):

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CREDIT

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CREDIT

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CREDIT (LEFT

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of Darwinism” in the late 19th whereas the ancestry of more distantly related as an explanation of adaptation. Unlike naturalMacleay
adaptive series
response of parallel
in some lines moved through the same
circumstances.
School of Philosophy and Anthropological The Queen's
www.sciencemag.org SCIENCE VOL 323have9 been JANUARYMore 2009seriously for the idea of cosmic tele- 223School of Philosophy and Anthropological Studies, The Queen's inal way.
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University of Belfast, University thatBelfast,
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Northern what ward Toansome
alternative evolutionary olencevision
extent, as anduring
Darwin may
explanationthe years of he adaptation. More Unlike seriously centuryfor the were idea of cosmic
introduced with tele- the aimUniversity
of subvert- forms must be traced
of Belfast, University Road Belfast, Belfast, Northern further back down
To somethe and
extent, Chambers,
Darwin Darwin
may havedid not
been expect his
Moretheory hierarchy
seriously for the of developmental
idea of cosmic stages, an updated
tele-
Ireland, BT7 1NN, UK. E-mail: p.bowler@qub.ac.uk
models could have been proposed tomerely
www.sciencemag.org worked
account infor
“aheadisolation.of
SCIENCE hisBytime,”
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VOL 1850s,
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the implications that
that the the ofproduction
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Ireland, BT7 1NN, UK. family
E-mail:tree to find the common point
p.bowler@qub.ac.uk of origin.
merely “ahead of to predict
his time,” an orderly pattern
anticipating of relations.
devel- ology, Darwin’sversion supposition of the thatidea suggested in Chambers’s
the production

18 19
224 www.sciencemag.org SCIENCE
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 REVIEW
Vestiges. The similarities linking the species in directed variation among individual organisms. tion thinking, and although he may have ex- descent (15). The TheAmerican
Struggle for Existence
neo-Lamarckians scale and that for thatbetransition
could investigated in the directly. century. It individuals.
late 19thinterbreeding the Men Traditionally,
Who Discovered species
It (Doubleday, New
a genus were due not to a recent common ances- Although convinced that the degree of variabil- aggerated the extent to which Darwin himself Edward DrinkerOne Cope and Alpheus Hyatt pro- There was a well-developed network
of the most disturbing aspects of Darwin’s did, however, highlight the harsher aspects of of breeders were treated as York,
idealized 1958).
types with a fixed es-
try, but to parallel trends independently reaching ity was artificially enhanced under domestica- made the conceptual transition, the subsequent posed that the evolution
theory was of each group should
its appeal to the be by for
struggle this exis-
time, andthe although
consequences their ofideas about The
struggle. sence,potential 2. P.
any variation Corsi,
from theThe normAgebeing
of Lamarck:
trivial Evolutionary
heredity and impermanent. TheTheories
breeders in France,
knew that 1790–1830
they (Univ. of
the same stage of development. Like Chambers, tion, Darwin, nevertheless, accepted that there development of the selection theory brought this seen as a series tence
of parallel
as thelines
natural moved
processthrough
that equates with and
the variation were distinctly
implications were drawn pregenet-
out even more clearly California Press, Berkeley, 1988).
they endorsed the recapitulation theory (ontog- must be some equivalent variability in every implication out more clearly. the same hierarchybreeder’s activity as a selecting agent. This very when Galton argued that it would be necessary 3. A. Desmond, The Politics ac-
of developmental stages, an up- ical (like Darwin’s own), they had a very clear could produce huge changes in structure by
of Evolution: Mor-
eny recapitulates phylogeny, in the terminology wild population. The analogy with artificial se- In the debates that followed the publication dated version of harsh
the idea suggested in Chambers’s appreciation of how they produced
vision of nature certainly threatened the to apply artificial selection to the human race changes in cumulating normal variations over a number
phology, Medicine and Reform in Radical
of
introduced by Ernst Haeckel) and saw evolution lection then allowed him to depict natural selec- of On the Origin of Species, the analogy with Vestiges. The similarities linking the species in a their artificially small populations.
traditional belief in a benevolent Creator. The in order to prevent “unfit” individuals from The insight generations. When Darwin linked this informa-
London (Univ. of Chicago Press, Chicago,
as the addition of preordained stages to ontog- tion as a parallel process in which a few variant artificial selection continued to play a keyREVIEW role
genus were due not to a recent common ancestry, that they worked by selection may have been tion with his conviction
term “struggle for existence” occurs in Thomas reproducing and undermining the biological 1989).
that species could change
but to parallel trends independently reaching the important (this is the point of contention among indefinitely over4.time, P. J.heBowler, Evolution:
was driven towardThe aHistory of an
eny. Adaptation was not crucial once the basic individuals, in this case with characters useful to by forcing even Darwin’s critics to think about Robert Malthus’s An Essay on the Principle health of the population. This was the eugenics
descent (15). The American neo-Lamarckians scale and that could be investigated directly. interbreeding individuals. Traditionally, species same stage of development. Like Chambers, they experts studying Darwin’s notebooks), but the new form of speciesIdea concept(Univ.inofwhichCalifornia Press, Berkeley, ed.
the pop-
character of the group was established, and the species rather than the human breeder, sur- the problems of heredity and variation in a new of Population, although used in the context of program, and in its most extreme manifestation 3, 2003).The natural range of
Edward Drinker Cope and Alpheus Hyatt pro- There was a well-developed network of breeders were treated as idealized types with a fixed es- endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing. He ulation becomes paramount.
the linear, orthogeneticposedevolution of the ofgroup
that the evolution each group vive andbe
should reproduce.
by this Those
time, andwithalthough
harmfultheir charac-
ideas about sence,Opponents
way (18). any variationsuch fromas theFleeming
norm beingJenkin,
trivial tribal groups competing for limited resources. at the hands of the Nazis, it led not just to the 5. J. A. Secord, Victorian Sensation: The Ex-
recapitulates phylogeny, in the terminology intro- realized that in a domesticated population there variability becomes part of the species’ character,
traordinary Publication, Reception, and Secret
might eventually generate
seen as abizarre series ofnonadaptive
parallel lines moved ters through
are eliminated
heredity byandthevariation
strugglewerefor existence,
distinctly pregenet- who saw selection working
and impermanent. on large
The breeders knewvariations
that they Darwin saw that population pressure would lead sterilization but also to the actual elimination of
duced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental Authorship deviations
of Vestigesfromof theaNatural History
characters as a prelude to extinction—the
the same hierarchy of developmental the- stages,just asan the
up- breeder
ical (likewill not permit
Darwin’s any had
own), they animal or “sports
a very clear of nature,”
could produce huge changes in structure by still
were, nevertheless, ac- to competition between individuals and was per- those unfortunates deemed unfit by the state. Did
the addition of preordained stages to ontogeny. undirected variation among individual organisms. fixed norm. This is what of Creation
Mayr called(Univ. oftheChicago
transi- Press, Chicago,
datedDarwin
ory of “racial senility.” version of could
the ideamake no intoChambers’s
suggested reproduce if it does not
appreciation of have the character
how they he working
produced changes within normal
in cumulating the framework
variations over defined by this
a number of
Adaptation was haps the first
not crucial once to realize
the basic that it might
char- represent
Although Darwin’s
convinced that theemphasis
degree on the natural tion
of variabil- elimination
from typological 2000).
thinking to population think-
Vestiges. The similarities linking the species in a their artificially small populations. The insight generations. When Darwin linked this informa-
sense of the theory proposed by Cope and Hyatt, wants. It was the breeders who taught Darwin analogy. For supporters such as Francis Galton,
genus were due not to a recent common ancestry, that they worked by selection may have been tion with his conviction that species could change
a means by which the population could change of maladaptive
acter of the group was established, and the linear, ity was artificially enhanced under domestication, variants help to
ing, create a 6. heD.may
and although Kohn, have The Darwinian
Ed.,exaggerated the Heritage: A
because he could notbutimagineto parallelantrends evolutionary
independently that variation
reaching is not directed
the important (this is toward
the pointsome preor- among
of contention artificial selection
indefinitely overhelped
time, he to was
clarify
driventhe nature
toward a throughoftime
orthogenetic evolution (19, 20).
the group mightTheeven-
processDarwin,
workednevertheless,
by climate of opinion
accepted that therein must
which be suchextentatrocities
to which Darwin Centennial
himselfRetrospect
made the(Princeton
con- Univ. Press,
process driven by predetermined trends. But Like
same stage of development. the Chambers,
dainedthey goal, allowing
experts studying build onnotebooks),
him toDarwin’s his exist- but of theboth
new heredity
form of andspecies concept inpaving
selection, which thethe pop-
way tually generate eliminating the least fitcharacters
bizarre nonadaptive variants within some theequivalent
popu- became in every wild popu- ceptual transition, thePrinceton,
possible?
variability subsequent NJ, 1985).
development of
flourished
fact that such theoriesendorsed the in the late 19th theorying conviction that adaptive
certainly evolution
taught himmust one be thing. for
He theulation
revolutionary impact The of Mendelian
natural rangege- lation and allowing theof better adapted to survive 7. J. Browne, Charles Darwin: Voyaging (Jona-
recapitulation (ontogeny breeders becomes paramount. of
as a prelude to extinction—the theory “racial lation. The analogyItwithhas to be admitted
artificial selectionthat,thenby making death it- theory
the selection brought this
than Cape, London, implication
1985).out
century demonstratesrecapitulates
just how radical phylogeny, the intheory an open-ended,
the terminology intro- realizedbranching
that in process.
a domesticated population there The notion
netics.variability becomesof part
“hard”
of theheredity was in-
species’ character,
senility.” Darwin breed.make
andcould Thisno wassense
whatofthethe philosopher
allowedHer- him to depict natural force
self a creative in nature,
selection as a par-Darwinmore introduced
clearly. 8. J. Browne, Charles Darwin: The Power of
duced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental deviations from a
of open-ended, divergent evolution was to the At the same time, the breeders’ attitude to- troduced in opposition to the “soft” form of
the addition of preordained stages to ontogeny. undirected variation among individual organisms. fixed norm. This is what Mayr called the transi- theory proposedbert Spencer
by Cope andwould
Hyatt,later refer he
because to as the
allel“survival a new and
process in which a few profoundly disturbing insightIninto
variant individuals, thethe
debates that Place (Jonathan
followed the Cape, London, 2002).
publication
naturalists of the time.Adaptation was not crucial once theward basic variation
char- Although Darwin toward
pushedconvinced the view
that the degree inheritance
of variabil- tion from implied by the
typological Lamarckian
thinking to population process.
think- could not imagine of an
theevolutionary
fittest.” Strictly process drivennatural
speaking, selection
in this case withworld, an insight
characters useful thatto the seems
species to have
of resonated
On the Origin 9. ofM. J. S. Hodge,
Species, G. Radick,
the analogy withEds., The Cam-
acter of the group was established, and that
the the species
linear, ity wasis artificially
just a population
enhanced under of domestication,
inter- The undirected natureheofmay
ing, and although variation was clarified
have exaggerated the by predetermined requires
trends.only But the differential
fact that reproduction
such ratheramong with thebreeder,
than the human thinkingsurviveof many andwho re- didartificial
not under- bridge Companion
selection continued to play atokey Darwin
role (Cambridge
Artificial Selection orthogenetic evolution of the group breeding might even- individuals. Traditionally, species
there mustboth extent to the
be through study of large
himselfpopulations by variants, Univ. Press, Cambridge, 2003).
Darwin, nevertheless, accepted that which Darwin made the con- theories flourished in the but lateDarwin thought
19th century that theproduce.
dem- pressureThose
of withstandharmful
or accept the details
characters areofelim-
his theory. Darwin-even Darwin’s
by forcing critics to think about
10. M. J. S. Hodge, Stud. Hist. Biol. 6, 1 (1982).
These non-Darwinian models
tually generate were ultimately
bizarre nonadaptivewere treated as
characters some idealized
equivalent types with in
variability a fixed es- popu-
every wild Galtonceptual
and through
transition, the
the subsequent studies of the
breeding development of
onstrates just howcompetition
radical the wastheory
necessary to makeinated
of open- it effective. ism wasfornotexistence,
by the struggle “responsible” just asforthe Darwinism
socialthe problems of 11.heredity and variation in a new Naturalists:
as a prelude to extinction—the theory of “racial lation. The analogy with artificial selection then the selection theory brought this implication out P. F. Rehbock, The Philosophical
synthesis
marginalized by thesenility.” of the selection sence, any variation from the norm being trivial geneticists. Although it took some time for the
Darwin could make no sense of the allowed him to depict natural selection as a par- more clearly. ended, divergentItevolution
seems that waswithout
to thethe input frombreeder
naturalists Malthus, henot permit
will or eugenics
any animalin anytosimple
reproduce way. if After
wayall,(18).
someOpponentsThemes such as Fleeming
in Early Jenkin,
Nineteenth-Century British
theory and genetics theory
in theproposedearly 20th by Cope century.
and Hyatt,and impermanent.
because he allel processThe breeders
in which aknew that they
few variant geneticists
individuals, to accept
In the debates the
that situation,
followed thetheir studies
publication of the time. would not have come up with the theory. it does not have the early geneticists
character endorsed
he wants. It was eugenics
the who by analogy Biology (Univ.
saw selection working on large of Wisconsin
variationsPress, Madison,
Genetic mutations seemedcould not toimagine
be essentially plu- process
an evolutionary coulddriven
produceinhuge changes
this case in structure
with characters usefulby to ac- of mutation
the species of On the ultimately
Origin ofendorsed
Species, the Darwin’s
analogyclaim
with The idea of struggle was pervasive in thewho
breeders lit- taught
with Darwin
animal that breeding
variation even whileordismissing
is not “sports of nature,” 1983).were, nevertheless, still
ralistic and undirected,by providing
predetermined justtrends.
the source
But the fact that such normal
cumulating variations
rather than the human overbreeder,
a number surviveof and that
re- the only way
artificial the continued
selection environment could
to play a keyaffect
role erature of the period, but could be directed
Artificial Selection exploitedtoward
in somenaturalpreordained
selection asgoal, the mechanism
allowing of within 12.
evolution.
working the R. J. Richards,
framework The Meaning
defined by thisof Evolution: The
that Darwin’s
of “random” variationtheories flourishedmechanism
in the late 19th centurygenerations. When Darwin
dem- produce. Those withlinked
harmfulthis infor-are elim-
characters the population
by forcing was evenby selection.
Darwin’s criticsModern
to thinkevolu-
about many different
These non-Darwinian models ways. In the 1850s, him
were ultimately Spencer had on his
to build Andexisting
the Nazis wanted
conviction thattoadapt-
purify a analogy.
fixed racial
For supporters Morphological
such as Francis Construction
Galton,and Ideological
onstrates just how radical the theory of open- inated by the struggle for existence, just as the the problems of heredity and variation in a new Reconstruction of Darwin’s Theory (Univ. of
required as its raw ended,
material. This later devel- mation with his conviction that species could tionary developmental biology has reopened the
divergent evolution was to the naturalists breeder will not permit any animal to reproduce if way (18). Opponents such as Fleeming Jenkin,
marginalized byalready seen how
the synthesis of competition
the selectioncould ivebe turned must
evolution bewhich
type, they certainly
an open-ended, did not want
branching to admit
artificial selection helped
ChicagotoPress, clarify the nature
Chicago, 1992).
opment highlights the of the importance
time. of another change indefinitely it does not over
have time, he was
the character driven
he wants. It wasquestion
the whoofsaw whether
selection working and
variation evolution
on large can
variations into ainvery
theory and genetics the different,
early 20thand in some respects
century. process. less had evolved gradually from an ape ancestry. But 13.
of both heredity and A.selection,
Desmond,paving the way
J. R. Moore, Darwin’s Sacred
insight gained by Darwin in the late 1830s, his toward a newbreeders form ofwho species
taughtconcept
Darwin that in variation
which is be not quite as open-ended
or “sports of nature,”aswere,Darwin and his still
nevertheless, fol- Genetic mutations disturbing,
seemed to mechanism
be essentially of plu-
progress (21). At the Forsamebytime,proposing that evolution
the breeders’ attitude for primarily
worked the revolutionary Cause: Race, of
impact Slavery and the Quest for Hu-
Mendelian
decision to investigate the work
Artificial of the animal the populationdirected
Selection becomes toward paramount. The natural
some preordained goal, allowing believed.
lowersworking Butthethe
within non-Darwinian
framework defined by vision
this Spencer,
ralistic and undirected, the interaction
providing betweentoward
just the source individualsvariationthrough
pushed the Darwin
elimination towardof useless
the variants,
genetics.Dar- The notion man ofOrigins
“hard”(Allen Lane,was
heredity London, 2009).
breeders (Fig. 3) and his recognition that
These non-Darwinian theirwererange
models of variability
ultimately becomes
him to build on hispart of the
existing species’
conviction of evolution
that adapt- analogy.unfolding to ansuch
For supporters orderly, predictable
as Francis Galton, stimulated their efforts to adapt to the chang- win created an image that could all too easily be
of “random” variation that Darwin’s mecha- view that the species is just a population of introduced in 14. E.
opposition Mayr, to One
the Long
“soft” Argument:
form of Charles Dar-
marginalized by the synthesis of the selection ive evolution must be an open-ended, branching artificial selection helped to clarify the nature win and the Genesis of Evolutionary Thought
method of artificial theory
selection offered a useful character, not the result of accidental deviations plan has
and genetics in the early 20th century. process.
been essentially marginalized by accep-
of both heredity and selection, paving the way
nism required asing social
its raw and physical environment. He then exploited by those who wanted the human race
material.
(Harvard Univ. Press, Cambridge, MA, 1991).
way of understandingGenetic
how the equivalent natural
mutations seemed to be essentially plu- from a fixed norm. At This
the is
same what
time,Mayrthe called
breeders’ the tance
attitude of
for the
thekey insights onimpact
revolutionary which Darwin based
of Mendelian invoked Lamarck’s
This later development high- concept of the “inheritance to conform to their own pre-existing ideals. In 15. P. J. Bowler, The Eclipse of Darwinism: Anti-
exactand
process operated. Theralistic role played by
undirected, Dar- justtransition
providing the sourcefrom toward variationthinking
typological to popula-
pushed Darwin toward histhe theory of natural
genetics. selection.
The notion of “hard” heredity was of acquired
lights the importance characteristics” to explain how these the same way, his popularization of the struggle
of another Darwinian Evolution Theories in the Decades
win’s study of breeding in the formulation
of “random” variation that of his Darwin’s mecha- view that the species is just a population of introduced in opposition to the “soft” form of insight gained by Darwin in the accumulated over many gen- metaphor focused attention onto the individual-
self-improvements Around 1900 (Johns Hopkins Univ. Press,
theory is much debated nism by historians
required as its raw (16–17),
material. late 1830s, his decision
erations,toleadinginves- to biological evolution and so- istic aspects of Spencer’s philosophy. Baltimore, MD, 1983).
This later development high- tigate the workcial ofprogress.
the animal 16. R. J. Richards, Stud. Hist. Philos. Sci. 28, 75
but there can be little doubt of how important
lights the importance of another
Spencer’s self-improvement mod- Modern science recognizes the importance (1997).
artificial
the analogy between insight andby natural breeders (Fig. 3)el and his recog-
gained Darwinselec-
in the of progress became immensely popular in the of Darwin’s key insights when used as a way 17. M. Ruse, J. Hist. Ideas 36, 339 (1975).
tion became in his later thinking.
late 1830s, In thistocase,
his decision inves-
nition that their later
method of artifi-
19th century, and because it too seemed to of explaining countless otherwise mysterious 18. J. Gayon, Darwinism’s Struggle for Survival:
Darwin was truly unique,tigate because
the workeven of the Wallace
animal cial selection offered
rely on a useful
struggle wayas the motor of change, it was aspects of the natural world. But some of those Heredity and the Hypothesis of Natural Se-
did not take this step and dissociated
breeders (Fig. 3) and his himself
recog- of understandingoftenhowconfused
the equiv-with the Darwinian mechanism. insights came from sources with profoundly dis- lection (Cambridge Univ. Press, New York,
nition that their method of artifi- alent natural process operated. 1998).
from the link with artificial selection expressed
cial selection offered a useful way
In fact, Spencer thought that all humans will turbing implications, and many historians now 19. P. J. Bowler, J. Hist. Ideas 37, 631 (1976).
The exact role played by Darwin’s
in Darwin’s later writings.
of understanding how the equiv- eventually acquire the faculties needed to inter- recognize that the theory, in turn, played into 20. A. Desmond, J. R. Moore, Darwin (Michael
study of breeding in the formula-
Darwin turned to alent
the breeders
natural processin search of a
operated. act harmoniously with one another. But his occa- the way those implications were developed by Joseph, London, 1991).
tion of his theory is much debated
clue as to how a population
The exactcould be changed—
role played by Darwin’s sional use of highly individualistic language al- later generations. This is not a simple matter of 21. M. Francis, Herbert Spencer and the Invention
by historians (16–17), but there of Modern Life (Acumen, Stocksfield, UK,
study ofwhere
here at least was a situation breeding modifications
in the formula- lowed him to be perceived as the apostle of free science being “misused” by social commenta-
tion of his theory is much debated can be little doubt of how impor- 2007).
were actually being produced
by historianson(16–17), a human buttimethere tant the analogy enterprise.
between artificialMuch of what later became known tors, because Darwin’s theorizing would almost 22. C. Darwin, Transmutation Notebook B, from
scale and that couldcanbebe investigated
little doubt of how directly.
impor- as “social
and natural selection becameDarwinism”
in his was, in fact, Spencerian certainly have been different had he not drawn Natural Selection portfolio p. 36 (Cambridge
There was a well-developed network of breed- social Lamarckism expressed in the terminology inspiration from social, as well as scientific, in- Univ. Library, Cambridge, 1838); P. H. Bar-
CREDIT: AMERICAN MUSEUM OF NATURAL HISTORY

tant the analogy between artificial later thinking. In this case, Darwin
ers by this time, andand although their ideas
natural selection became about
in his of struggle popularized by Darwin. fluences. We may well feel uncomfortable with rett, P. J. Gautrey, S. Herbert, D. Kohn, S.
was truly unique, because even
CREDIT: AMERICAN MUSEUM OF NATURAL HISTORY

heredity and variationlaterwere distinctly

thinking. In this pregeneti-
case, Darwin This point is important in the context of those aspects of his theory today, especially in Smith, transcribers and Eds., Charles Dar-
was truly unique, because even Wallace did not take this step and win’s Notebooks p. 180 (British Museum of
cal (like Darwin’s own), theydid had a very clear the charge raised by modern opponents of light of their subsequent applications to human
Wallace not take this step and dissociated himself from the link Natural History, Cornell Univ. Press, Ithaca,
they produced
appreciation of how dissociated himself changes
from the link in Darwinism
with artificial selection that the theory is responsible for the affairs. But if we accept science’s power to up-
expressed NY, 1987); available at the Darwin Digital
their artificially smallwithpopulations.
artificial selectionThe expressed
insight writings. of a whole range of unpleasant social set the traditional foundations of how we think
in Darwin’s laterappearance Library, http://darwinlibrary.amnh.org/.
that they worked byinselection
Darwin’s later may have been
writings. Darwin turned to the based
policies breeders on struggle. Darwin exploited the about the world, we should also accept its po- 23. G. Neumeister, Das Ganze der Taubenzucht
important (this is the point Darwin turned to theamong
of contention breeders idea as of tothehowstruggle (B. F. Voigt, Weimar, 1876).
in search of a clue as to how a in search of a clue a for existence in a way that tential to interact with moral values.
experts studying Darwin’s notebooks),
population could be changed— but the was unique
population could be changed— until paralleled by Wallace nearly
breeders certainly taught him one thing.
here at least was a situation where He real- here at least was 20 years later.
a situation whereTheir theory certainly fed into
ized that in a domesticated
modifications population
were actuallythere be- is modifications were actually be-that led toward various kinds of References and Notes
the movements
1. L. Eiseley, Darwin’s Century: Evolution and
always a fund of apparently
ing produced purposeless
on a human and un- time Fig. 3. Pigeons (23). ing produced onsocial Darwinism,
a human time but it was
Fig. not the only
3. Pigeons (23).vehicle

20 www.sciencemag.org SCIENCE VOL 323 9 JANUARY 2009 225 21

www.sciencemag.org SCIENCE VOL 323 9 JANUARY 2009 225
 Speciation
disentangle key aspects of clade histories. Clades
REVIEW are monophyletic, including all descendants of an SPECIALSECTION
Speciation ancestor, whereas taxa may be monophyletic or
vestigations, provide an outline of how of these new taxa could become established only by on diversity, SPECIALSECTION
and other correction
because regimes
The Red Queen and the Court Jester: paraphyletic, excluding
and other Comparative
studies correspond
some descendants
to the predictions
the
driving others
marine ecosystem
to extinction.
Sepkoski’s
became saturated.
coupled logistic Key evidence
model (5)
plants,
may
these be
insects,
groups
or
so complex
vertebrates,
seem to have as toradiated
produce data in

3000

600
ancestor.
disentangle key aspects macroecological
of clade histories. studies
Clades
of
add the RedtoQueen,
rigor analyses Court showing Jester,that andsister
multilevel
clades is that both
marine origination
identified
ecosystem threeand
became extinction
equilibria,
saturated. rates
in the Cam- which
explosively, geologic
plants, without
insects, and orbiologic
diversity plateaus,signals
vertebrates, are
because

Number of genera
Species Diversity and the Role of Biotic
REVIEW

genera
are monophyletic, including all descendants of an

blue)
particularly
mixed models (Table 1), and outline some phy- appear to have brian,been
most density-dependent
of the Paleozoic, and per-
model (5) (5– not these ingroups
obviously the past 100 million
separated.

(empirical; red)
Sepkoski’s coupled logistic seem to have radiated

2000 of 3000
may vary whereas
in rate of taxa evolution, timing of increases

(corrected;600
ancestor, may be monophyletic or haps a third, beginning in the Pliocene years (My) (10).
7), limiting

2000
logenetic studies ofand themorphospace
macroevolution of spe- risesequilibria,
in diversity andCam-promoting Life on land today themay be as much as

400
in species richness occupation, identified three in
to the explosively, without diversity plateaus,
The Abiotic
Red Queen andThrough
the Court Jester: paraphyletic, excluding some descendants of the and continuing the present (Fig. Resolution between equilibri-

Number of genera
and Factors Time cies diversity. of evolutionary novelties across rapid recovery after extinction andevents. 25
um times asanddiverse in as thelife inandthe
100sea, so it

Number of genera

(corrected; blue)
brian, most 2A).of the Paleozoic, per- levels particularly past million

(empirical; red)
and distributions These three equilibrium models, between these

Number
ancestor. Comparative macroecological studies
lineages hapsAlternative models
a third,correspond
beginning for
theglobal
tointhree Pliocene
sets diversi-
of phyla, the may be
years
expansionist wrong(My) to(10).
models, generalize
might seem from marine
add rigorand to subclades. Here, I that will sister
explore the

400
1000
analyses showing clades

200
Species Diversity and the Role of Biotic
Michael J. Benton
The
an
Global global,
largest-scale
in species of
Patterntaxic
how these
richness
of Diversification
investigations,
may vary in rate of evolution, timing of increases
Through
outline Time and other studies
and morphospace
provide
corre-
occupation,
fication
and
species
2A). These
areCambrian,
continuing expansionist,
to the
interacted
diversity
Paleozoic, allowing
present
and successively
threetoequilibrium
rise,
each other through the Cambrian-
and (Fig.
Modern, global
levelsreplaced
with damping,
that
but
paleontological
straightforward,
pendsand
land um
Resolution
on adequate
sea
models,
but
show
studies
thebetween
assessment
similar
and
quality of the fossil record. The long-
to all de-
solution
of
between
life.equilibri-
the Perhaps
the these
patterns of and
ex-
A key toquestion ofabout thetheorigin of modern without a predictable
correspond to three sets limit of phyla, (8–11). the Den- ponential increase
expansionist in species
models, numbers
might (8,
seem
and Abiotic Factors Through Time spond the predictions of Red Queen, Court

1000
and distributions evolutionary novelties across Ordovician and Permo-Triassic inter- term saturation model for global diver-

200
0

0
Evolution may be dominated by biotic factors, as in the Red Queen model, or abiotic factors, biodiversity
Jester, is how today’s
lineages and subclades. Here, I will exploreand
and multilevel mixed 10
models million
(Table species
1), the sity dependence
Cambrian, Paleozoic, of origination
vals, reaching and Modern,
higher and thatextinc-
equilibrium levels
Cm O S D C P Tr J K Pg Ng
9, 11),straightforward,
sification or(Fig.
perhaps2, bluethey butdiffer
curve) the
arisesin their key
solution de-
as in the Court Jester model, or a mixture of both. The two models appear to operate arose from a single ultimate speciesofofthe microbial tion rates and does notlong-term
preclude expansionist rules (13, 14), with the seaassessment
acting
data as aof giant
interacted 500 400 300 200 100 0 pends on adequate the
outline some
largest-scale phylogenetic
global, studies
taxic investigations, macro-
provide after successively
each replaced
replacement event. from extensive attempts to correct
tion predominantly
Michael J. Benton over different geographic and temporal scales: Competition, predation, and other life 3500 of
evolution
an outline million
howyears
ofspecies diversity.
these ago
and (Ma)
other (Fig.
studies1).corre-
Two models
each because
other they may
through
The second the
model be(6,dampened
Cambrian-7) identifiesby a Time (Ma)
Gaussian
sets forquality petri
sampling dish,
of error
the (6,where
fossil 7),record.species
where- Thediver-
long-
biotic factors shape ecosystems locally and over short time spans, but extrinsic factors such as models for global diversification are termed the limiting factors
Ordovician single equilibrium
such as shortage
and Permo-Triassic level from
inter- the food
of early as theterm multiple-equilibria
the past sity is equilibrial
saturationand and
model expan-
density-dependent,
for global diver-

0
spond to the predictions of the Red Queen, Court Ma, to the Fig. 2. Patterns O of S marine animal genus Trdiversification K through
climate and oceanographic disentangle key aspects of clade histories. Clades The Paleozoic, perhaps 400levels Fig. 2. Cm Patterns D
of marine C
animal P
genus J
diversification Pg Ng
through sion models originally used raw data,
Evolution may be dominatedand by tectonic
biotic factors, events as shape
in the larger-scale
RedareQueen patterns regionally
model,including
monophyletic, or abiotic and
all descendants
Global Pattern ofmodel
factors, of an saturation/equilibrium
Jester, and multilevel mixed
Diversification
models(5–7)(Table
and the ex-
1), and
vals, reaching
or space, orpresent higher
active(Fig. equilibrium
predation,
2B). In both as well
models, astheby 530 My,
the empirical
past500
the Phanerozoic.
530(uncorrected)
My, the
The
400Phanerozoic. two lines
300 The200 compare
two(red
current
linesline)
compare
100 estimates from
current
0 and
without
sification (Fig.
land witnessing
thecorrection 2, blue
(5, 8–11),continuing
curve) arises
although (damp-
globally,
as in the and through
Jester thousands
model, or and millions of of years. ThePaleobiological studies tosuggest that speciesor pansion Through model Time (8–11). The equilibrium model after each long-term
climate andequilibria replacement
other physical event.
factors. Further, ened) from extensive attempts to correct data
more recent analyses return a some- as ever
exponential rise in diversity
Court a mixture both. two ancestor,
models whereas appear taxa operate
may be monophyletic the Sepkoski database and sampling-
outline some phylogenetic studies of the macro- correspond to biodiversity estimates from the empirical
standardized (corrected) analysis Time (uncorrected)
(Ma)
of the Paleobiology Sepkoski
Database (blue database
line).
diversity is driven largely by abiotic factors such as climate, landscape, or food supply, and The second model (6, 7) identifies a sets for sampling error (6, 7), where-
Red Queen and the Court Jester:
predominantly over different geographic and temporal scales: Competition, predation, and other
comparative
biotic factorsphylogenetic shape ecosystems approaches locallyoffer and new over insights
short time
paraphyletic,
intospans,
clade but
ancestor.
excluding
dynamics.
Comparative
some descendants
macroecological
extrinsic factors such as
of the
studies
has
A key
least,
prevailed,
evolution question
for
diversity
of species
isa how
long
among
about
time,
today’s
marine
the
diversity.
and
origin paleobiologists
of modern bio-
represents
10 million a
species classic
arose
at it seems that
single
may be equilibrium
partly
the coupled
saturation
become anlevel
in whichlogistic
from the
artifact
established
new taxamodel
onlyearly
of taxonomic
could The (redempirical
by driving aPaleobiology
line) and
possible
sampling-standardized
curve (red line) suggests that global
Database
plateau throughanimal(blue line).
the Paleozoic The
(corrected)
(450 empirical
to 250 Ma) curve
and (red
of the new
analysisreached
marine diversity
line)
has risen, (9,
when 14).
sectors of
what dampened
as Any
corrections
butecospace
model
congruent signal
the multiple-equilibria
for global
are imposed.
are conquered
Cor-and expan-
diversifica-
add rigor to analyses showing that sister clades Fig. 2. Patterns of marine genus diversification through the past
ies Diversity and the Role of Biotic Paleozoic, perhaps 400 itMa, toworked
the out sion models
samplingoriginally used
es- raw data,

T
climate and oceanographic and tectonic events shape larger-scale andof increases Red from Queen viewpoint
a singlePattern
ultimate because
of species ofitmicrobial
implies pri- life scale (Fig. 2, others
red to extinction.
curve); was Key evidence is apparently rection
tion must for encompass is the
clearly
independent evi-
may varypatterns regionally
in rate of evolution, timing The Global Diversification
that both
suggests that global
exponentially, marine
ever diversity
since. The
530 My, the Phanerozoic. The two lines compare current estimates from reached a possible
sampling-standardized plateau
curve
sentialwithout
(6, 7), and future investigation
here
here andare
are twotwo ways
ways of of viewing
viewing evolu-of years.
evolution, scales,
portant andinto
not itspecies
is likely
export thatand evolution
organism-level operates
processes in
to marily
3500 biotic
million controls
years ago (density
(Ma) (Fig. dependence)
1). Two mod- on present
at ordinal(Fig.and 2B). In origination
familial bothlevelsmodels, and the
but
extinction
does not (blue
through line)thesuggests
Paleozoic that (450
globaltomarine diversity
250database
Ma) and(red reached
has risen, near-modern
apparently dence for correction
increasing (5, 8–11),of
complexity although
organ-

T
globally, through thousands and millions Paleobiological studies
richness suggest
morphospace that species
occupation, Through Time the empirical (uncorrected) Sepkoski line) and sampling-
rates appear to have been density- levels some 400 Ma and there has been only modest increase since then. must determine
to biodiversity appropriate indepen-
Abiotic Factors Through Time
diversity tion,
through through
is driven the largely the by
spectacles spectacles
of either
abiotic oftheeither
factors Red a pluralistic
such asregionalclimate,orand way
global
landscape,
lineages
(3).scales,
distributions
and
oroffood
insubclades.
andsupply,
it isnovelties
evolutionary
Here,way
likely
and across
I will(3).
that globalels
A key fordiversity.
global diversification
question about the originare
explore the saturation/equilibrium model (5–7) and the ex-
termed bio-
of modern the equilibria correspond
work convincingly
saturation in dependent (5–7), at generic
which new taxa limitingorrises specific
could in The
exponentially,
standardized
di- Cm, Cambrian;
line)
ever analysis
(corrected)
suggests
since. The
C, Carboniferous;
that global
ofD,
marine
sampling-standardized
the Paleobiology
Devonian;
diversity
Database
J, Jurassic;
reached
curve(blue(blueline).
K, Cretaceous;
near-modern
isms,
more recent
increases
dent proxies
what
analyses
in the occupation
for preservation
dampened but
return a some-
and hu- of novel
congruent signal
comparative the Red
Queen or Queen
the Court
phylogenetic or Jester.
the Court
approaches The Red Jester.
offerQueen The
new insights There
evolution intoare
operatestwo broad
clade
largest-scale methodologies
a pluralistic
dynamics.
global, taxic investigations, for provide
stud- diversity There isare how two versions
today’s of the species
10 million equilibrium
arose 11), there
levels (10, versity and promotingare problems rapid recovery with empirical
Ng, Neogene; curveO,(red line) suggests
Ordovician; P, Permian; that global marineS,diversity
Pg, Paleogene; Tr, ecospace,
Silurian;reached man error; some explosive evolution
current proxies (suchwithin par-
pansion become established only by driving levels some 400 Ma and there has been only modest increase when corrections are imposed. Cor-
enton model (1) stems from Darwin,
Red Queen model (1) stems from Darwin, who ies of species who viewed evo- There are two
an outline broad methodologies
of howthrough
diversity these and time, for
taxic
other studies studies
and model,
corre- from a modeldiffering
single (8–11).
in the
ultimate The equilibrium
time
species when model
the
of microbial has
global
life key numerical assumptions
after extinction events. (11, 12), and a possible plateau
Triassic. Based on through
(6). the Paleozoic (450 to 250 Ma) and has risen, ticular
as number clades, and addition
of fossiliferous of novel clades
localities)
lution as primarily a balance of biotic pressures, of species diversity through time, taxic and phy- prevailed, among marine paleobiologists at least, others to extinction.AlternativeKeymodels evidence for is apparently
global di- since then. Cm, Cambrian; C, Carboniferous; D, Devonian; J, Ju-curve are rection dependent
themselves for sampling on is clearly es-
diversity,
viewedhere evolution
are twoasways primarily of viewing a balance of bi- phylogenetic
evolution, portant not to (4). spond to the
export The taxic approach
predictions
organism-level of the Red involves
Queen,
processes Courtto marine ecosystem
3500 million yearsbecameago (Ma) (Fig. 1).Sepkoski’s
saturated. Two mod- the background assumption of a global rassic; K, Cretaceous; Ng, Neogene; O, Ordovician; P, Permian; Pg, without the loss of precursors (9, 11, 15),
exponentially, ever since. The sampling-standardized
y be dominated
urt Jester model,
most
ized
y over different T
Through
to
shape ecosystems
model
by biotic

wasgeographic
Alice
notably
oticorpressures,
by the
factors,
mixture ofmost
a through
characterized
Queenand
the
(1)in
locally
Red
the
as in the Red
competition,
or temporal
Through
and
stems
the
Looking-Glass
overfrom
notably
both.spectacles
Queen’s
short the time
and
The two models
byCourtthescales:
RedJester.
Queen
statement
Looking-Glass
Darwin, spans,
ofit was
competition,
Queen’s
model,
either
appear the
The Red
Competition,
thatwho buttakes
“it
to
extrinsic
viewed
or abiotic factors,
character-
toand
Alice
statement
Red
operate
Queen and
predation,
allevo-
that the
in
“it such
factors
logenetic
it treating
regional species,
ing species,
other entities
pendent
evolution
entities
against
asThere and
time
(4).
Jester,The
or
outline
global
operates
areand
and
counting
twoother
taxic
and multilevel
genera,
some or
genera, in
scales,approach
counting
a
mixed models
phylogenetic
families
pluralistic
evolution of species diversity.
their
broadfactors.
itinvolves
orandfamilies
their
occurrences
methodologies
is (Table
studies
asway
likely
occurrences
(3).
1), and for a long time, and represents a classic Red Queen
treat-
as inde-

foragainst
The phylogenetic
that coupled
els for global
equilibria,
trols
studies Paleozoic,
pansion
logisticdiversification

(density
model
in
saturation/equilibrium
and
the
model (5) identified
of the macro- viewpoint because it implies primarily biotic con-
independent
dependence)
perhaps
(8–11).
Cambrian,
model
Theaon
are termedthree
(5–7)
global
third,
equilibrium
mostand of
beginning
the
diversity.
model has
the
the
ex-
in
that both origination
Further, it has
dependent
gistic model
versity
versification and
carrying capacitydiversity
rates appearspecies
out proved
(5–7),
and dence
is doubtful
to have been
a predictable
to the
promoting
limiting
much
hard to
of origination
rapid
extinction allowing
are expansionist,
to rise,

more
limit
rises
with10,
(8,
density-
export
recovery
(blue line)
11).
damping,
levels
di-theDensity
in(8–11). lo-
Cm,
extinctionterrestri-
andspeciose
global
Paleogene;
but
some
partly that
suggests an artifact
S, Silurian;
with-400curve);
Ma and it was
globalof marine
Tr,worked
there
taxonomic
Triassic.out
has been Based
atonly
scale (Fig.
diversity
on (6).
ordinal and familial
modest
depen- levels but does not work convincingly at generic signals are the
Cambrian;
rates does notcurve)
Ng, Neogene;
C, Carboniferous;
ariseslevels
or specific
O,keyOrdovician;
from
D, Devonian;
(10,extensive
11), there are
P, Permian; Pg,
J,
attempts
increase
Jurassic;
problems to
Paleogene;
K,
and other correction
2, red near-modern
reached
as to produce
since
Cretaceous;
all data
then.
sential
of which
regimes
in which
must
(6, may
have
past 500 separated.
not obviously
dent proxies
withcor- Life on land today may be as much as 25
Tr, man
My.
7), and
geologic
determine
be sofuture
happened
and
complex
biologic
appropriate
investigation
many times in
for preservation and hu-
error; some current proxies (such
indepen-

oceanographicrunningand you
tectonic can
events do,
shape to keep
larger-scale in the same
patterns place.”
regionally andtime and other factors. The phylogenetic ap- There are twocontinuing
versions of the present
equilibrium back-S, Silurian;
timesLarge-Scale
as Controls ofonfossiliferous
takes
lution all the
as primarily running you
a balance can do,
of biotic to keep
pressures, in approach
of speciesuses The Global
diversity Pattern
cladograms
through oftime,
or Diversification
moleculartaxic and treesphy- to the Pliocene
prevailed, and
among marine to the
paleobiologists at (Fig.
least, al realm, whether
preclude one considers
expansionist models plants,
becauseinsects,
they mayrect datanumerical
sets forassumptions
sampling(11, error12),(6,and7),thewhereas as diverse as life in the sea, soSpecies
it may be Diversity
through thousands and millions of years. Paleobiological studies suggest that species Through Time to model, differing after extinction events. Triassic. Based on (6). assumption of a global carrying capacity is wrong to generalize number localities)
The
riven largely the
Court
same
Jester
place.” suchThe
model (2)
Courtand
isit that
Jester model
evolution, proach
(2)supply,
is and disentangle
uses cladograms or molecular trees time, andinrepresents the timea classic when the Red global be dampened by limiting factors such as shortage ground from marine paleontolog-
A key aspects
taxicofapproach
clade histories. Clades bio- 2A). These three equilibrium levels correspond or vertebrates, because these groups seem to the multiple-equilibria and expansion models Taxic paleobiological studies have provided
diversity,a
most
by abiotic notably
factors competition,
as climate, landscape, was orcharacter-
food logenetic (4). The involves treat- for a long Queen
speciation, and extinction rarely happen except in key question about the origin of modern Alternative of foodmodels
or space, fororglobal di-
active predation, as well as by doubtful (8, 10, 11). Further, it has proved hard to ical studies to all arelife.themselves
Perhaps dependent
land and sea on
phylogenetic thatized
approaches evolution,
by the Red
offer new speciation,
Queen’s
insights into andclade
statement extinction
dynamics.rarely
to Alice in are monophyletic,
ing species, diversity is including
genera, or families
how today’s 10 allmillion
descendants
as independent
species aroseof to three sets of phyla, the Cambrian, Paleozoic,
viewpoint because it implies primarily biotic con- have radiated explosively, without diversity pla- originally used raw data, without correction (5, great deal of evidence about controls, mainly
response to versificationclimateare expansionist,
and other physical allowing Further, itpartly
factors.global an artifact
export the logistic of taxonomic
model to the scale much(Fig.more 2, redshowand otherpatterns
similar correction regimes increase
of exponential may beinso complex
happen
Throughexcept theunpredictable
in responsethat
changes“it in the
to unpredictable
physical
all the an ancestor, whereas taxa may be monophyletic life and
trols Modern, that interacted and successively teaus, particularly in thewithpastdamping,
100 million years 8–11), although more recent analyses return
familialaspecies abiotic, on species diversity. Bioticthey factors, such
Looking-Glass takes entities
Fig. 1. and from
Operation counting
a singleof their
ultimate
Red occurrences
species
Queen against
of microbial (density dependence) on global diversity.
environment, recalling the capricious behavior 1).A
species seems to
diversity that the
rise, coupled logistic model
but with- may becurve); speciose
it was terrestrial
worked realm,
out whether
at ordinal oneand considers as tonumbers
produce (8,data9, in
11), or perhaps
which geologic and biologic
re two ways of changes
viewing
running you in the canphysical
evolution, portant
do, to keep environment,
not to export
in the same recalling
organism-level
place.” processes or
timeparaphyletic,
(biotic to
and 3500
other
causation) excluding
million years ago
factors.
and Court some
The(Ma) (Fig.descendants
phylogenetic
Jester Two mod-ap- replaced There each are two other versionsthrough of thethe equilibrium
Cambrian- (My)a (10).
out predictable
Table 1.limit (8–11). Density
Macroevolutionary phenomena depen- somewhat
levels
and their but does
support dampened
for not the
either work but congruent
Redconvincingly
Queen (biotic, signal whenor Court
atintrinsic)
generic as body
signals size,
Jesterare notdiet,
(physical, colonizing
obviously
extrinsic) separated.
models. Manyor ecologi-
ability
h the spectaclesof
Thethe of Courtlicensed
either theJester
Red foolmodelof Medieval
regional or global times.
scales, Neither
and it is likely that uses els for global diversification are termed the
trees Genus
the
or the Court Jester. capricious
Thewas Red Queen behavior evolution of (2)the islicensed
that
operates in a and fool
evolution,
pluralistic of of
proachthe
(abiotic
way (3). ancestor.
causation) Comparative
cladograms
models or
at macroecological
molecular
differ-
saturation/equilibrium model (5–7) and the life
to Ordovician
ex-span
model, differing and in the Permo-Triassic
time when the intervals,
global Resolution
dence couldbetween
of origination andthe
fit either equilibrium
worldview,
extinction and models,
ratessodoes are noted
not asor corrections
“multilevel
specific levels are (10,
mixed.” imposed.11), thereCorrection
are problems for sam- with cal Life specialization,
on land today appear mayto havebe aslittle much effect
as 25on
model
speciation, andproposed
extinction asrarelyexclusive, happen except both in
Medieval times. evo-Neither model was proposed as for studies
ent studies add
geographic rigormodel to analyses
and temporal showing
scales that sisterhas reaching higher equilibrium levels after each
(3-6 My) and between these and expansionist models, plingnumerical
is clearlyassumptions
essential (6,(11, 7),12),
and andfuture inves- the diversity of asmodern organisms, although
Temporal scale

ms from Darwin, who viewed There are two broad methodologies pansion (8–11). The equilibrium model preclude expansionist models because they may key the back- times as diverse life in the sea, so it may be
Darwin
response
of biotic to
and Van Valenspecies
unpredictable (1) allowed
changes infor extrinsic
theValenphysical Court Red Queen Court Jester Multilevel mixed
marily a balance exclusive,
influences and
pressures,
on both ofDarwin
evolution in andprimarily
diversity
their Van through time,
biotic,(1)taxic clades
(A).
and phy-
Fig.
Themay
1.
Red vary
Operation
Queen
prevailed, inamong
rate ofprevail
maymarine
of Red evolution, at timing
paleobiologists
Queen of long-term replacementJester
at least, event. The second model might
be seem by
dampened straightforward,
limiting factorsbut suchthe solution ground
as shortage tigationassumption
must determine of a global appropriate
carrying capacityindepen- is abundance
wrong to generalize and r-selected from marinelife-history charac-
paleontolog-
competition, environment,
and it was character- recalling logeneticthe capricious
(4). The taxic approachbehavior involves treat- for
organismic and a long time, and
species levelrepresents
on short a classic Red Queen
Red Queen’s Red
allowed Queen for extrinsic
views. influences on evolution in increases
(biotic causation) in species richness
and Court and
Jester morphospace
A Species (6, 7) identifies a single equilibrium level from depends
of food oron adequate
Interspecific
space, or active assessment
predation,ofasthe
competition
well quality
Waxing
as
and waning
by doubtful
of cladesfor
dent proxies preservation
in association
(8, 10, 11).
with and humanVicariance
Further, it has proved hard error;
to teristics
and dispersal
ical studies (short to gestation
in major
Perhaps landlitter
all life. period,
phylogenetic splitslarge (17)
andsize,
sea
statement
of the to Alice
licensed in
fooling ofRedspecies,
Medieval genera, times.or families
Neither as independent
time scales,viewpoint
whereas because it implies
the Court primarily biotic con-
Jester life span tectonic and oceanographic events (2, 17)
Looking-Glasstheir that primarily
“it
Species takes all biotic,
the entities Queen
and countingviews. their occurrences occupation,
(abiotic
against causation)
trols and distributions
(density models
dependence)at of
differ-
on evolutionary
global diversity. Genus the early Paleozoic, perhaps 400 Ma, to the of the fossil
climate record.displacement
andCharacter
other The long-term
physical saturation
factors. Further, it some
export current
the proxies
logistic (such
model to as number
the much of fos-
more and
show short
similarinterbirth
patterns intervals)
of sometimes
exponential corre-
increase in
model
inSpecies wasdiversity
proposed
diversity
in as a Red
in and a exclusive,
Red
Queen world
Queen and world
de- holds his own on larger scales. The
both noveltiesap- across lineages andscales
subclades. Here,
(1-2 My)
life span
present (Fig. 2B). In both models, the equilibria model thatfor global diversification (Fig. may
Mass extinctions and smaller extinction events
2, triggered
blue siliferous localities)
Latitudinal diversity gradient (22–24)
can do, to keep the same place.” time other factors. The phylogeneticent geographic There and aretemporal
two versions of the equilibrium (3-6 My) seems the coupled logistic model be by speciose
extrinsicterrestrial asare
suchrealm, themselves
whether onedependent considers late withnumbers
species high species (8, richness
9, 11), (16). or perhaps they
Temporal scale

pends primarily on intrinsic factors, such as body stippled green shape shows an timeareawhen the global Red causes eruptions,
Darwin
depends is that and Van Valen
primarily on (1)uses
intrinsic allowed factors, for extrinsic
orsuch as I(A). willThe
ester model (2) evolution, proach cladograms or molecular trees toexplore
model,
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Apparent climate change, anoxia, impact (10, 11)
size,
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and their support for either the Red Queen (biotic, intrinsic) or Court Jester (physical, extrinsic) models. Many
body in
ability size,
to hard breadth
times. of aphysiological
In Court Jester tolerance,
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Species(100 ky)
from scale effect Evolutionary arms races (1) turnovers, originations, and extinctions
“multilevel
Occupation of new ecospace (25)
Red Queen views. Fig. 1. Operation of Red Queen identified
npredictable changes the physical erroneously, but these are could fit either worldview, and so are noted as mixed.”
orcapricious
recalling thecies adaptability
diversity behavior to hardontimes.
depends fluctuations In a Court in Jester likely
climate, time
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whereas the Court Jester
of spatial averaging of
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Fig. 1. Operation of Red Queen (biotic causation) in response to physical perturbations– termed
Species Neither diversity(biotic in a causation)
Red Queen and world
Court Jester de- holds his own on larger scales. The (1-2 My) Locality Average Biotic Entire “coordinated stasis” or “turnover pulse” hypothesis
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life span shape shows an area ferent geographicRed and temporal scales (A). The Red
in climate,
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ability totimes,
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scale Jester holds tectonic and oceanographic events (2, 17)
iews. ferent ways
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Traditionally,
scales, whereas what could
biologists
Court Jester rections, life spanand so cancel each other, Incumbency advantage
Character displacement Mass
Lack of evidence for a global carrying capacity and
extinctions and smaller extinction events
Declining global extinction rates through time (1, 5)
Latitudinal diversity gradient (22–24)
cies diversity depends on fluctuations in climate, likely (1-2theMy) result of spatial averaging of his own on larger scales.
Locality Average Biotic The stippled green
Entire shape
perhaps
iversity in a Red
have Queen
tended be called
world
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de-
to think holds
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(3, 24) equilibrium levels (8, 10)
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ly on intrinsiclandscape,
factors, such and as body supply. In reality, of course, regional responses to climate change species region/ continent Lack ofby extrinsic causes
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of the great as eruptions, Onshore-offshore patterns and disturbance (3)
of physiologicalTraditionally,
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tolerance, biotic biologists
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geologiststo think
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aninarea
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physical pertur- Apparent B identified erroneously, rangebut these climate are likely the re- climatefaunas”
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where Red Queen effects might be Physical-environmental Red Queen zone
adifferent
Court
d times. In a Court Red Jester Queen,
Jester,
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calledthese fac-are
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Species turnovers, originations,
richness–energy relationshipand
(18,extinctions
19) Occupation
Resource of new are
use: stenotopes ecospace (25) than
more speciose
tors
depends on fluctuations way,
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of thegeologists
climate, likely theinresult
divergence a Court
between
of spatial Jester,
the
averaging ex-
Red of may rections,
elicit biotic responses
and so cancel
Locality each
along the
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other complexscale physical pertur- in response to physical perturbations– termed eurytopes (29, 30)
multilevel mixed model. Traditionally, biologists red line separating Red Queen
species and
trinsic, physical factors way.
d food supply.QueenIn reality, of course, regional responses to climate change region/ continent(3-6 My)
Temporal scale

and Court Jester world views may depend suggesting no controlling effect range ofclimate
the bations that may be in opposite directions, and so Inverse relationship between global temperature and
“coordinated stasis” or “turnover pulse” hypothesis
have tended to think in a Red Queen, Darwinian,
might prevail in different ways and at and other complex physical pertur- Court Jester outcomes (B). The usage
Much of the divergence between the driveRed zone cancel each other, suggesting Court no controlling effect biodiversity (21)
s, what couldon perhapsscale
intrinsic, (2)
be biotic
called (Fig.factors
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bationsBiotic
way, thatand interactions
may geologists
be in opposite in di-a here physical environment on evolution. (2, 29, 30)
is the microevolutionary Red Queen, scale B Speciesof the physical environment Jester on evolution. Physical- Lack of clear correlation of species richness with
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body probability
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o think in a Reddepend Queen,on
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suggesting noBiotic
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may elicit biotic responses along the Genus
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evolution. Queen that posits constant ex- life span
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ic factors way, and geologists in a
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by B line separating Red Queen and
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disruptions risk, a view that has been largely and Court Jester Incumbency advantage Lack of evidence for a global carrying capacity and Declining global extinction rates through time (1, 5)
extrinsic, physical factors way.
Court Jester outcomes (B). The usage Milankovitch Red outcomes (B). The usage here is
the divergencefailure
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life span Scale the ky)
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www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009 729
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Earth Sciences,at
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Bristol,
macroevolutionary 10
Bristol
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BS8 1RJ,
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E-mail: mike.benton@bristol.ac.uk Milankovitch Red eurytopes (29, 30)
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728 6 FEBRUARY 2009 VOL 323
Less
SCIENCE www.sciencemag.org
More
Less More
Department of Earth Lack of clear correlation of species richness with
Earth Sciences, University of Bristol, Bristol Sciences, University of Bristol, Bristol
Environmental scale
BS8 1RJ, UK. E-mail: mike.benton@bristol.ac.uk Environmental scale body size or other biotic factors (16)
mail: mike.benton@bristol.ac.uk

22 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 23

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 their continuing diversification in the Late Jurassic shifts should mainly occur low in a clade’s history: Court Jester worldviews. If the majority of diver-
and Cretaceous was mainly indistinguishable from Clade shapes vary from bottom-heavy to top- sification shifts are coordinated, and associated
a random walk. In particular, dinosaurs did not heavy, and diversification shifts may be concen- with particular climatic, tectonic, and geographic
participate in the Cretaceous Terrestrial Revolu- trated low (dinosaurs and bats) or high (insects drivers, then the Court Jester model of macro-
tion, some 130 to 100 Ma, when flowering plants, and ants) in a clade (26). evolution would prevail. This would link most
leaf-eating insects, social insects, squamates, and In the future, the identification of diversification increases in species diversity to particular large-
many other modern groups radiated substantially. shifts across numerous taxa may provide evidence scale radiation events, such as the Cretaceous Ter-
restrial Revolution (26), or recoveries after mass
A
245.9 237 232.5 228 203.6 199.6
extinctions. If, on the other hand, the majority of
diversification shifts are unique to particular clades,
and upland habitats of the later Paleozoic when macroevolution, and dinosaurs provide a classic Comparing Sister Taxa macroevolution. Viewed close up, evolution is
Anisian Lad Crn Norian Rh. EJ and not coordinated temporally with others, then land animals first burrowed, climbed, and flew, example. The standard view was that dinosaurs A powerful element of the comparative phyloge- all about biotic interactions in ecosystems (Red
the Red Queen worldview might be considered.
PTEROSAURIA through the introduction of herbivory, giant size, originated in the Late Triassic, some 230 Ma, by netic approach to species diversity through time Queen model), but from further away, the large
Comparing Sister Taxa
“Dinosauromorphs”
A powerful element of the comparative phyloge- endothermy, and intelligence among vertebrates, a process of competition in which they prevailed is the opportunity to compare sister taxa. Sisters patterns of biodiversity are driven by the physi-
ORNITHISCHIA Fig. 3. Phylogenetic
netic approach to species diversity relationships
through time and mor- and the great blossoming of flowering plants over their precursors, the crocodile-like crurotar- arose from a single ancestor, and so their trajec- cal environment (Court Jester model).
is the opportunity to compare sister taxa. Sisters
Dinosauria phospace occupation fortheirTriassic archosaurs.
(with associated vast expansions in diversity of sans and others, because of superior adaptations. tories occupy the same amount of time, and they
SAUROPODOMORPHA
arose from a single ancestor, and so tra-
THEROPODA
(A)
jectoriesFramework
occupy the same amountphylogeny of time, and for Triassic cru-
PHYTOSAURIA
they started with the same genotype and phe-
rotarsans scaled tosubsequent
the Triassic time scale. plant-eating and social insects and modern ver- A comparative phylogenetic study (28) shows, started with the same genotype and phenotype.
Crurotarsi
AETOSAURIA
notype. Any similarities in their evo-
tebrates) during the Cretaceous Terrestrial Revo- however (Fig. 3), that the Dinosauria expanded Any similarities in their subsequent evolution References and Notes
Numbers at top refer to millions of years
lution probably reflect this phylogenetic signal of
a common origin, but differences reflect inde- 1. L. M. Van Valen, Evol. Theory 1, 1 (1973).
CROCODYLOMORPHA
before theof their
present; gray bars represent the lution 100 Ma (26). in two steps, one after an extinction event 225 probably reflect this phylogenetic signal of a
2. A. D. Barnosky, J. Vert. Paleont. 21, 172
pendent aspects separate histories.
“Rauisuchids”

POPOSAUROIDEA
Comparisons of sister taxa have allowed tests
observed
of the resource-use durations
hypothesis (29),of thatmajor
general- lineages; ver- The other mode of species increase globally Ma that removed dominant herbivores, and the common origin, but differences reflect indepen- (2001).
ORNITHOSUCHIDAE tical dashed lines denote two extinction
ists are less speciose and have longer species
durations than specialists. Specialists divide the
or regionally is by niche subdivision, or increas- second following the end-Triassic extinction 200 dent aspects of their separate histories. 3. D. Jablonski, Evolution 62, 715 (2008).
events, at theintoCarnian-Norian
physical environment small patches, each
occupied by a species, and each probably more
and Triassic- ing specialization. This is hard to document be- Ma that removed most of the crurotarsans. Dino- Comparisons of sister taxa have allowed tests 4. A. Purvis, Annu. Rev. Ecol. Syst. 39, 301
B
Jurassic boundaries;
subject to environmental arrowheads
crises than their gener- indicate cause of the number of other factors that vary sauria remained at moderate diversity and low of the resource-use hypothesis (29), that gener- (2008).
lineages that
alist relatives. Classic survived
examples the
in support
resource-use hypothesis come from studies of Ne-
of latter
the event. Lad,
between ecosystems through time. However, disparity, and at lower disparity than the cruro- alists are less speciose and have longer species 5. J. J. Sepkoski Jr., Paleobiology 10, 246 (1984).
Ladinian;
ogene mammalsCrn, Carnian; Rh, Rhaetian; EJ, Early 6. J. Alroy et al., Science 321, 97 (2008).
mean species number in communities (alpha di- tarsans they supposedly out competed, during durations than specialists. Specialists divide the
0.12 (29). For example, two antelope
subgroups, the tribes Alcelaphini and Aepycerotini,
Jurassic.
diverged 6 to (B)8 Ma.Empirical morphospace for Late 7. J. Alroy, Proc. Natl. Acad. Sci. U.S.A. 105,
versity) has increased through time in both ma- the 25 My between the events, suggesting that physical environment into small patches, each
0.06 The former is now highly
Triassic
speciose, witharchosaurs,
some 7 living and 25 based on the first two
extinct spe- 11536 (2008).
Principal coordinate 2

rine (15, 25) and terrestrial (10) systems, even there was no insistent competition driving other occupied by a species, and each probably more 8. T. D. Walker, J. W. Valentine, Am. Nat. 124,
0 cies, and the latter is represented by two species,
Dinosaur morphospace principal
only one, the impalacoordinates.
Aepyceros, surviving. Large The circles, dino-
-0.06
saurs; ovals, pterosaurs;
slowly evolving Aepycerotini consists of few
squares, poposau- though niche subdivision may be less important groups to extinction but rather that the dinosaurs subject to environmental crises than their gen- 887 (1984).
-0.12
species at any time, and each of those is long
roids; hexagons,
lived, whereas the speciosephytosaurs;
Alcelaphini consistsstars, aetosaurs; than occupation of new ecospace in increasing occupied new ecospace opportunistically, after it eralist relatives. Classic examples in support of 9. M. J. Benton, Science 268, 52 (1995).
of many short-lived species. The ecological 10. M. J. Benton, B. C. Emerson, Palaeontology
-0.18 Pterosaur morphospace
crosses, crocodylomorphs;
habits of both clades differ: The impala has a smaller black biodiversity. Further, morphological complexity had been vacated. the resource-use hypothesis come from studies 50, 23 (2007).
dots, “rauisuchids”;
broad, generalist diet, whereas the larger
specioseblack
al- dots, nondi- may be quantified, and a comparative study of A further study on Dinosauria explored the of Neogene mammals (29). For example, two
-0.24
celaphines show more dietary specialization. In 11. S. M. Stanley, Paleobiology 33, S1 (2007).
-0.3
nosaurian
wider studies of manydinosauromorphs,
clades of Neogene African Scleromochlus.
crustaceans shows, for example, that complexity subsequent evolution of the clade (26). Classic antelope subgroups, the tribes Alcelaphini and 12. J. Alroy, Evol. Ecol. Res. 6, 1 (2004).
and South American mammals (30), the resource-
Crurotarsan morphospace
Based onwas (28). 13. G. J. Eble, Geobios 32, 223 (1999).
-0.36 use hypothesis supported, and some subsidiary
has increased many times in parallel in separate views that the dinosaurs arose with a flourish, Aepycerotini, diverged 6 to 8 Ma. The former
14. M. J. Benton, Geol. J. 36, 211 (2001).
predictions confirmed: Specialists are more com-
mon than generalists, carnivores include more lineages (27). and then finally gave way in the Cretaceous to is now highly speciose, with some 7 living and
-0.24 -0.16 -0.08 0 0.08 0.16 0.24 0.32 generalists than herbivores, and there are more 15. R. K. Bambach, A. H. Knoll, J. J. Sepkoski Jr.,
Principal coordinate 1 specialists in habitats that underwent recent en- the superior mammals, or that they dwindled to 25 extinct species, and the latter is represented Proc. Natl. Acad. Sci. U.S.A. 99, 6854 (2002).
Phylogenetic Studies of Clade Histories by two species, only one, the impala Aepyceros,
vironmental change (tropical rain forests and
Fig. 3. Phylogenetic relationships and morphospace occupation for Triassic archosaurs. (A) Framework deserts). The resource-use model then stresses extinction because of “racial senility,” had long 16. N. J. B. Isaac, K. E. Jones, J. L. Gittleman, A.
Species are not randomly distributed; they have been abandoned. The dinosaurs seemed to be surviving. The slowly evolving Aepycerotini
the role of climate and tectonic movements in
phylogeny for Triassic crurotarsans scaled to the Triassic time scale. Numbers at top refer to millions of years
before the present; gray bars represent the observed durations of major lineages; vertical dashed lines denote determining species diversity rather than biological Purvis, Am. Nat. 165, 600 (2005).
Geographic and tectonic history has gener-
two extinction events, at the Carnian-Norian and Triassic-Jurassic boundaries; arrowheads indicate lineages that tween temperature and biodiversity on the glob-
controls such as competition and predation.
an evolutionary history, and so occur as twigs radiating actively in the Cretaceous, with many consists of few species at any time, and each 17. D. E. Wildman et al., Proc. Natl. Acad. Sci.
U.S.A. 104, 14395 (2007).
survived the latter event. Lad, Ladinian; Crn, Carnian; Rh, Rhaetian; EJ, Early Jurassic. (B) Empirical morphospace
ated patterns of species diversity through time.
for Late Triassic archosaurs, based on the first two principal coordinates. Large circles, dinosaurs; ovals, for both marine and terrestrial organisms
al scaleOutlook on a great phylogenetic tree. Studying species new clades appearing through their last 55 My, of those is long lived, whereas the speciose Al-
pterosaurs; squares, poposauroids; hexagons, phytosaurs; stars, aetosaurs; crosses, crocodylomorphs; smaller Paleontologists and evolutionary ecologists have 18. G. Hunt, T. M. Cronin, K. Roy, Ecol. Lett. 8,
The slow dance of the continents as Pangaea
black dots, “rauisuchids”; larger black dots, nondinosaurian dinosauromorphs, Scleromochlus. Based on (28). (21), where generic
debated species diversity and independently. richness were
largely familial as members of clades is a fruitful approach to and especially in their final 15 My. The new celaphini consists of many short-lived species. 739 (2005).
broke up during the www.sciencemag.org
past 200 My has affected
SCIENCE VOL 323
relatively low during warm “greenhouse”
6 FEBRUARY 2009 731
phas- understanding the drivers and controls on spe- study (26) shows that most diversification shifts The ecological habits of both clades differ: The 19. G. G. Mittelbach et al., Ecology 82, 2381
modern distribution patterns. Unique terrestrial es of Earth history, coinciding with relatively ciation. Key questions include (i) Do species (departures from ERM assumptions) fall in the impala has a broad, generalist diet, whereas the (2001).
faunas and floras, notably those of Australia and high origination and extinction rates. diversify early in a clade’s history? (ii) How do first one-third of the history of the clade and that speciose alcelaphines show more dietary spe- 20. D. N. Schmidt, H. R. Thierstein, J. Bollmann,
South America, arose because those continents A much-studied manifestation of energy and diversity and disparity (variance in characters their continuing diversification in the Late Juras- cialization. In wider studies of many clades of R. Schiebel, Science 303, 207 (2004).
21. P. J. Mayhew, G. B. Jenkins, T. G. Benton,
were islands for much of the past 100 My. Fur- temperature gradients is the latitudinal diversity or morphology) covary? (iii) Do major lineages sic and Cretaceous was mainly indistinguishable Neogene African and South American mammals
Proc. R. Soc. London B. Biol. Sci. 275, 47
ther, major geologic events such as the forma- gradient (LDG), namely the greater diversity of within a clade follow similar, or different, pat- from a random walk. In particular, dinosaurs (30), the resource-use hypothesis was support- (2008).
tion of the Isthmus of Panama have permitted life in the tropics than in temperate or polar re- terns, and if different, why? (iv) Do evolutionary did not participate in the Cretaceous Terrestrial ed, and some subsidiary predictions confirmed: 22. G. G. Mittelbach, Ecol. Lett. 10, 315 (2007).
the dispersal of terrestrial organisms and have gions, both on land and in the sea. There are two radiations follow the acquisition of new charac- Revolution, some 130 to 100 Ma, when flow- Specialists are more common than generalists, 23. D. Jablonski, K. Roy, J. W. Valentine, Science
split the distributions of marine organisms. A explanations (22): (i) the time and area hypoth- ters or emptying of ecospace? (v) How do major ering plants, leaf-eating insects, social insects, carnivores include more generalists than herbi- 314, 102 (2006).
24. J. W. Valentine, D. Jablonski, A. Z. Krug, K.
classic example of vicariance is the fundamental esis, that the tropical belt is older and larger than clades of apparent competitors interact over long squamates, and many other modern groups radi- vores, and there are more specialists in habitats
Roy, Paleobiology 34, 169 (2008).
division of placental mammals into three clades, temperate and polar zones, and so tropical clades spans of geologic time? and (vi) How do sister ated substantially. There is no geometric reason that underwent recent environmental change 25. R. K. Bambach, A. M. Bush, D. H. Erwin,
Edentata in South America, Afrotheria in Africa, have had longer to speciate, or (ii) the diversifi- clades vary in species diversity and why? that diversification shifts should mainly occur (tropical rain forests and deserts). The resource- Palaeontology 50, 1 (2007).
and Boreoeutheria in the northern hemisphere, cation rate hypothesis, that there are higher rates For such analyses, the ideal is a complete low in a clade’s history: Clade shapes vary from use model then stresses the role of climate and 26. G. T. Lloyd et al., Proc. R. Soc. London B.
presumably triggered by the split of those conti- of speciation and lower rates of extinction in the species tree, a phylogenetic tree that contains bottom-heavy to top-heavy, and diversification tectonic movements in determining species di- Biol. Sci. 275, 2483 (2008).
27. S. J. Adamowicz, A. Purvis, M. A. Wills, Proc.
nents 100 Ma (17). Other splits in species trees tropics than elsewhere. There is geological and all species living and extinct, plotted accurately shifts may be concentrated low (dinosaurs and versity rather than biological controls such as
Natl. Acad. Sci. U.S.A. 105, 4786 (2008).
may relate to dispersal events, or there may be paleontological evidence for a mixture of both against geologic time (4). Simple to say; hard bats) or high (insects and ants) in a clade (26). competition and predation. 28. S. L. Brusatte, M. J. Benton, M. Ruta, G. T.
no geographic component at all. hypotheses (23, 24). to achieve. More commonly, incomplete trees In the future, the identification of diversifi- Lloyd, Science 321, 1485 (2008).
Species richness through time may correlate Species diversity may increase by the occu- have been used, with the risk of error in calcu- cation shifts across numerous taxa may provide Outlook 29. E. S. Vrba, Am. J. Sci. 293A, 418 (1993).
with energy. The species richness–energy re- pation of new ecospace. The number of occu- lations of evolutionary rates or comparisons of evidence for the relative importance of the Red Paleontologists and evolutionary ecologists have 30. A. M. Bofarull et al., BMC Evol. Biol. 8, 97
lationship (18) posits correlations with evapo- pied guilds, that is, broad ecological groupings subclades. In paleontology, it has proven much Queen and Court Jester worldviews. If the ma- debated species diversity largely independently. (2008).
31. S. Finnegan, J. L. Payne, S. C. Wang,
transpiration, temperature, or productivity, and of organisms with shared habits, has increased easier to work with higher taxa such as genera or jority of diversification shifts are coordinated, The realization that the Red Queen and Court Paleobiology 34, 318 (2008).
studies of terrestrial and marine ecosystems in several steps through time, from 20 in the families because species fossil records are less and associated with particular climatic, tectonic, Jester models may be scale-dependent, and that 32. Thanks to S. J. Braddy, P. C. J. Donoghue, D.
have shown that these factors may explain as early Paleozoic to 62 in post-Paleozoic ma- complete than those of higher taxa, and yet it and geographic drivers, then the Court Jester evolution may be pluralistic (3), opens oppor- Jablonski, A. Purvis, M. Ruta, D. N. Schmidt,
much as 90% of current diversity, although rela- rine faunas (25). Further, marine animals have is not clear how higher-level patterns relate to model of macroevolution would prevail. This tunities for dialog. Taxic studies in paleontol- and anonymous referees for comments and to
tionships between species diversity and produc- shown several step increases in tiering, the abil- those at species level. Many key questions can would link most increases in species diversity ogy continue to have great value in highlighting S. Powell for drafting the figures. Supported by
the Natural Environment Research Council and
tivity change with spatial scale (19). Over long ity to occupy and exploit different levels in the be tackled by comparing a real tree to a hypo- to particular large-scale radiation events, such correlations between species richness and other the Royal Society.
time spans, there are strong correlations between habitat: At times, burrowers have burrowed thetical tree that follows an equal-rate Markov as the Cretaceous Terrestrial Revolution (26), or factors, but comparative phylogenetic methods
plankton morphology and diversity and water deeper, and reef-builders have built taller and (ERM) model, equivalent to tree growth after a recoveries after mass extinctions. If, on the other will illuminate questions about clade dynam-
temperature: Cooling sea temperatures through more complex reefs. Analogous, if even more random walk, where equal chances of speciation hand, the majority of diversification shifts are ics, species richness, and the origin of novelties.
the past 70 My, and consequent increasing ocean dramatic, expansions of ecospace have occurred and of extinction are shared by all species (4). unique to particular clades, and not coordinated Further, methods are shared by paleontologists
stratification, drove a major radiation of Fora- on land, with numerous stepwise additions of Major biotic replacements, where one clade temporally with others, then the Red Queen and neontologists, and this allows direct com-
minifera, associated with increasing body size new habitats, from the water-margin plants and replaces another, have been a focus of debate worldview might be considered. munication on the patterns and processes of
(20). More widely, there is close tracking be- arthropods of the early Paleozoic to the forests about the roles of competition and progress in

24 25
 REVIEW theories of the process (8, 11). I leave out dis- Speciation
cussion of sympatric
Under
instead identifythis the
SPECIALSECTION
and allopatric speciation but
Darwinian
likelihoodperspective, of ecologicallink- and once again receiving attention. The two most again theBoth models
parasitic lampreysof speciation,
have evolved ecologi-into non- A Gambusia way becau
Evidence for Ecological Speciation
41. D. Jablonski, Evolution 62, 715 (2008).
42. R. J. Whittaker, K. A. Triantis, R. J. Ladle, J. Biogeogr. 35,
52. O. Seehausen et al., Nature 455, 620 (2008).
53. R. Lande, Genetics 128, 443 (1991).
ing speciation
mutation-order with
speciation adaptation when
61. R. C. Albertson, J. T. Streelman, T. D. Kocheer, J. Hered.
straightforward,
flow. 94,I ignore
291 (2003). requiring onlyaaspecial
reinforcement,
was
there relatively
test of whether
is gene
type of
general hypotheses involving selection are parasitic
ecological and mutation-order speciation. Eco- streams,
cal and mutation-order,with
forms...correlated are theoretically
where a suitable food supply in the way
plausible, and only data can determine
life in small ulations d
mutations
of large fish is scarce or seasonal” (12). When cor- order. Div
and Its Alternative
977 (2008).
43. R. Gillespie, Science 303, 356 (2004).
44. J. Todd Streelman, P. D. Danley, Trends Ecol. Evol. 18,
54. D. A. Joyce et al., Nature 435, 90 (2005).
55. G. Fryer, Environ. Biol. Fishes 45, 109 (1996).
56. J. W. Valentine, D. Jablonski, in Evolution, Time and
phenotypic
62. K. Schwenk,
natural
caused
mating London
selection
by
differences
N. Brede,
natural
Ser. B 363,
reproductive
thought
selection.
between
B. Streit,
to favor
isolationFor
2805 (2008).
Philos.species
once
63. D. Garant, S. E. Forde, A. P. Hendry, Funct. Ecol. 21, 434
Trans. R. Soc.
stronger
example,postzygotic
were
pre-
at the
logical speciation is defined as the evolution related their
of reproductive isolation between populations is unlikely
with
key is to
relative
to figure
importance
environmental factors,insuch
out bychance;
result from
nature. The
repetition
whichenvironmental
mechanism
chastic bu
from gene
126Schluter
(2003). Space, R. W. Sims, J. H. Price, P. E. S. Whalley, Eds. American
isolation
(2007). hasAssociation
evolved. I also for the ignoreAdvancement
speciation by of reproductive
by divergent natural selection arising from dif- selection pressures must isolation firstbeevolved
therefore the cause(3). of both smal
Dolph
45. D. Ackerly, D. Schwilk, C. Webb, Ecology 87, S50 (2006). (Academic Press, London, 1983), pp. 201–226. Science
polyploidy, 1939
64. O. Seehausen, evenspeciation
though 16,symposium
Curr. Biol.selection R334 might
(2006).be [the last
crucial ferences between ecological environments (2, speciation.
Once “As result ofgenetic
the aearliest our recentdifferences
studies on infinite) p
46. C. E. Parent, B. J. Crespi, Evolution 60, 2311 (2006). 57. C. O. Webb, D. D. Ackerly, M. A. McPeek, M. J. Donoghue, in major
65. symposium
theC.early Voyage on
Darwin,stages. of thespeciation
Boogle (Collier, before Newthe York,bio- 8, 9, 14). It predicts that reproductive isolation fishes...weight
have accumulated is constantly between
being addedpopulationsto the can be ec
Natural
47. J. A. selection
Coyne, T. D.commonly drives the origin
(2000). of species, Annu.as Darwin initially
Syst. 33,claimed. Mechanisms of mutation-
Price, Evolution 54, 2166 Rev. Ecol. 475 (2002). logical1909), p. 383.concept (7)], an extensive com-
species should evolve between populations adapting to theory by that
either speciation
process, is...under the rigidmutations
subsequent control of
speciation
48. J. B. Losos, by D. selection fall into
Schluter, Nature 408,two847 broad
(2000). categories: 58. ecological
J. J. Wiens, C.and mutation-order.
H. Graham, Annu. Rev. Ecol. Under 66. We thankand
Syst. 36, 519 Speciation A. Birand,
AdaptationR. Glor, A.from Harrison, L. Harmon, the environment” (12). However, this case is only ecology d
49. D. Lack,speciation,
Darwin’s Finches (Cambridge is Univ. Press, by divergent(2005). parative and biogeographic
D Jablonski, L. Mahler, C. Marshall, studyand showcased
the anonymous in- contrasting environments but not between pop- referringmight beorigin
favored in one population
ecological divergence driven natural selection between environments, Darwin to Dobzhansky to the of morphological species. gence as s
Cambridge, 1947). 59. S. Skulason, T. B. Smith, Trends Ecol. Evol. 10, 366
whereas under mutation-order speciation, divergence occurs when different mutations arise and stances in
reviewers which
for usefulderivedcomments. morphological
Supported by the and NSFlife ulations adapting to similar environments. The The and turning
not the other
point because studies
for speciation of epistatic came evolution
50. U. Dieckman, M. Doebeli, J. A. J. Metz, D. Tautz, Adaptive
are fixed in separate
(1995). history
Appreciation
(grantforms ofthe
of
DEB-0519777) fishes had
connection
and thearisen
NIH betweenoverGM56693).
(grant and over
adapta- basic idea has been around for a while (7), al- withinteractions
the modern concept with geneticof speciation background
“Species ductive iso
Speciation (Cambridgepopulations adapting
Univ. Press, Cambridge, to similar60.
2004). selection pressures.
H. D. Bradshaw, D. W.Tests
Schemske,of parallel
Nature 426, evolution
176
of51.reproductive again
tion andfrom the
speciation same ancestral
began withtype Darwin (12). The
when re-a though it was tested only recently. The agents of separation
(10). Hence, is defined epistasis,
as a stage including
of the evolu- that tion of eco
U. K. Schliewen,isolation, trait-based
D. Tautz, S. Pääbo, Nature 368, assortative
629 (1994). mating, and reproductive isolation by active
(2003). 10.1126/science.1157966
selection have demonstrated that ecological speciation is a common means by which new species peated,
morphological parallel origin
concept of
of nonparasitic
species largely lampreypre- producing
divergent selection are extrinsic and can include tionary process Dobzhansky-Muller
at which physiologicalincom- isolat- B Mimulus postzygot
in streams
vailed. In Onfrom the Originthe same migratory,
of Species, Darwin parasitic
wrote ing mechanisms become
abiotic and biotic factors such as food resources, patibilities in hybrids between speciesdeveloped” (6) (here, Specia
arise. Evidence for mutation-order speciation by natural selection is more limited and has been “physiological” is interpreted to mean evolved tragenomi
best documented by instances of reproductive isolation resulting from intragenomic conflict. ancestor
that “I look at thethat
showed term“Again species, and asagain the
one arbitrarily para- climate, habitat, and interspecies interactions reproductive
(3), can result from either ecological
isolation between populations, as
or otic drive
given
sitic
theories forofthe
lampreys the sake
have
process ofevolved
convenience
(8, 11). into
I to aout
nonparasitic
leave setdis-of such as disease, competition, and behavioral in- distinct
mutation-order speciation.
However,
REVIEW we still have not identified all aspects of selection, and identifying the underlying genes from geographical barriers to interbreed- sterility (F
individuals
forms...correlated
cussion of sympatricclosely resembling
withand lifeallopatric each
in small other...”
speciation and
streams, but terference. Ecological speciation can lead to the ing). Subsequently,
Speciation can be rapid
species were under
definedboth as mutation-
for reproductive isolation remains challenging.
“The
where
instead amount
a identify
suitable of difference
foodlikelihood
the supply is oneinofthevery way
ecologicalimportant
of largeand evolution of any type of reproductive isolation, “groups
speciation models,natural
of interbreeding because alleles that
populations are cause, by c
Evidence for Ecological Speciation criterion in settling whether(12). two forms should be

II
fish is scarce
mutation-order or seasonal”
speciation when When there correlated
is gene including premating isolation, hybrid sterility, are driven to fixation
reproductively by natural
isolated from other selectionsuch tions cau
tttook evolutionary biologists nearly 150 years, ries: ecological
took evolutionary biologists nearly 150 would nevertheless be advantageous in both of with speciation and mutation-order ranked as species
flow. environmental
I ignore reinforcement, or varieties”
factors, such (1).
a special Under
repetition this
type of is groups” (7). From this point
and intrinsic hybrid inviability as well as extrin- in both cases. However, under the mu- on, the study of countering

and Its Alternative

but
origin
at last
years, butwe can we
at last agreecanwith agreeDarwin
with that Darwinthe speciation.
their environments. Ecological
of species, “that mystery of mysteries” evolution of reproductive isolation between pop- sufficiently
that the origin of species, “that mystery of these two categories of mechanism for the ori- selection
Thespeciation refers to the
relative importance of view,
unlikely
natural speciation
to result
selection is thought
defined
from chance;
many differences
pressures must
mating reproductive
as
to the
therefore
isolation
favoraccumulation
environmental
between
stronger pre-
oncebepostzygotic popula-
the cause
of speciation was the study of the evolution of
sic, ecologically based pre- and postzygotic iso- reproductive
tation-order
if present,the
lation. Speciation by sexual selection is ecologi- understanding
process,
would
the
be favored
link between
same
isolation (3). Progress up to then in
alleles,
in every
morphological
the same i
Speciation
mutation-o
(1), really does occur by means of natural selection ulations or subsets of a single population by ad- tions to warrant their Iclassification as separate
mysteries”
Dolph Not Schluter(1), really does occur by means of gin of species in nature is unknown. of speciation. “As a result of our recent studies
isolation has evolved. also ignore speciation by cal speciation if ecologically based divergent se- speciation
population, at least in
and adaptation wasthelargely
early forgotten,
stages of vergence
(2–5). all species appear to evolve by aptation to different environments or ecological taxonomic species. Darwin understood the im-
natural selection (2–5). Not all species appear to In this review, I summarize progress in un- on fishes...weight
polyploidy, even though is constantly
selection being
might be addedcrucial to lection drives divergence of mating preferences, its contributions
divergence.uncertain For this reason,
under the new mutation-
concept.
Fig. 1. (A) Example of ecological speciation. Repeatedly and
gamete re
selection, but the evidence suggests that most of niches (2, 8, 9). Natural selection is divergent, portance of reproductive barriers between species
evolve
Natural by selection, but the evidence suggests derstanding the general features of speciation the
in thetheory
early that
stages. speciation is...under the rigid for example by sensory drive (15). The speciation
orderbiological is difficult
species concept when must surely there Fig. 1. (A) Example of ecological speciation.
independently, the mosquito fish, Gambusia hubbsi, inhabiting Repeatedly and fixation o
them do.selection
The effortcommonly leading updrives to thisthe origin of species,
conclusion actingas in Darwin
contrasting initially claimed.
directions Mechanisms
between environ- of (1), but the study of speciation after the pub-
that most of
speciation bythem do. The
selection fall effort
into broadupcategories:
leading to by selection. Ianddo mutation-order.
not differentiateUnder speciation control of the environment” (12). However, this In accordance with (10), mutation-order spe- haveismadegeneitflow,more because
difficult togene
investigate any link independently,
flow increas- blue holes in the the mosquito
Bahamas fish, Gambusia
has evolved hubbsi,
a larger caudal and geous mu
inhabit-
region
involved many experimental and twoconceptual ad- ments, ecological
which drives the fixation of different lication Speciation of this work focused mainly on the evo-
is onlyand Adaptation from of their ulations,
between speciation and natural selection. T. ing bluehead
holesin inthethepresence
Bahamas of has evolved a larger
than incaudal
this conclusion
ecological speciation, involved many isexperimental
divergence by sexual selection herebetween
becauseenvironments,
natural selec- case referring to the origin morpho- ciation is defined as the evolution of reproduc- Dobzhansky
es the possibility that favorable muta- smaller predators (top)
vances, including a revision of the drivennotionbyofdivergentalleles,natural selection
each advantageous in one environment lution Darwin oftospecies
Dobzhansky differences, particularly of (13) suggested that the genes under- region and smaller head in the presence ofprobability
predatorsof(top) (16). Div
and conceptual
whereas under
speciation advances,
itself, mutation-order including
80 years after publication a revision
speciation,ofdivergence tion
On but not drives
occurs the
when
in the divergence
different
other. Following of mate
mutations preferences,
G. S. arise
Maniand logical
and morphological species. tive isolation by the fixation of different advan- lyingtions occurring
differences between in one population
populations in ordinary will than in their absence (bottom) (29). In laboratory trials, two
absence (bottom) (29). In laboratory trials, the
the other learn
of Appreciation oftraits
the but also of between
connection behavioral and
adapta- individuals mating was higher when they were from different
arethe
the notion
fixed
Origin in of Species,
of separate
the speciation to aitself,
populations 80 years
adapting
definition basedafter
toon byselection
similar
B. C.either
Clarke ecological
pressures.
(10), I define orTests
mutation-order mecha-
of parallel evolution
mutation-order specia- other The turning
phenotypic point
traits. for speciation studies tageous mutations in separate populations ex- phenotypic
spread traits to otherwerepopulations,
unlikely to be preventing
the basis of probability of twothe
populations having individuals matingenvironment
same predation was higher (and whensimilar
they havior und
publication On
ofisolation the instead
Origin of the Species, to mating,
nisms, in most theories of the process tion and
(8, 11).byI came with speciation
the Darwinian
modern beganconcept with Darwin of speciation when a periencing similar selection pressures. Whereas reproductive
divergence (17, 18).
isolation. Anychanged
He later process hisresult-
mind, were from different
body shape) than when populations
they were having the same
from opposite preda- tion, not m
predation
of reproductive
reproductive isolation, trait-based
of assortative
morphological tion as and
the reproductive
evolution isolation
of reproductive byisolation
active Under this
a definition based on reproductive isolation in- leave out discussion of sympatric and allopatric morphological
“Species separation concept is of perspective,
defined speciesas a largely
stage
linking
of pre-
the different alleles are favored between populations but ing
at thein time
low thislevels of geneand
viewpoint, flow,theincluding
generally tion environment
environments. [Photo(and similar
credit: Brianbody shape)(29)].
Langerhans than (B)when they efficient s
Example
selection have
differences (6, 7).demonstrated that ecological speciation is a common
the chance occurrence means andbyfixation
which of newdifferent
species speciation with adaptation was relatively straight-
stead of morphological differences (6, 7). speciation but instead identify the likelihood of vailed.
evolutionary In On the Origin
process of
at Species,
which Darwin
physiological wrote under ecological speciation, the same alleles greater difficultyfacilitates
selection, of studyingsubsequent
reproductivediver- isola- were from opposite
of reproductive predation
isolation evolving environments. [Photo credit: is the cul
under the mutation-order
arise. Evidence for mutation-order speciation by natural selection
The main question today is how does selec- alleles between populations adapting to similar forward, is more limited and has been requiring
that “I look at theonly termabecometest of whether
species, as one phenotyp-
arbitrarily tion than morphology, must have discouraged Brian Langerhans
mechanism. (29)]. (left)
Male-fertile (B) Example of reproductive
and male-sterile isolation
(right) flowers of mutation-o
bestThe
tion lead main
documented question
to speciation? todayare
by instances
What is of
how does selec-isolation
thereproductive
mechanisms ecological
selection resultingand mutation-order
pressures. from intragenomic
Reproductive speciation
conflict.
isolation when ic
evolves isolating
differences mechanisms
between species developed”
were caused (6)
by would be favored in different populations under gence by the mutation-order process evolving
many from pursuing the connection. Virtually no F2 hybridsunder betweenthean mutation-order
Oregon population mechanism.
of monkeyMale-fertile
flowers (M. al scenario
tion lead to speciation? What are the mecha- there is gene flow. I ignore reinforcement, a spe- given
(here, for the sake
“physiological” of convenience
is interpreted to toa set
mean of mutation-order speciation. Divergence occurs research (19).effortIn contrast,
However, we still have not identified all aspects of selection, and
of natural selection, what genes are affected, and because populations fix distinct mutations that natural identifying the underlying genes
individuals selection.
closely For example,
resembling at
each the American
other...” and followed ecological
that tested the speciation
role of (left) andhaving
guttatus) male-sterile (right)male
a cytoplasmic flowers of F2
sterility hybrids
element andbetween
nuclear Both
nisms doofchanges
for reproductive
how naturalatisolation
selection,
these genes what
remainsyield genes are af- would
challenging.
the habitat, cial type of naturalbeselection
nevertheless advantageous thought in to
bothfavor evolved reproductive
of Association forofthedifference isolation between
Advancement popula- anyway because, by chance, the populations do adaptation
can proceed with or without gene flow, an
in speciation. Oregon
restorer and population
a closely relatedof monkey
species flowers (M. guttatus)
(M. nasutus) hav- ecologica
having neither
“The amount is oneofvery Science 1939
important
fected, and mechanical,
behavioral, how do changes chemical,at these genes yield their
physiological, stronger premating reproductive
environments. The relative importanceisolation once tions, as distinct
of speciation symposium from[the geographical
last major barriers to
symposium not acquire the same mutations or fix them in the although it is easiest when gene flow ing (46,a47).
cytoplasmic
Both flowersmaleshownsterility
haveelement and nuclear
M. guttatus restorer
cytoplasm. The are theore
criterion in settling whether two forms should be and
flowera closely related
on the left also has species (M. nasutus)
the nuclear restorer,having
whereasneither
the one(46,
on only data
and habitat, behavioral, mechanical,
the other chemical, these postzygotic isolationofhas evolved. for I also
the ignore interbreeding). Subsequently, species were de- same order. Divergence is therefore stochastic Models of Speciation by Selection
is absent.
t took incompatibilities
evolutionary biologists that arenearly 150 years, ries: two
the reproduc- categories
ecological speciation mechanism and mutation-order origin on speciation
ranked as speciesbefore the varieties”
or biological species
(1). Underconcept this the right,
47). Both with undeveloped
flowers shown have anthers, lacks the cytoplasm.
M. guttatus restorer. [Photo
The ative imp

I
physiological,
tive
many
barriers

cies? As can
selection
species
between

a start,
might
be
and other new

the many
grouped
arise by
incompatibilities
species?

intoways
selection
two
As

by
can
broad
a

which
be
start, that
the speciation
of species inbynature
polyploidy,is even though selection (7)],
unknown.
but at last we can agree with Darwin that the speciation. Ecological speciation refers to the view, speciation is defined as the accumulation of
are theways reproductive
origin ofbyspecies, which barriers
new
“thatspecies
between new
mysterymight arisespe-
of mysteries” by might be crucial
In this
evolution review, in the early stages.
I summarize
of reproductive progress
isolation
new standing the general features of speciation by se- phological
catego-
(1), really does occur by means of natural selection ulations or subsets of a single population by ad- tions to warrant their classification as separate
grouped Speciation
lection. I do and
not Adaptation
differentiate from
speciation
in under-
between
Darwin
by sexual
finedanasextensive
pop- study
other such and
study
arisen of
over
“groups of
that are instances
lationsshowcased
sufficiently many
groups”
speciation
and
life
over
interbreeding
comparative
reproductively
differences
(7). From
history
was
again
in which

the
from
forms
and

this of
study
the
natural popu-
biogeographic
isolated
between derived
point
of
same
fishes
the
from
mor-
popula-
on,had
evolu-
ancestral
the
but the process is distinct from genetic drift. It The Experiments with laboratory popu- credit: Andrea
topic of natural selection in speciation
again receiving attention. The two most general flower
hypotheses involving selection are ecological and
infinite) populations. Selection can be ecologi- mutation-order
onstrate the
cally based under mutation-order speciation, but is defined
speciation.
plausibility
speciation. Ecological
In thoseofinstances
as the evolution
of ecological
is once

speciation er.
reproductivewhen
on theCase
can occur in both small and large (though not lations of Drosophila and yeast dem- one on the right, with undeveloped anthers, lacks the restor-
[Photoincluding
isolation,
left (47)]
also has the nuclear restorer, whereas the key is to

credit: Andrea Case isolation,

premating (47)]
mechanism
hybrid first evolved (3). Once the
iso- sterility, and intrinsic hybrid inviability as well as ences have accumulated b
(2–5). Not all species appear to evolve by aptation to different environments or ecological taxonomic species. Darwin understood the im-
into two broad
selection, but categories:
the evidence ecological
suggests speciation to
most of selection Dobzhansky here8, because natural selection is drives tion
the type of reproductive
(12). ofThe repeated, isolationparallel (3).between
Progress
origin up
ofspecies
non- to ecology does not favor divergence as such. It lation measurable
between populationspre- andby postmating
divergent natural re- extrinsic, ecologically based pre- and postzygotic either process, subsequen
Biodiversity Research Centre and Zoologythat Department, niches (2, 9). Natural selection divergent, portance reproductive barriers
and
themmutation-order
Universitydo.ofThe British
effort speciation.
Columbia,
leading up toEcological
Vancouver, V6T spe-
thisBCconclusion 1Z4, Appreciation
divergence of of
acting in contrasting mate the preferences,
connectionbetween
directions between
by either adap- then
eco- parasitic
environ- in understanding
(1), but lamprey
the study of the
in streams link
frombetween
speciation theaftersame morpho-
themigra-
pub- can lead to the evolution of any type of repro- selection
productive
arising isolation evolved,
from differences it waseco-
between greater be- (Odsh,
isolation. Speciation JYAlpha),
by sexual and selection
sexual isolation
is favored (ds2)inbe-one populatio
ciation
Canada.
involved refers
E-mail:
many toexperimental
the evolution
schluter@zoology.ubc.ca andofconceptual
reproductive tation
ments,and
ad- logical orwhich drives began
speciation
mutation-order with Darwin
themechanisms,
fixation of in when logical
most tory,
different lication speciation
parasitic workand
of thisancestor adaptation
showed
focused that was
mainly “Again
on the largely
and
evo- ductive isolation, with the exception of ecologi- logical
tween lines subjected
environments (2, 8, 9, to It predictsenvironments
14).different that ecological tween
speciationDrosophila
if ecologicallyspecies.
basedMostdiver- of because
these genes of epistatic inte
reproductive isolation should evolve between gent selection drives divergence of mating background (10). Hence, e
vances, including a revision of the notion of alleles, each advantageous in one environment lution of species differences, particularly the
isolation between populations or subsets of a a morphological concept of species largely forgotten, its contributions uncertain under of cally based pre- and postzygotic isolation. than between lines raised under homogeneous show molecular signatures of positive selection,
populations adapting to contrasting environments preferences, for example by sensory drive (15). producing Dobzhansky-M
single
speciation population
itself, 80byyears adaptation to different
after publication of en-
On prevailed.
but not in In On
theSCIENCE the Following
other. Origin of Species, Darwin and new concept. traits but also of behavioral and Speciation resulting from intragenomic con- but conditions
not between (20, 21). adapting
Laboratory experiments provingwith natural
(10), selection’s (3), provided
rolespe- in hybridsthat
www.sciencemag.org VOL G. 323 S. Mani
6 FEBRUARY morphological
2009 737 populations to similar In accordance mutation-order between specie
vironments
the Origin oforthe ecological
Species, to niches (2, 8, 9).
a definition Natu-
based on wrote that “I(10),
B. C. Clarke lookI at the mutation-order
define term species, as one other
specia- Thephenotypic
biologicaltraits. species concept must surely flict such as meiotic drive or cytoplasmic male environments.
on various Themicrobes
basic idea has maintained
been around under
for homo- fixation
ciation is defined occurred
as the evolution before complete reproductive
of reproductive either ecological or mutati
ral selection isisolation
reproductive divergent, insteadacting of in contrasting arbitrarily
morphological given forofthe
tion as the evolution sake of convenience
reproductive isolation by haveUnder made this it more Darwiniandifficultperspective,
to investigate any
linking sterility (Fig. 1B) is likely to be mutation-order a while
geneous conditions
(7), although it wasfor many
tested onlygenerations have by
recently. isolation isolation rather
the fixation of than afterward.
different advanta- The top-down
Speciation can be rapid
directions
differencesbetween (6, 7). environments, which drives to thea chance
set of individuals
occurrence closely and fixation resembling each link
of different between
speciation with speciation
adaptationand was natural
relativelyselection.straight- T. speciation because, by chance, the initial muta- Thedetected genetic divergence
agents of divergent consistent
selection are extrinsic and with the mutations
geous approach in separate identifying
involvespopulations (i) themodels,
expe- phenotypicbecause alleles ar
the Thefixation
mainofquestion differenttoday alleles,
is howeachdoes selec- other...”
advanta- and “The
alleles between amount ofadapting
populations difference is one Dobzhansky
to similar forward, requiring (13) only suggested
a test ofthat whetherthe genes phenotyp- un- tions causing drive and those countering it are can mutation-order
include abiotic andprocess (22),such
biotic factors butaseffects
food on re- similar
riencing traits under
selection divergent
pressures. Whereas(ii) natural
selection, those selection
traits in both
resources, climate, habitat, and interspecies inter- different alleles are favored between populations the mutation-order proces
geous
tion lead in toonespeciation?
environment Whatbut arenot
thein the other. very
mechanisms important
selection pressures. criterion in settling
Reproductive whether
isolation two derlying
evolves ic differences differencesbetween between
speciespopulations
were caused in or-by unlikely to be the same in separate populations. productive isolation have not been explored. associated with reproductive isolation, and (iii)
actions such as disease, competition, and behav- under ecological speciation, the same alleles present, would be favored
Following G. S. Mani
of natural selection, whatandgenes B. C.areClarke
affected, (10),andI forms
because should be ranked
populations fix as speciesmutations
distinct or varieties” that dinary
natural phenotypic
selection. For traits were unlikely
example, at the Americanto be the Speciation by sexual selection is mutation-order ioral interference.
Two approaches Ecological investigate
speciation the can mechanisms
lead would be favoredthe genes underlying
in different traits and
populations reproductive
under least in theiso-
early stages o
define
how domutation-order
changes at these speciation
genes yield the habitat,
as the evolu- (1). would Under this view,be
nevertheless speciation
advantageous is defined
in bothas the
of basis of reproductive
Association for the Advancement isolation. He oflater
Science changed
1939 speciation if divergence of mate preferences or to the of speciation
evolution ofbyany type selection
natural of reproductive in nature.mutation-order
The lation. Step (iii)
speciation. has beenoccurs
Divergence challenging
any- reason,undermutation-order
both spe
tion of reproductive
behavioral, mechanical,isolation chemical,byphysiological,
the chance accumulationtheir environments. of sufficiently
The relative many differences
importance of his mind, but
speciation at the time
symposium [thethis lastviewpoint,
major symposium and the gamete recognition occurs by the fixation of bottom-up approach involves (i) genetic map- approaches but is needed to understand how se-
occurrence and fixation of that
and other incompatibilities different
are theallelesreproduc-be- between
these twopopulations
categories of to mechanism
warrant their forclassifica-
the origin generally
on speciation greater
beforedifficulty
the biological of studying
species concept repro- alternative advantageous mutations in different ping of reproductive isolation between closely lection has led to reproductive isolation.
738 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
tween populations
tive barriers betweenadapting new species? to similar
As a start, selec-
the tion as separate
of species in nature taxonomic
is unknown. species. Darwin un- ductive isolation than
(7)], an extensive comparativemorphology, must have
and biogeographic populations, as by sexual conflict (16). Diver- related species, (ii) testing whether discovered
tion
manypressures.
ways by which Reproductive
new species isolation
might evolves
arise by derstood In thisthe importance
review, I summarizeof reproductive
progress inbarriers
under- discouraged
study showcased many from pursuing
instances in which derived the connec- mor- gence in song and other learned components genes exhibit a genomic signature of positive Ecological Speciation
because
selectionpopulations
can be grouped fix distinct
into twomutations
broad catego- that between
standing species
the general (1), features
but the study of speciation
of speciation by se- tion. Virtually
phological and no liferesearch
history effort forms followed
of fishes that had of behavior under purely social selection, not selection, and (iii) identifying the phenotype Evidence for ecological speciation has accumu-
after theIpublication
lection. do not differentiateof this work focused
speciation bymainly arisen the
sexual tested overrole andofover adaptation
again from in speciation.
the same ancestral molded by selection for efficient signal trans- and source of fitness effects of alternative alleles lated from top-down studies of adaptation and
Biodiversity Research Centre and Zoology Department, on the evolution of species differences, particu-
selection here because natural selection drives the type (12). The repeated, parallel origin of non- mission (5), is the cultural equivalent of the at selected loci. The approach has been hugely reproductive isolation [reviewed in (2, 8, 9)].
University of British Columbia, Vancouver, BC V6T 1Z4, larly of morphological
divergence of mate preferences, traits but also of behav-
by either eco- Models of Speciation
parasitic lamprey in streams by Selection
from the same migra- mutation-order process. Additional scenarios successful in identifying major genes implicated We now know of many real species that have,
Canada. E-mail: schluter@zoology.ubc.ca ioral and other phenotypic traits.
logical or mutation-order mechanisms, in most The topic of natural selection that
tory, parasitic ancestor showed in speciation
“Again and is are elaborated in (5). in hybrid inviability (Hmr, Lhr, Nup96), sterility at least in part, evolved by divergent natural se-

26 27
www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009 737
y to mate if they are of nents of reproductive isolation lacking identifiable
less of relatedness as causes (Fig. 2). The unidentified component of
affinity. speciation, if built by selection and not genetic
is also
premat-
n which Components – divergent selection plants (28), Littorina marine snail ecotypes of reproductive isolation lacking identifiable of mutation-order divergence. It may be that the between genes could generate reproductive iso- 20. W. R. Rice, E. E. Hostert, Evolution 47, 1637
rentially 15 inhabiting different zones of the intertidal causes (Fig. 2). The unidentified component of mutation-order process is more difficult to de- lation (45). Mostly, I expect that he would be (1993).
basis of (24), and mosquito fish inhabiting blue speciation, if built by selection and not genetic tect, or perhaps we have not looked hard enough chuffed by mounting evidence for the role of 21. J. R. Dettman, C. Sirjusingh, L. M. Kohn, J.
e under B. Anderson, Nature 447, 585 (2007).
10 holes with and without fish predators in the drift, could be the result of either ecological or at species with only small ecological differences natural selection on phenotypic traits in the ori-
nt selec- 22. Z. D. Blount, C. Z. Borland, R. E. Lenski,
ortative
Bahamas (29) (Fig. 1A). In these studies, it mutation-order mechanisms. (5). We still do not know much about the selec- gin of species. This is really what On the Origin Proc. Natl. Acad. Sci. U.S.A. 105, 7899
5
insects, was shown that males and females are more These examples indicate a growing knowl- tive factors causing mutation-order speciation. of Species was all about. Between 1859 and the (2008).
Number of studies

in fish, 0
likely to mate if they are of the same eco- edge of the mechanisms of selection and its Evidence for mutation-order speciation present, the general acceptance of the biologi- 23. D. Schluter, L. M. Nagel, Am. Nat. 146, 292
or pref- type, regardless of relatedness as indicated consequences for reproductive isolation. At comes from instances in which reproductive cal species concept altered the focus of specia- (1995).
notypic by phylogenetic affinity. this point, the most glaring deficiency is our isolation apparently evolved as a by-product tion studies. Yet, the discovery that reproductive 24. R. K. Butlin, J. Galindo, J. W. Grahame,
Components – unknown cause
flower- Philos. Trans. R. Soc. London Ser. B Biol. Sci.
15 Ecological speciation is also supported knowledge of the impact of selection on genes. of conflict resolution between genetic elements isolation can be brought about by ecological 363, 2997 (2008).
be under
environ- by examples of premating reproductive Optimistically, progress is being made with ge- within individuals (intragenomic conflict), such adaptation in ordinary phenotypic traits bridges 25. H. D. Rundle, L. Nagel, J. W. Boughman, D.
30, 31)]. 10 isolation in which individuals choose or netic mapping to identify quantitative trait loci as cytoplasmic male sterility in hermaphroditic Darwin’s science of speciation and our own. Schluter, Science 287, 306 (2000).
vergent preferentially encounter mates on the basis (QTLs) and genes or regulatory control regions plants (Fig. 1B), and genetic elements confer- The most obvious shortcoming of our cur- 26. E. B. Taylor, J. D. McPhail, Proc. R. Soc.
directly 5
of phenotypic traits that are under ecologi- that affect individual phenotypic traits on which ring meiotic drive. Under both mechanisms, a rent understanding of speciation is that the London Ser. B Biol. Sci. 267, 2375 (2000).
27. J. S. McKinnon et al., Nature 429, 294 (2004).
uced fit- cally based divergent selection. Examples components of reproductive isolation depend. mutation arises that can distort representation in threads connecting genes and selection are still 28. P. Nosil, S. P. Egan, D. J. Funk, Evolution 62,
he envi- 0
-0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1
include assortative mating by host choice Examples include the yup QTL, which affects gametes and spreads in a selfish manner, even few. We have many cases of ecological selec- 316 (2008).
migrant
31, 32)] in insects, body size and coloration in fish, flower color differences between the monkey though such an element reduces overall fit- tion generating reproductive isolation with little 29. R. B. Langerhans, M. E. Gifford, E. O. Joseph,
Cumulative reproductive isolation
ybrids in beak size in birds, pollinator preferences for flowers, Mimulus cardinalis and M. lewisii (35). ness of the organism that bears it. This, in turn, knowledge of the genetic changes that allow Evolution 61, 2056 (2007).
Fig. 2.2. Estimates
[extrin- Fig. Estimates of of
the the
magnitude
magnitudeof reproductive isolation
of reproductive specific phenotypic floral traits, and varia- Swapping alleles of this QTL between the spe- places selection on mutations in other genes that it. We have strong signatures of positive selec- 30. S. Via, Trends Ecol. Evol. 16, 381 (2001).
resulting
isolation from divergent
resulting from selection
divergentcomponents
selection (top), compared
components 31. D. B. Lowry, J. L. Modliszewski, K. M.
3)]. For
with othercompared
componentswith lacking identifiable causes (bottom). tion in flowering time—traits inferred to be cies with repeated backcrossing resulted in shifts counter the selfish element’s effects and restore tion at genes for reproductive isolation without Wright, C. A. Wu, J. H. Willis, Philos. Trans.
l peren- (top), other components lacking
Divergent
identifiableselection components
causes (bottom). includeDivergent
those attributable
selectionto under divergent selection between environ- in pollinator preference and, hence, indirectly more equal genetic representation in gametes. enough knowledge of the mechanisms of se- Royal Soc. London Ser. B Biol. Sci. 363, 3009
s of the active selection on traits (immigrant inviability and extrinsic
components include those attributable to active ments [see examples in (8, 30, 31)].
uttatus) postzygotic
affected premating isolation. Survival and salt Distorter and restorer mutations are unlikely to lection behind them. But we hardly have time (2008).
selectionisolation)
North preference, on traits and(immigrant
to trait-basedinviability
assortative and
mating (habitat
extrinsic Ecologically based divergent selection tolerance of second-generation hybrids between be the same in different populations regardless to complain. So many new model systems for 32. P. Nosil, T. H. Vines, D. J. Funk, Evolution 59,
postzygotic floralisolation)
isolation, and
and breeding
to time). The assortative
trait-based unattributed 705 (2005).
s when components include intrinsic hybrid inviability, sexual selection has also been directly measured, as shown the sunflowers Helianthus annuus and H. peti- of environment; thus the process leads to diver- speciation are being developed that the filling of
mating (habitat preference, floral isolation, and breeding 33. H. D. Rundle, M. C. Whitlock, Evolution 55,
of the against by reduced fitness of each ecotype in the en- olaris transplanted to the salt marsh habitat of gence. The mismatch between the distorter in major gaps is imminent. By the time we reach
time).hybrids, pollen competition,
The unattributed and reduced
components hybrid fecundity.
include intrinsic 198 (2001).
mple of Data were taken from (32, 31) (table S1). A negative value vironment of the other [immigrant inviabil-
hybrid inviability, sexual selection against hybrids, pollen their hybrid descendent species (H. paradoxus) one population and the restorer in the other can the bicentennial of the greatest book ever writ- 34. N. H. Martin, J. H. Willis, Evolution 61, 68
ypic dif- indicates
competition, and reduced hybrid fecundity. Data were ity; reviewed in (31, 32)] and by reduced fit-
that hybrids had higher fitness than the parental species mapped strongly to a QTL identified as the salt result in hybrid sterility or inviability and, thus, ten, I expect that we will have that much more (2007).
utes di- for at least one component of postzygotic isolation. One data value
taken from (32, 31) (table S1). A negative value indicates ness of hybrids in the parental environments tolerance gene CDPK3 (36). reproductive isolation (3, 41). Numerous exam- to celebrate. 35. H. D. Bradshaw, D. W. Schemske, Nature 426,
because of –2.66 was left out of the bottom panel.
that hybrids had higher fitness than the parental species [extrinsic postzygotic isolation (33)]. For Another form of investigation involves the ples of selfish elements, such as those observed 176 (2003).
for at least one component of postzygotic isolation. One example, each of the coastal perennial and 36. C. Lexer, Z. Lai, L. H. Rieseberg, New Phytol.
analysis of genome scans of ecologically differ- in cytoplasmic male sterility of plants, support 161, 225 (2004).
VOL 323 data value of –2.66
6 FEBRUARY 2009 was left out of the bottom panel. 739
inland annual races of the monkey flower ent populations and species. These scans com- these hypotheses (42, 43). In addition, partial re- References and Notes 37. M. A. Beaumont, Trends Ecol. Evol. 20, 435
(Mimulus guttatus) along the west coast of pare allelic variation within and between popu- productive isolation generated by meiotic drive 1. C. Darwin, On the Origin of Species by Means (2005).
lection between environments. The connections North America has low fitness when transplant- lations at many marker loci spaced throughout has been identified in Drosophila [reviewed of Natural Selection (J. Murray, London, 38. P. Nosil, D. J. Funk, D. Ortiz-Barrientos, Mol.
1859). Ecol. 18, 375 (2009).
between selection on ordinary phenotypic traits ed to the habitat of the other (31). This is an ex- the genome (37). Markers that show excessive in (3, 41)]. Sexual conflict is also expected to 2. D. Schluter, The Ecology of Adaptive 39. S. M. Rogers, L. Bernatchez, Mol. Biol. Evol.
and reproductive isolation are often strong and ample of active selection on phenotypic differ- differentiation between populations (outliers) lead to mutation-order speciation, but there are Radiation (Oxford Univ. Press, Oxford, 2000). 24, 1423 (2007).
straightforward. It follows that much of the ge- ences, and it also constitutes direct reproductive may indicate selection on nearby genes. The few compelling examples (3). The contribu- 3. J. A. Coyne, H. A. Orr, Speciation (Sinauer 40. S. Via, J. West, Mol. Ecol. 17, 4334 (2008).
netic basis of reproductive isolation should in- isolation because it is an evolved barrier to gene method is particularly informative when applied tion by these mechanisms to speciation is still Sunderland, MA, 2004). 41. H. A. Orr, J. P. Masly, N. Phadnis, J. Hered.
volve ordinary genes that underlie differences in flow between parental populations. Multiple to populations with ongoing hybridization, be- uncertain, however. The alleles responsible for 4. P. R. Grant, B. R. Grant, How and Why 98, 103 (2007).
Species Multiply: The Radiation of Darwin’s 42. D. A. Levin, Syst. Bot. 28, 5 (2003).
phenotypic traits. But we still know little about traits are probably involved, including flowering cause outlier markers may identify points in the meiotic drive and cytoplasmic male sterility Finches (Princeton Univ. Press, Princeton, NJ, 43. L. H. Rieseberg, J. H. Willis, Science 317, 910
the genetics of ecological speciation. time and tolerance of salt and drought. This type genome that resist the homogenizing influence may be prevented from spreading to fixation be- 2008). (2007).
One line of evidence comes from tests of of reproductive isolation is context-dependent of gene flow, perhaps indicating genomic re- cause selection on such elements is frequency- 5. T. Price, Speciation in Birds (Roberts & 44. D. C. Presgraves, Trends Genet. 24, 336
parallel speciation, whereby greater reproduc- and is weakened in intermediate environments. gions under divergent selection. However, sets dependent (43) and because restorer alleles arise Company, Greenwood Village, CO, 2008). (2008).
tive isolation repeatedly evolves between in- On the other hand, active selection favors the of genes that diverged under a mutation-order and weaken selection on the distorter elements 6. T. G. Dobzhansky, Genetics and the Origin 45. D. C. Presgraves, Curr. Biol. 17, R125 (2007).
of Species (Columbia Univ. Press, New York, 46. L. Fishman, J. H. Willis, Evolution 60, 1372
dependent populations adapting to contrasting evolution of ever-greater differences between process can produce the same pattern (17, 18), (44). Second, if divergent populations come 1937).
environments than between independent popu- populations, which may strengthen the barrier which makes analysis of such studies more diffi- into secondary contact, the alleles within each (2006).
7. E. Mayr, Systematics and the Origin of 47. A. L. Case, J. H. Willis, Evolution 62, 1026
lations adapting to similar environments (20, to gene flow (20). cult. Clues to whether ecologically based diver- population causing cytoplasmic male sterility Species (Columbia Univ. Press, New York, (2008).
23). A major challenge in applying the test to It is unclear how much reproductive isola- gent selection is involved are gained if outliers or meiotic drive (and the corresponding restorer 1942). 48. We thank M. Arnegard, R. Barrett, A. Case,
natural populations is to eliminate the possibili- tion typically evolves by ecologically based at the same genomic locations turn up repeat- alleles) will spread between the populations by 8. D. Schluter, Trends Ecol. Evol. 16, 372 (2001). H. Hoekstra, M. Noor, P. Nosil, S. Otto, T.
9. H. D. Rundle, P. Nosil, Ecol. Lett. 8, 336 Price, L. Rieseberg, S. Rogers, A. Schluter,
ty that each ecotype has originated just once and divergent selection in nature. We can approxi- edly in scans between populations that inhabit gene flow, eliminating that component of repro- (2005).
has spread to multiple locales. This is difficult mate an answer from estimates of the combined contrasting environments (38) and by identify- ductive isolation (43). Hence, for these mecha- S. Via, M. Whitlock, J. Willis, and a reviewer
10. G. S. Mani, B. C. Clarke, Proc. R. Soc. for assistance and comments. This work was
because gene flow of neutral markers between contribution of active selection on traits and ing phenotypic traits under divergent selection nisms to contribute to speciation, the fitness of London Ser. B Biol. Sci. 240, 29 (1990). supported by grants from the Natural Sciences
closely related but nearby populations can result trait-based assortative mating, as compared with that map to those locations in the genome (36, hybrids must be reduced to very low levels, or 11. M. Turelli, N. H. Barton, J. A. Coyne, Trends and Engineering Research Council of Canada
in the false appearance of multiple independent other forms of reproductive isolation (Fig. 2 39, 40). As genomic resources increase for more other incompatibilities must arise that interact Ecol. Evol. 16, 330 (2001). and the Canada Foundation for Innovation.
12. C. L. Hubbs, Am. Nat. 74, 198 (1940).
origins of these populations when evaluated by and table S1). These estimates are incomplete species, it will be possible to measure natural with these genes to prevent their spread after
13. T. Dobzhansky, Am. Nat. 74, 312 (1940).
phylogenies (3, 24). However, multiple origins because individual studies may lack data on selection directly on genomic regions of inter- secondary contact. 14. Additional references are available as Supporting Online Material
are supported in several examples of parallel components of reproductive isolation, separate est by transplanting otherwise relatively ho- supporting material on Science Online. www.sciencemag.org/content/full/323/5915/737/
DC1
speciation, including the sympatric benthic- components may not be independent, and the mogenous experimental populations containing Conclusions 15. J. A. Endler, Am. Nat. 139, S125 (1992).
16. W. R. Rice et al., Proc. Natl. Acad. Sci. U.S.A. Tables S1 to S3
limnetic species pairs of threespine stickleback strength of barriers between species may not be alternative alleles into the environments of the Our understanding of the role of natural selec- References
102, 6527 (2005).
in young lakes of British Columbia (25, 26), the symmetric (34). Nevertheless, compilation of parent species (35). tion in speciation has come a long way since 10.1126/science.1160006
17. N. Barton, B. O. Bengtsson, Heredity 57, 357
repeated origin of divergent marine and stream the data shows that the amount of reproductive Darwin’s time. If he were here to witness, he (1986).
populations of threespine stickleback around the isolation attributable to active selection and trait- Mutation-Order Speciation would most likely be staggered by the discover- 18. A. S. Kondrashov, Evolution 57, 151 (2003).
Northern Hemisphere (27), ecotypes of Timema based assortative mating is at least as strong, Mounting evidence for divergent selection in ies of genes and molecular evolution and aston- 19. L. H. Rieseberg, personal communication
walking stick insects living on different host on average, as the amount from components speciation does not diminish the potential role ished at the prospect that evolutionary conflict (2008).

28 29
 REVIEW
values that place two bacterial isolates into the Speciation
same or different species. The overall genetic
pneumoniaeof isisolates
relatedness SPECIALSECTION
a major mayhuman be measured pathogen, by the S. A S. pseudopneumoniae B
The Bacterial Species Challenge:

s
S. pneumoniae

si
mitis is a commensal bacteria with a history
extent of DNA hybridization between them, and 3% divergent

en
1.2% divergent

oi
32. P. Nosil, T. H. Vines, D. J. Funk, Evolution 59, 705 (2005). 40. S. Via, J. West, Mol. Ecol. 17, 4334 (2008). S. Rogers, A. Schluter,
70%S. or Via,more
M. Whitlock, J. Willis, and
of taxonomic
those
a reviewer foruncertainty
that show
assistance and (11), and
DNA pseudo-
S. work
hybrid- V. ordalii

s
um

icu
33. H. D. Rundle, M. C. Whitlock, Evolution 55, 198 (2001). 41. H. A. Orr, J. P. Masly, N. Phadnis, J. Hered. 98, 103 comments. This
Making Sense of Genetic and

lyt
pneumoniae
ization are defined as
is abyrecently the same
described species
the Naturalorganism (2, 10).of

V.
34. N. H. Martin, J. H. Willis, Evolution 61, 68 (2007). (2007). was supported grants from Sciences and

o
in
Such
uncertain cutoffsstatus imply that
that nonethelesssequences thatthecluster
corresponds to s i

lg
35. H. D. Bradshaw, D. W. Schemske, Nature 426, 176 (2003). 42. D. A. Levin, Syst. Bot. 28, 5 (2003). Engineering Research Council of Canada and Canada nu ge

a
ia
i/lo

V.
36. C. Lexer, Z. Lai, L. H. Rieseberg, New Phytol. 161, 225 43. L. H. Rieseberg, J. H. Willis, Science 317, 910 (2007). together with
Foundation
a distinct foraInnovation.
cluster certain
in theseamount data (12). of There similarity are r
Ecological Diversity
(2004).
37. M. A. Beaumont, Trends Ecol. Evol. 20, 435 (2005).
44. D. C. Presgraves, Trends Genet. 24, 336 (2008).
45. D. C. Presgraves, Curr. Biol. 17, R125 (2007).
must
striking
Supporting
that
be differences
this
fromOnline
cutoff
the Material
value
same
in the
is
species,
amount
applicable
and of moreover
to
sequence
all groups Entero
vibrio n
orvegic
us
ae is
V. V. f
ua
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e r

38. P. Nosil, D. J. Funk,1D. Ortiz-Barrientos, Mol. Ecol. 18, 46.2L. Fishman, J. H. Willis,1 Evolution 60, 1372 (2006). diversity observed within homologous
www.sciencemag.org/cgi/content/full/323/5915/737/DC1
house-
Christophe Fraser, * Eric J. Alm, 2,3,4
Martin F. Polz, 47. A.Brian
L. Case,G.J. Spratt, William 62,P. Hanage 1 Tables
of S1 to S3or archaea. Recent MLSA studies,
bacteria nsis eri teu
s
keeping V. calvie
References genes in these named species, ranging
375 (2009). H. Willis, Evolution 1026 (2008). ch rs
. fis pe
39. S. M. Rogers, L. Bernatchez, Mol. Biol. Evol. 24, 1423 48. We thank M. Arnegard, R. Barrett, A. Case, H. Hoekstra, which
from
use the concatenated sequences of mul-
1.2% for S. pneumoniae to 3.0% for S. S. mitis V su
M. Noor, P. Nosil, S. Otto, of T. Price, 10.1126/science.1160006 V.
The (2007).
Bacteria and Archaea are the most genetically diverse superkingdoms life, L.and
Rieseberg,
techniques tiple housekeeping genes to discern clustering
pseudopneumoniae and up to 5.0% for S. mitis.
5% divergent a*
e cid
for exploring that diversity are only just becoming widespread. Taxonomists classify these patterns among populations of closely related an
The distance between two randomly selected V.
p
organisms into species in much the same way as they classify eukaryotes, but differences in their taxa, suggest that species defined by taxono-
S. mitisthat
values genotypes
place is similar
two bacterial to theisolatesaverage into dis-
the
biology—including horizontal gene transfer between distantly related taxa and variable rates of mists in many cases correspond to well-resolved
REVIEW tance between
same or different S. pneumoniae and S. pseudo-
homologous recombination—mean that we still do not understand what a bacterial species is. This sequence clusters. species.However,The these overall
studies genetic
also
pneumoniae
relatedness ofgenotypes
isolates (5.1%)
may (2). This implies
be cutoff
measured by the
is not merely a semantic question; evolutionary theory should be able to explain why species show that there is no universal or descrip-
The Bacterial Species Challenge:
exist at all levels of the tree of life, and we need to be able to define species for practical
applications in industry, agriculture, and medicine. Recent studies have emphasized the need to
that
extent
tor oftheclusters
ofuseDNA of that
ahybridization
fixed level of
characterizes
thermore, inspection of the clusters does tend
gence
those for
that differentiating
show 70% or species
more
sequence
between a species.
DNA would
them, diver-
and
Fur-
hybrid-not
S. oralis
0.005
Vibrio splendidus
to either arerejoin S. pneumoniae in theS.hierarchy
and pseudo-
Making Sense of Genetic and
combine genetic diversity and distinct ecology in an attempt to define species in a coherent and
convincing fashion. The resulting data may help to discriminate among the many theories of
ization
always
pneumoniae,
Such
is
clearly
morecutoffs
defined
or
fundamental
reveal
imply
aswhich
breakthan
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S. mitis
up sequences
that any otherso(Fig. that 1)
that
(2, 10).
nearly
cluster
(7).
every
together isolate
with was a a species
certain of
amount its own.
of This
similarity is 0.005
Ecological Diversity
prokaryotic species that have been produced to date.
ships
As an example, Fig. 1A shows the relation-
clearly
must be unsatisfactory.
among frommultiplethe sameisolates species,of and threemoreover closely

T
he species debate in microbiology is not reflect only a tiny subset of those characters that related that this streptococcal
cutoff value is species. applicableStreptococcusto all groups Fig. 1. Multilocus sequence analysis of closely related species. (A) Radial associations of Vibrionaceae sequence clusters (13). Habitats (colored dots) were

TChristophe

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Archaea
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but environment,
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Brian
bacteria
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distinguished
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G. Spratt,
to use
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true diversity
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and
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this, taxaa small
muchin1ofthe
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too fraction
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this ofsuperkingdom rRNA
to is
Habitats
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it pneumoniae
A aclear
which
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natural
use
commensal
tiple housekeeping
is aEcological
or archaea.
major human
criterion
the concatenated
uncertainty
bacteria with
importance,
(11),
Recent

andwhich
genes
Differentiation

S.
MLSA S.
pathogen,
to identify
sequences
a history
we might
topseudopneumoniae
discern
studies,
clusters
mitis
of taxo-
of mul-
want
clustering
of
minimum evolution tree constructed using MEGA4, showing clusters among 97
isolates of four Streptococcus species identified as indicated. The tree was built
using concatenates of six housekeeping loci, resulting in a total of 2751 positions
in the final data set (2). Distances were calculated as the percentage of variant
estimated as differential distributions of groups of closely related strains among
samples (size fractions enriched in different environmental resources). Clusters
associated with named species are evident, and in most cases species show a clear
predilection for one of the habitats. The exception is V. splendidus, which breaks
ner, butabout
is alsoour
for exploring
reveals a fundamental
that diversity of
ignorance argument
arehow justbecause
onlyevolutionary becomingMore quences
widespread. have Taxonomists
recently, revealed
molecular further diversity
classify
methods these through is
[particularly to acall
patterns species,
recently among is populations
described to find ecological
organism features
of uncertain
closely that
related
status
of whatform, it into
reveals about our ignorance of way
how multilocus
nucleotide sites. The mean distance within the clusters, calculated by MEGA4, is up into many closely related ecological populations. Asterisk denotes that trees
organisms
forces species
shape, and in much
extinguish thebacterial
same ge-as they
DNA-DNAclassifysequence
eukaryotes,
hybridization analysis
butand (MLSA)
ribosomal(2)
differences inRNAand that
their distinguishsuggestthem
taxa,nonetheless that from
species
corresponds close to arelatives.
defineddistinct Among
bycluster
taxono- in shown. To the right, the pneumococcal cluster is shown at larger scale, and based on additional loci indicate that the placement of V. panecida within V.
evolutionary
biology—including
netic lineages, forces
of the form,
horizontalshape,
mechanisms geneandoftransfer
extinguish
differen- between metagenomic
(rRNA)distantly studies
related
sequencing] taxa(1),
have andand
helped to this
variable diversity
definerates of
species, pathogens,
mists data
these in many thecases
(12). ability
There aretostriking
correspond causeto differences
awell-resolved
distinctive in putative subclusters are indicated in dark gray, purple, and green. (B) Ecological splendidus may be an artifact of horizontal gene transfer at the Hsp60 locus.
bacterial
homologous
tiation genetic
between lineages, of thesharing
recombination—mean
subpopulations mechanisms
thatcommon of dobut
we still needs
not theseto be
understand explained
methods whathave a by theory.limitations
bacterial
serious Thus, is.
species practi-
This
and the disease
sequence
amount has ofhistorically
clusters.
sequence However, beenthese
diversity used
observed to within
studies define
also
differentiation
is not merely
descent, and ofabetweensemantic
the process subpopulations
question;
of adaptation sharing
evolutionary
to new theory cal difficulties,
cannot should
reliably lack
able of
beassign a theory,
to explain
large and
whyobservations
collection species species,
show thatbut
of similar homologous pathogens
therehousekeeping constitute
is no universal genescutoff inonlytheseora descrip-
minute
named
common
exist
niches atanddescent,
all levels
changing andenvironments.
of theof the process
tree of life, of adapta-
and
Animal we need of vast to
to
spe- strains be able speciesof(e.g.,
amountsto define as yet
species
rRNA unclassified
for microbial
practical
sequences are too fraction of overall bacterial diversity. Mapping
tor of
species, clusters
ranging that
from characterizes
1.2% for S. a species.
pneumoniae Fur-of
to vation;
but pathogens or most models
many constitute of a population
only a minute fraction of diversity.
not, per se, The
a veryfirst proposed
interesting mechanism
observation; many was
or makes
strict thereference
accumulation to the unifying
of neutral biological
diversity. The
tion to new
applications
cies are definedniches by and
in industry,theirchanging
agriculture,
morphological environments.
andand medicine. diversity have
Recent studies
be- conserved allhave
to resolve fueled the controversy
emphasized
similar species).therRNAneedof howto bacterial
thermore,
se- 3.0% for S. diversity
inspection ontoofenvironmental
pseudopneumoniae and up toresources
the clusters does
5.0% not for reproducing
overall withdiversity.
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amount of of mutation
bacterial based on artificial
most models selection reproducing
of a population experimentswith witha principles
first proposed of mechanism
selection and wasniche
basedpartitioning,
on artificial
Animal
combine traits
havioral species
geneticandare by defined
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their and bydistinct
ability their morpho-
ecology
or inability to in anoneattempt
quence defines
surveys a bacterial
to define speciesinrevealed
species
have, however, (3–8).
a coherent and S.
the extra- indicates
always
mitis.clearlythatdistance
The closely
reveal which related
between levelgroups
two theofhierarchy
in randomly bacteriase- will eventually
diversity produce populations
onto environmental resourcesconsisting bacteria
indicates small amountgrown for extended
of mutation will eventually under the
periodsproduce ecotype
selection has rightly
experiments become
with bacteriapopular
grownasfora
logical and behavioral traits and by their abil-
convincing
interbreed, fashion.
but such The resulting
categories cannotdata may
easily help
be to discriminate
ordinary variety amongof the
microbial many theories
life, much ofof it can be ecologically divergent. For example,
is more
lected S. fundamental
mitis genotypes than is any
similar other to (Fig. 1)fine-
the average (7). of clusters
that closely of related
related organisms,
groups irrespective
of bacteria can be eco- of stable conditions
populations in chemostats,
consisting of clusters of which showed
related orga- framework
extended periods within which
under to conditions
stable discuss bacterial
in che-
ity or inability
prokaryotic
applied to the to interbreed,
species
Bacteria thatorhave but
been
Archaea such categories
produced
(or indeed to Genetic Clustering
to date.
uncultured (1). Beyond this, taxa too similar to be distance scale Asresource
anbetween
example, S. Fig.
partitioning 1A has
pneumoniae shows andthe
been relation-
S.observed
pseudo- the detailsdivergent.
logically of the evolutionary
For example, forces or ecologi-
fine-scale re- repeated selective of
nisms, irrespective sweeps in which
the details of the the whole evolution,
evolution- mostats, which speciation,
showedand ecology.
repeated selective sweeps
cannoteukaryotic
many easily be microbes).
applied toInstead, the Bacteria or Ar- distinguished
taxonomists Darwin commented that “all trueby
and circumscribed classification
rRNA se- pneumoniaeships among
among coastal multiple
Vibrio isolates
genotypes populations
(5.1%) of three
(2). This closely
coexisting
implies cal differentiation.
source partitioningAhas more
beensubstantial
observedobserva-
among genomeary forceswas or ecological hitchhike to A
thought todifferentiation. fixation
more in The which ecotype
the whole (4, 16, 24)
modelgenome waspredicts
thoughtthatto
he species debate in microbiology is not reflect only a tiny subset of those characters that related streptococcal species. Streptococcus

Tchaea (or indeed to many eukaryotic microbes). is genealogical” [(9), p. 404]. Taxonomists have in the water column (13). Partitioning was
have
limited
pose.
been
Instead,only
terial
forced
taxonomists
morphological
Naturally,
to
about a human
diversity
is also a fundamental
selected
rely

biochemical
for the convenience
characteristics for this
in
on
have
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argument
biochemical
desire
been forced
characteristics
consistent
purpose.
characters
of because
to catalog
tests
for this
manner,
taxonomists;
have
Naturally,of what
and
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to pur-
but
been
they
bio- it to
quences
allowused
rely multilocus
thus
environment,
metagenomic
thebetrue
same
have
bacteria
revealed
sequence
and
studies
diversity
differentbyin
explained
or
only
further
to userelatedness
sequence
capture
(1), and a
diversity
different(MLSA)
analysis
this
this superkingdom
theory.
species.
resources
small
on biochemical tests and limited morphological values that place two bacterial isolates into the distinct, ecologically informative samples, and
Thus,overall
The
through

fraction
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practical
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of life.
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that
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rejoin
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the
the
pneumoniae
discovered
is a
break
use

S.
of
differentiating
commensal
a
because
pneumoniae
uncertainty
fixed
is a major

up S. mitis(11),
phylogenetic
level
strains
species
bacteriaand
so that
of
human
S.
andnearly
structure
sequence
were
would
with
pathogen,
a
collected
history
pseudopneumoniae,
S.ofpseudopneumoniae
every
the
divergence
tend toS.either
of
mitis
from
taxo-
isolate was
ecologically
tion is that
coastal

we may
strains
Vibrio
in many(13).
column
were
informative
there
populations
infer
is very little
populations
Partitioningof was
some from
collected
microbes,
features
samples,diversity
landscape. Neutral
neutral
coexisting
discovered
of the
distinct,
and the phylogenetic
is the amount
diversity
in the
frombecause
along with observation
water substantial
which neutral
selection)
selective almost
ecologically
struc-
from which
of selective
an advantageous
(22). inSelective
diversity
all genetic
we maydiversity
is thatmutation
sweeps ofcan
many populations
infer some
landscape.a candidate
and thus constitute
in the
Neutral diversity
(periodic
there is very little common

population
features
mechanism
of the be
is the
hitchhike ancestry
purge terial
microbes, mutation
to fixation
populations
canmonophyletic),
purge almost alland
ulationare
for types andcoherent
will be preserved
along
within niches
(periodic selection)

thus constitute
thusdiversity
genetic
among bac-
with an advantageous
(which sweeps
(22). Selective
predictsinthat
a candidate
self-contained
should
eco-
the pop-
genemecha-
pools.
reveals about our ignorance of how evolutionary More recently, molecular andmethods [particularly isspecies
a recently described organism of uncertain status
chemical characters have been selected for the ficulties, relatedness lack ofofisolates
theory,may observations
be measured of the adifferentiated
byvast of its own. This
populations is clearly unsatisfactory.
was superimposed ture of the ecologically
polymorphism differentiated
that is evident populations
in noncoding re- amount
reducingofneutral
polymorphism
variationthat (23).is evident in non- As nisma result,
for reducing
it has neutral variation that
been suggested (23).ecotypes
1forces form, shape, and extinguish bacterial ge- DNA-DNA
amounts of as hybridization
yet unclassified and ribosomal
microbial RNA
diversity that nonetheless corresponds to a distinct cluster in was Habitats were coding regions or results in synonymous sub- should be considered as putative or actual spe-
Department of of
convenience taxonomists;
Infectious they
Disease Epidemiology, reflect Imperial
only a extent of DNA hybridization between them, and on their habitats. Habitats were defined using gionssuperimposed
or results inonsynonymous
their habitats. substitutions.
netic lineages, of the mechanisms 2 of differen- (rRNA) sequencing] have helped to define species, Habitats
these dataand (12).Ecological
There are Differentiation
striking differences in stitutions. Niches and Ecotypes
College London, London W2 1PG, UK. Department of Civil have all fueled the controversy
tiny subset of those characters that allow bac- those that show 70% or more DNA hybridiza- an empirical modeling approach. This analysis of how one de- defined
One common using measure
an empirical modeling
of neutral approach.
diversity is the Niches andOne common measure of neutral cies,
Ecotypes depending on the level of genetic differ-
and Environmental
tiation Engineering, Massachusetts
between subpopulations sharing Institute
common of but these
fines methods
a bacterial have(3–8).
species serious limitations and A theclear
amount of sequence
natural criterion diversity
to identify observed clusterswithin of This analysis revealed high levels of specialization diversity is the effective population size N , de- To extendfrom this model, one can population.
consider multiple
teria to use
Technology, differentMAresources
Cambridge, 02139, USA. in 3the environ-
Department of tion are defined as the same species (2, 10). Such revealed high levels of specialization for some effective population size Ne, defined as the size To extend this model, one can consider multiple e entiation the ancestral This
descent, and of the process of adaptation to new cannot reliably assign a large collection of similar evolutionary homologous housekeeping importance, genes we
which in these
might named
want for some populations (e.g., V. ordalii is only found fined as the size of a population evolving in the ecological niches characterized by oftheproviding
selective
ment, and
Biological only capture
Engineering, a smallInstitute
Massachusetts fraction of the cutoffs imply that sequences that cluster together populations (e.g., V. ordalii is only found as
of Technol- of a population evolving in the absence of se- ecological niches characterized by the selective model therefore has the advantage
niches and changing environments. Animalofspe- Genetic
strains toClustering
species (e.g., rRNA sequences are too to species, rangingisfrom
call species, to find 1.2% for S. pneumoniae
ecological features that to as singlethat
free-swimming cells),
true Cambridge,
ogy, diversity in MAthis USA. 4Broad Institute
superkingdom
02139, of life. More MIT with a certain amount of similarity must be from single free-swimming cells), whereas others are lection would generate aswhereas others are
much neutral di- absence
advantages of selection
they conferthat would generate
to specific genes. This aadvantages
as much mechanistic theyunderstanding
confer to specific genes.
of the This is
evolution-
ciesHarvard
and are defined by their
University, morphological
Cambridge, MA 02139, USA. and be- Darwin conserved to resolve that
commented similar“allspecies). 3.0% for S. pseudopneumoniae
rRNA se- distinguish
true classification them from close relatives. and up to 5.0% Among for more generalist (Fig. 1B) and can colonize a wide neutral diversity as is actually observed. Esti- the ecotype model, where genes adapted to
recently, molecular methods [particularly DNA- the same species, and moreover that thisthecutoff more generalist (Fig. 1B) and can colonize a wide versity as is actually observed. Estimates of N is the ecotype model, where genes adapted to ary processes, as well as an organizing principle
havioral
*To whom traits and by
correspondence their
should ability or inability
be addressed. E-mail:to is quence surveys
genealogical” have,
[(9), however, revealed
p. 404]. Taxonomists extra- S. mitis.
have pathogens, The thedistance
ability between
to cause two randomly
a distinctive se-
dis- variety of surfaces, including5 organic9 particles ande mates of Ne for bacteria range from 105 to 109 specific niches cause selective sweeps within
DNA hybridization
interbreed, but suchand ribosomal
categories RNAeasily
cannot (rRNA) be thus value
ordinary is applicable
variety of tomicrobial
all groups of much
life, bacteria of orit variety
lected S. ofmitis
surfaces,
genotypes including
is similar organicto the particles
average for bacteria range from 10 to 10 (14–18). To specific niches cause selective sweeps within for classifying species, that is based on experi-
c.fraser@imperial.ac.uk used sequence relatedness to define cutoff ease has historically been used to define species, zooplankton in the water column (13). Most of the (14–18). To put this into context, the numbers of those niches but not in other niches. In this way
sequencing]
applied to thehave helped
Bacteria or to define (or
Archaea species,
indeedbut to archaea.
uncultured Recent
(1). BeyondMLSAthis, studies,
taxa too which
similar usetothebe and zooplankton
distance between inS.the water column
pneumoniae and (13). Most
S. pseudo- put this into context, the numbers of Vibrio cells those niches but not in other niches. In this mental observations of bacterial populations.
predicted Vibrio populations are deeply divergent Vibrio cells per cubic meter of seawater in tem- the population will undergo adaptation and dif-
these
many methods have serious Instead,
limitations and can- concatenated
distinguished sequences of multiple byhousekeep-
rRNA se- of the predicted Vibrio (5.1%)
populations are implies
deeply per cubic meter of seawater in temperate coastal way the population will undergo8 adaptation However, these observations of repeated
eukaryotic microbes). taxonomists and circumscribed pneumoniae genotypes (2). This from each other, and in 8many cases are congruent perate coastal regions range from 10 to 109 (19), ferentiation while maintaining relatively low levels
not
havereliably
been forced assign to arelylarge collection www.sciencemag.org
on biochemical oftests
similar
and ing geneshave
quences to SCIENCE
discern
revealedclustering patterns
VOLdiversity
further 323 6through among
FEBRUARY divergent
that the2009 usefromof a fixedeachlevel other, and in many
of sequence cases 741
divergence regions range from 10 to 109 (19), which sug- and differentiation while maintaining relatively selective sweeps were made in chemostats,
with named species; however, V. splendidus is a which suggests vast census population sizes of neutral diversity, as selective sweeps confined
strains to species (e.g., rRNA sequences are too populations of closely related taxa,
limited morphological characteristics for this pur- multilocus sequence analysis (MLSA) (2) and for differentiating species would tend to either suggest that are congruent with named species; however, V. gests vast
notable census and
exception population sizes
splits into (>1020closely
numerous ). This low ). Thisofobservation—a
(>1020levels neutral diversity, mismatchas selective
of many whereas natural environments
to each ecotype regularly purge arethemarkedly
populationun-
conserved
pose. Naturally, to resolve
biochemicalsimilarcharacters
species). have rRNAbeen se- species
metagenomic defined by taxonomists
studies (1), and this in many needs
diversity cases splendidus
rejoin S. pneumoniae is a notableand exception and splits into
S. pseudopneumoniae, observation—a mismatch of many orders of sweeps confined to each ecotype regularly stable and
related groups with distinct ecological preferences, orders of magnitude between effective population of any diversity that might have accumulated diverse. How would one detect the
quence
selectedsurveys have, however,
for the convenience revealed thethey
of taxonomists; ex- correspond
to be explained to well-resolved
by theory. Thus, sequence clusters.
practical dif- numerous
or break up closely S. mitis so related groups
that nearly every with distinct
isolate was magnitude indicating
presumably between effective population
recent ecological size purge
radiation size andthe census
population of any diversity
population size (truethatof might
most presence
(Fig. 2A). of selective
Crucially, sweeps
what in diversity
neutral natural bacte-
we do
However,
ficulties, lack these studies and
of theory, alsoobservations
show that there of vast is ecological
a species of preferences,
its own. This is presumably
clearly unsatisfactory. indicating and census
from population
a sympatric size
ancestral (true of (13).
population mostThus,
bac- have accumulated
bacteria (Fig. 2A). originally
studied to date)—was Crucially,used what to rial populations?
observe is predicted Thetomost conclusive
be associated examples
with adapt-
1
Department of Infectious Disease Epidemiology, Imperial no universal
amounts of ascutoff or descriptor
yet unclassified of clusters
microbial that recent ecological radiation from a sympatric
diversity genetic clusterstothat
teria studied date)—was originally
correlate with ecologyused can be to neutral diversity
counter claims we do observe
of neutrality and instead is argue
predicted
that come not The
ive traits. fromability
bacteria but from
of such RNA
selective viruses,
sweeps to
College London, London W2 1PG, UK. 2Department of Civil characterizes
have all fueled a species. Furthermore,
the controversy of how inspection Habitats population
one de- ancestral and Ecological (13). Differentiation
Thus, genetic clusters counter claims of neutrality and instead argue to
discerned. all be associated
genetic variationwith wasadaptive
adaptive traits. The which
(20, 21). mutate
limit the at much
effective highersize
population rateshasthan
beenDNA-
rec-
and Environmental Engineering, Massachusetts Institute of of the
fines a clusters
bacterial does
species not always
(3–8). clearly reveal that
A correlate
clear natural with ecology
criterion to can be discerned.
identify clusters of thatWhat
all genetic
do thevariation wastell
genetic data adaptive
us about (20, 21). ability
mech- However, of there
such areselective
several sweeps
different to limit the based
mechanisms ognizedlifeforforms.
some time been
It has(17, established
23), from
and this model
Technology, Cambridge, MA 02139, USA. 3Department of which level in the hierarchy is more fundamen- evolutionary What do the genetic data tell us about mech- However,
Biological Engineering, Massachusetts Institute of Technol-
importance, which we might want anisms of there are several
population different and
differentiation mecha-the effective population
that can explain size has (Fig.
this mismatch been2).recognized sequences collected over
has been substantially many by
developed years
Cohan the
that and
ogy, Cambridge, MA 02139, USA. 4Broad Institute of MIT tal than any
Genetic other (Fig. 1) (7).
Clustering anisms
to call species,of populationis to finddifferentiation
ecological features and that the nisms that can
evolutionary explain
history thismicrobes
of the mismatchin(Fig. 2).
question? for Whatever
some time (17, 23), are
mechanisms anddriving
this model has population
the differ- colleagues (4, structure
16, 24).ofBecause
the human influenza
it links patternsvi-
of
and Harvard University, Cambridge, MA 02139, USA. As ancommented
Darwin example, Fig. that1A “allshows the relation- evolutionary
true classification distinguish them history fromof close relatives. inAmong
the microbes ques- ThatWhatever
bacteria aremechanisms
organized intoare driving
genetic clustersthe is been substantially
entiation of bacteria developed
into clusters,bythey Cohan
mustand re- rus is predominantly
genetic differentiation withdriven by repeated
adaptation, selec-
and makes
*To whom correspondence should be addressed. E-mail: ships among multiple
is genealogical” [(9), p.isolates of three closely
404]. Taxonomists have tion?
pathogens, That the bacteria
abilityare to organized
cause a distinctive into genetic dis- differentiation of bacteria into clusters, they colleagues (4, 16, 24). Because it links patterns tive sweeps (25) and that the resulting effective
c.fraser@imperial.ac.uk related
thus usedstreptococcal
sequence relatedness species. toStreptococcus
define cutoff clustersease hasishistorically
not, per se, been a very
usedinteresting
to define species, obser- must restrict the accumulation of neutral of genetic differentiation with adaptation, and population size Ne (<100) is very much smaller
742 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
30 31
www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009 741
 and diversity generated only by neutral drift. This ples shown in Fig. 3 differ only in the rate of to recombination will depend more on the accu-
and diversity
version of thegenerated
model wasonly by neutral
dismissed drift.of
because This ples shown in
its homologous Fig. 3 differbetween
recombination only inthetheclusters, to recombination
rate of mulation will depend
of differences more on
at neutral locithethan
accu-at
version of the
association model
with a verywaslow dismissed
estimate because
of popula- homologous
of its all recombination
other parameters being heldbetween the clusters,
constant. mulation loci.
As re- adaptive of differences
The modelsatalsoneutral lociathan
assumed homo- at
SPECIALSECTION association with a very low estimate of popula- all other parameters being held constant. As re-
tion size (14). However, estimates of effective combination increases, we see a distinction be- geneous distribution of polymorphisms across adaptive loci. The models also assumed a homo-
tion size (14).
population size N However, estimates of effective combination increases, we see a distinction be- geneous distribution of polymorphisms across
e are often grossly disconnected
iples of A E1 E2 B Metapopulation structure, in which the popu- using
from established
population
census size Ne ecological
are often
population sizes. criteria,
grossly a hypoth-
It hasdisconnected
proven very Recombination rate relative to mutation
from census population Recombination rate relative to mutation
ype has new and empty lation is divided into patches and where indi- esis that can be
challenging find models Itthat
to tested. sizes. has successfully
proven very
3 0.10 clonal
colonization challenging to find
within viduals disperse between patches, can generate This problem
explain low estimatedof lowmodelsvalues tothat
power Nesuccessfully
ofdetect selection
while pro- 3 0.10 clonal
explain low estimated 0.53 threshold
very low effective population sizes if patches (or, more accurately, tovalues
than of
reject Ne while
neutrality)
basedis pro- a

between
ciation, viding better predictions models on 0.53 threshold
*

between
* turn over (i.e., if patches are only intermittently viding
very
simple
simple
better
general
neutral
neutral
predictions
problem
drift. in
drift.
The
The
than
population models
analysis
analysis
of based
genetics
of
on
that
Bacillus
Bacillus
2 2.00 sexual
2.00 sexual
cts that
* able to support bacterial growth, and if a small does
partlynot didnegate thepredicting
importancemore of adaptation
ecotypes in 2

-9)-9)
this by in
* partly did this by predicting more ecotypes in

(x10
distance
ng bac- number of bacteria are dispersed to colonize evolution,
the model than but rather suggests using
were observed that more work
established
*

(x10
distance
colonization theneeded
model than were aobserved usingthat
established
ould be empty patches) (Fig. 2B) (27). This structure is
ecological if we want
criteria, model-based
hypothesis methods
can be 1

generation
cotypes ecological criteria, a hypothesis that can be 1
well describes the situation for parasites, which to discriminate among different biologically
tested.

generation
tested.

in in
As a re- can colonize a host but are then forced to move plausible explanations
This problem of low power of genetic
to detectdata.selectionIn

change
(or, This problem of low powerneutrality)
to detect selection 0
should
* on because the host develops immunity or dies Table more1 we proposetoa reject
accurately, scheme for performing is a very

change
0
ies, de- (or, more accurately, to reject neutrality) is a very
old and void (17). It also describes any situation where bac- analyses that could
general problem be used genetics
in population to test, develop,
that does

per
general problemimportance
in population genetics that does

per
ntiation
* teria use a limited resource intensively for short and
not validatethedifferent
negate competing modelsinmore
of adaptation evo-

r of of
clusters
not negate the importance ofthat
adaptation in evo- -1
l there-

r rate
lution, but rather suggests more work is

clusters
bursts, followed by dispersal to new resource systematically. -1

rate
hanistic lution, but rather suggests
needed if we want model-based methods to dis-that more work is "Speciation point" for
stable ecotype patches (e.g., colonization of organic particles

Relative
sses, as needed if amongwe wantdifferent
model-based methods to dis- "Speciation
sexual point" for
species
concept criminate biologically plausible
in seawater by Vibrio populations). This meta- Homologous Recombination

Relative
-2 sexual species
ssifying C D criminate
explanations among different biologically plausible -2
population model is fundamentally different One specific of
explanations of
genetic data.
challenge
genetic data.
In Table
to models
In Table
1 we
that
1that
pro-
invoke
we pro-
bserva- pose a scheme for performing analyses could
from the ecotype model because it does not ecotypic
poseused structure
a scheme involves a feature of bacterial
20
Bacteria Phage
predict an association between neutral diversity be to test,fordevelop,
evolution—homologous
performing and analyses
validatethat
recombination—that
could
different -3
ated se- be used
competing to test,
models develop,
more and validate
systematically. different -3
0% 10% 20% 30%
and adaptive traits. we have notmodels yet discussed. Bacterial reproduc-
Population size

whereas 15 competing more systematically. 0% 10% 20% 30%

ble and The relevance of the metapopulation model tion does not involve
Homologous Recombinationthe obligate reassortment Mean genetic distance between clusters
Mean genetic distance between clusters
to the species question is that, although highly of genetic material
Homologous observed in most higher or-
Recombination 3. The dynamics of cluster divergence. The figure summarizes some key results from (15) in a
ence of 10 One specific challenge to models that invoke Fig. Fig. 3. The dynamics of cluster
idealized and simplified, it may capture some of ganisms.
One However,
specific recombination
challenge to amodels does occur in phase-space plot of the geneticdivergence.
dynamics of Thetwofigure summarizes
populations, withsome key results from
recombination (15) in
occurring be-a
lations? ecotypic structure involves feature that invoke
of bacterial phase-space plot of the genetic dynamics of two populations, with recombination occurring be-
ot from 5 the effects of complexity and instability of actu- ecotypicand
bacteria archaea
structure (29) and
involves typically
a feature of involves
bacterial tween them at a rate that is varied for the three different simulations. The y axis shows the rate of
evolution—homologous recombination—that tween them at a rate that isbetween
varied for the three as different simulations. The y distance
axis shows the(xrate of
utate at al ecosystems on population structure. Selective the replacement
evolution—homologous of a short piece of DNA
recombination—that with change of genetic distance the clusters a function of the genetic itself axis).
we have not yet discussed. Bacterial reproduction When changethe of rate
genetic distance between the clusters as a function of the genetic distance itself (x axis).
orms. It 0 sweeps are predicted to be inevitable in simple, the
does homologous
we have notnot segment
yet discussed.
involve the obligate from reassortment
Bacterial another strain.
reproduction of converge.
of change is positive, the populations will diverge genetically; when negative, they
When the rate The of change of
direction is positive,
change for the each
populations
scenario willisdiverge
shown genetically; when negative,
by arrows color-coded they
to each
ollected 0 20 40 60 80 100 stable environments but not in complex meta- Recombination
does not involve becomes
the less
obligate probable
reassortment
genetic material observed in most higher orga- scenario. withof converge. For Thelowdirection of change for each scenario is shown by arrows color-coded
recombination rates, the populations are effectively clonal and always diverge to each
cture of Time populations [a point partly addressed in (28)]. A increasing
genetic However, sequence
material observeddivergence
in mostdoes between
higher the
orga- scenario. For As
lowthe recombination
metapopulation may evolve, differentiate, and
nisms.
donor
nisms. and the
However,
recombination
recipient (30,
recombination 31), which
does
occur
reduces
occur
in (green
in line). recombinationrates,rate the populations
increases, are effectively
the cohesive clonal
effects of and alwaysslow
recombination diverge
the
y driven Fig. 2. Different models of microbial evolution that lead to low values of Ne. (A) The ecotype bacteria and archaea (29) and typically involves rate (green line). As the recombination rate increases, the cohesive effects of
of divergence, until a threshold is passed (red line) and the populations become effectively recombination slow the
hat the adapt without global selective sweeps. Diver- but does
bacteria not archaea
and eliminate
of a(29) recombination
and typically between
involves rate of indivergence,
model of bacterial population differentiation. The tree shows a single bacterial lineage that dif- the replacement short piece of DNA with sexual the sense untilthat athethreshold is passed
populations (red line)
no longer and For
diverge. the recombination
populations become effectively
rates above this
100) is ferentiates into two sublineages (E1 and E2) that differ in some aspect of their ecology. Periodic sity lost by a local selective sweep in one patch closely
the related species.
the replacement
homologous of a short
segment Because of
of such
pieceanother
from inter-
DNAstrain. with sexual in the sense that the populations no longer diverge. For recombination rates above this
level, the fate of the two populations will depend on how genetically distinct they are at the outset.
acteria. selection (a selective sweep) occurs at the points marked by asterisks and eliminates almost all of may be rescued and reintroduced from other species
the recombination,
homologous segment any given
from
Recombination becomes less probable with in- If isolate
another within
strain. level,
theythe
arefate of the
within thetwo populations
“speciation will then
point,” depend on how genetically
recombination distinct
will cause themthey are at the
to merge. outset.
If they are
genetic the diversity that has arisen since the last episode of periodic selection, which is shown by the patches. The ecotype model, with its predicted acreasing
speciessequence
Recombination is almostbecomes certain
divergence lesstobetween
containthe
probable at donor
with least
in- farther
If they are within the “speciation point,” then recombination will cause them
away than this “speciation point,” they will continue to diverge from each other. These to merge. If they are
models dashed branches (diversity purged by periodic selection) or solid branches (existing diversity) on monophyletic relationship between niche and some
and thegenetic
creasing sequence
recipient material
(30, 31),that
divergence whichisbetween
characteristic
reducesthe butdonorof curves
does farther are
away this “speciation
than using
derived the model point,”
described theyin will
(15).continue to diverge from each other. These
karyotic the tree. As the two populations are ecologically distinct (i.e., ecotypes), periodic selection in one genotype, may therefore not be an appropriate other
and the closely
recipientrelated
(30, species.
31), which Hence,
reduces whereas
but does it curves are derived using the model described in (15).
alogies, sublineage does not influence diversity in the other sublineage and vice versa. Each ecotype can model of speciation in complex ecosystems. was once thought that bacteria do not form spe-
iven by therefore diverge to become separate species. Reproduced from (24) with permission. (B) A meta- 744 cies in the eukaryotic sense because they 6 FEBRUARY
do not 2009 VOL 323 SCIENCE www.sciencemag.org
744 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
ngitudi- population. Patches of varying size (gray circles) are vacant (empty) or may be colonized by a Choosing Between Models recombine at all (32), one current view is that process that reduces the rate of recombination Illegitimate Recombination and Gene
ons, as single genotype randomly acquired from another patch. Strains may diversify within a patch (as It has proven difficult to discriminate between they do not form species because they recom- between them—for example, a period of allopa- Content Variation
shes in shown by different colors representing distinct genotypes), which may colonize empty patches as models of population differentiation that fo- bine too much (5). try or ecological differentiation. The speciation Illegitimate recombination or gene acquisition
changes described above. A characteristic of this sort of metapopulation is patch turnover, in which patches cus on ecotypes or metapopulations. For ex- In asexual clonal organisms, even in the point is the amount of divergence between clus- is another unusual feature of bacteria. In this
occasionally become unable to support colonization and their inhabitants are removed (solid gray
ological ample, the ecotypic structure of a soil Bacil- absence of any selective pressure, clusters will ters that needs to accumulate to prevent them case, genes or clusters of genes are acquired
circles). (C) A neutral model with small population size. Different genotypes (different colors) arise
by mutation or recombination and increase or decrease in the population by random drift. For lus has been modeled to predict a priori which spontaneously split into multiple lineages or from returning to a single cluster if the barriers that typically have no homolog(s) in the recipi-
some purposes, this simple model is an adequate effective description of the more complex pro- sequence clusters were ecotypes, and hence “daughter” clusters (15). However, under cer- to recombination are removed. A recent study ent strain. The importance of this phenomenon
cesses represented in (A), (B), and (D), and of other more complex evolutionary models not de- which ones should be associated with specific tain circumstances recombination can prevent hypothesized that two related Campylobacter is evident in the clear and ubiquitous signature
scribed in this review. (D) Predator-prey dynamics and population bottlenecks. Regular population ecological properties (16). Some clusters are this, and we can hence divide the bacteria into species are currently undergoing this process of such events in the growing body of genomic
del with associated with certain phenotypic traits, such “sexual” and “nonsexual” species. This effect, of merging into a single species as a result of data. These are identified by differences in the
bottlenecks can drastically shrink the effective population size. In this case, bacteria-phage
ot niche predator-prey dynamics are simulated with a classical Lotka-Volterra model, which can generate as a propensity to grow on shady north-facing described at greater length elsewhere (15), is changes in their environment (33). characteristics of the acquired DNA and that of
bottle- oscillations in population size of any amplitude. Population sizes and time axes are in arbitrary slopes or sunny south-facing slopes. However, summarized in Fig. 3, which shows the rate The above insights were reached using mod- the host strain, for example, in base composition
whole units for illustrative purposes only. this model fitted no better (and in fact slightly at which two clusters diverge over time—that els based on the assumption that genetic varia- or codon usage; in most cases, the donor of the
le indi-
worse) than a version of the model with several is, the increase in the mean genetic distance tion is neutral. Although this is obviously not DNA in question is unknown. Gene acquisition
ll other
subpopulations and diversity generated only between them. If this becomes negative, then always an appropriate assumption, it is plau- leads to genomes being punctuated by stretches
induce (27). This structure well describes the situation does not predict an association between neutral
than observed for bacteria. The use of longitu- Bottlenecks, Metapopulations, and Local by neutral drift. This version of the model was the two clusters will stop diverging and instead sible that the number of loci explicitly involved of foreign DNA. The largest of these (which
ks will for parasites, which can colonize a host but are diversity and adaptive traits.
dinal ecological and genetic data to distinguish Extinctions dismissed because of its association with a very converge. The three examples shown in Fig. 3 in adaptive ecological differentiation will be may be many kilobases in length) were initially
pulation then forced to move on because the host develops The relevance of the metapopulation model to
between competing models of evolution has a The essential element of the ecotype model low estimate of population size (14). However, differ only in the rate of homologous recom- small, and thus that in an unstable landscape, termed “pathogenicity islands,” because the new
ded into immunity or dies (17). It also describes any the species question is that, although highly ide-
etween long pedigree
situation whereinbacteria
eukaryotic
use abiology
limited (26). On with
resource alizedrespect to limiting
and simplified, neutral
it may diversity
capture some isof not
the estimates of effective population size Ne are of- bination between the clusters, all other param- genomic barriers to recombination will depend functions encoded by the imports were often
e popu- the basis offor
intensively these
shortanalogies, any inference
bursts, followed of a niche
by dispersal effects adaptation
of complexityper se,
andbut rather the
instability of effec-
actual ten grossly disconnected from census popula- eters being held constant. As recombination in- more on the accumulation of differences at neu- involved in virulence, but a better term is “ge-
patches population structure
to new resource driven(e.g.,
patches by selective sweeps
colonization of tive bottleneck
ecosystems caused by structure.
on population the replacement of
Selective tion sizes. It has proven very challenging to find creases, we see a distinction between a “clonal” tral loci than at adaptive loci. The models also nomic islands” as the phenomenon is far from
acterialorganic particles in seawater by Vibrio popula- sweeps are predicted to be inevitable in simple,a
would require good longitudinal data from natu- the whole population by descendants from models that successfully explain low estimated organism in which clusters are predicted to di- assumed a homogeneous distribution of poly- limited to pathogens (36, 37). Although it is
eria are ral bacterial
tions). populations, as well
This metapopulation model as is
observations
fundamen- single individual andbutthenotresulting
stable environments in complexextinction
meta- values of Ne while providing better predictions verge (the green line) and a “sexual” organism morphisms across the genome, and violation hard to quantify the selective impact of import-
ig. 2B) of episodic crashes in diversity causally associ-
tally different from the ecotype model because it populations [a point partly addressed inmecha-
of all other lineages (Fig. 2A). Other (28)]. than models based on simple neutral drift. The (the blue line) in which they are predicted to be of this may alter the tempo and mode of these ing any given gene(s) into a new background,
ated with genetic changes and not associated nisms that induce or involve regular population analysis of Bacillus partly did this by predicting held together by recombination. For “sexual” processes (34, 35). the occasional ability to gain a new adaptation
with changes in ecological covariates. bottlenecks will also restrict neutral diversity. more ecotypes in the model than were observed species, the divergence of clusters requires a in this fashion—such as a new metabolic capa-
ww.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009 743
32 33
the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in
The importance of this phenomenon is evident in between them by mobile elements. The evolu- different genera on the basis of their specific char-
in the growing body of genomic data. These are loosely coupled with that of any particular gene content and recombination. In any case, no
the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in
identified by differences in the characteristics of species or strain in which they are found, and biologist would deny the importance of ecology
in the growing body of genomic data. These are loosely coupled with that of any particular gene content and recombination. In any case, no
the acquired
identified DNA by and that of inthethehost
differences strain, for of they
characteristics are maintained
species or strain in throughwhich they selection
are found, by andthe biologist
to what would we observe, deny thebut it may not
importance be easy to
of ecology
example,
the in base
acquired composition
DNA andof thator co-
of the host strain, for they are maintained through selection by the to what we observe, incorporate but it mayit in a fashion
not beineasy that
to is
bility
don usage; inormosta new mode
cases, the trans-
donor of ticular species
convenient for ortaxonomists.
strain which None- these alternatives. One clear result from all of niches within (for example) the nasopharynx or 21. R. Milkman, Trends Biochem. Sci. 1, N152
example,
mission for in base composition or co-
a pathogen—may incorporate
they are found, it inand a fashion
they arethat main- is the studies discussed here is that the underlying gut is difficult, and studies of the relationships (1976).
the DNAdon in question
usage; in most cases,is unknown.the donor of theless,
convenient population
for taxonomists. geneticists None-may 22. K. C. Atwood, L. K. Schneider, F. J. Ryan,
be of enormous importance in tained through selection by the theoretical questions concerning species will between bacterial populations and ecology may
Gene theacquisition
DNA inleads question to genomes
is unknown. have little
theless, population choice geneticists
but to tackle may the Proc. Natl. Acad. Sci. U.S.A. 37, 146 (1951).
terms of speciation. habitat to which each host strain is not be answered in the absence of more detailed be more fruitful for some environmental spe-
being Gene
punctuatedacquisition by leadsstretches to genomes of question
have little of defining
choice but bacterial
to tackle speciesthe 23. B. R. Levin, Genetics 99, 1 (1981).
Perhaps even more striking adapted. In the case of very mobile genetic-environmental mapping. Moreover, cies where the categorization of niches is a more 24. F. M. Cohan, E. B. Perry, Curr. Biol. 17, R373
foreignbeing
DNA. punctuated
The largest by of stretches
these of question
or, at of
the defining
very bacterial
least, species
populations.
is the amount of variation in elements—for example, plasmids some guidelines for the types of ecological tractable enterprise. Hopefully, we will soon ob- (2007).
(whichforeign DNA. largest ofintheseEcological
Thekilobases or, at the veryareleast,
Whether populations.
maycontent
gene be many
revealed by mul- factorEcological
b encoding we resistance estimating
to antibioticseffective studies that will be most informative are emerg- tain richer data sets that map bacterial diversity 25. A. Rambaut et al., Nature 453, 615 (2008).
length)(which
were may be termed
initially many kilobases“patho- in Whether
population we size are estimating
from neutral effective
diversity
tiple genomes from the same factor b or heavy metals—the ecological ing. Most important, the ecological data collect- onto ecology and provide a way to distinguish 26. R. A. Fisher, E. B. Ford, Heredity 1, 143
length)
genicity islands,”were because
initially termed the that new “patho- population
or choosing size from neutral diversity
an appropriate set of (1947).
species, which implies specificity determined by these ed must be relevant to the niche boundaries of among various models of population differen-
genicity
functions encoded islands,” because
by the occurs
importsatwere the new orstrains
choosing to test anforappropriate
positive set of at
selection 27. M. Slatkin, Theor. Popul. Biol. 12, 253
gene acquisition a accessory loci may have no link the populations studied. And if genetic groups tiation and speciation, including those based on
functionsin
often involved encoded
virulence,by the butimports
a bet- were strains
a locus to oftestinterest,
for positive species selection at
definitions (1977).
surprisingly
often involved high frequency.
in virulence, butIta bet- a tolocusthe of interest, we
sequence speciesobserve using
definitions do not map exclusively onto sampling catego- ecotypes or metapopulations. 28. J. Majewski, F. M. Cohan, Genetics 152, 1459
is now
ter term
ter termcommonplace
is “genomic islands”
is “genomic islands” to speak
as the
as the arehousekeeping
are implicit ingenes
implicit in much
much(Fig. of the 4).analytical
of the analytical ries (as is likely to be the case), more complex (1999).
of
phenomenon the “core”
is far genome,
from
phenomenon is far from limited to which
limited to toolkit of population
toolkit of population genetics.
genetics. statistical models will be needed to identify and 29. E. J. Feil, B. G. Spratt, Annu. Rev. Microbiol.
encodes
pathogens (36, 37). fundamental
Although func-
it is hard Identifying
Distinguishing Mechanisms among and mecha- describe the underlying niche structure. Lon- 55, 561 (2001).
pathogens (36, 37). Although it is hard Distinguishing among mecha- References and Notes
30. J. Majewski, F. M. Cohan, Genetics 153, 1525
tions
to quantify
to shared
the
quantify the by
selective all
impact
selective membersof im-
impact of im- Delineating
nisms
nisms ofofpopulation Speciesdifferentiation
population differentiation gitudinal studies that measure the dynamics of 1. J. Handelsman, Microbiol. Mol. Biol. Rev. 68,
(1999).
ofanya species (and, gene(s)
it into
should goa new What do ultimately
we want comesfrom bacterial ecological associations over time will also be 669 (2004).
portingporting given
any given gene(s) aintonew Ecological
Ecologicalfactor
factoraa inin bacteria
bacteria ultimately comes down down to to 31. J. Majewski, P. Zawadzki, P. Pickerill, F. M.
withoutthesaying, otherabilityrelated species? Do weofneed theoretical helpful to determine how transient natural habi- 2. W. P. Hanage, C. Fraser, B. G. Spratt, Philos.
background,
background, occasional
the occasional to to
ability testing
testing thethe ability
ability of different
different modelsmodels Cohan, C. G. Dowson, J. Bacteriol. 182, 1016
4. Differences between
betweencore coreandandauxiliary
auxiliary genes.
genes. This schematic
schematic toto Trans. R. Soc. London Ser. B 361, 1917
species),
gain a new
gain newonto
aadaptation which
in thisinis
adaptation bolted
fashion—
this fashion—Fig.Fig. 4. Differences consistency
explainhighly
explain evenvariable
highly atvariable
the expense patterns
patterns tats are, and thus how likely bottlenecks are to (2006).
(2000).
the “auxiliary” or “accessory” illustrates
illustratesthe therelationships
relationships between
between three
three species
species in
in “ecotype
“ecotype space,” within
space,” of taxonomic practicality, incorpo- result. Finally, whole-genome sequences from 32. S. T. Cowan, in Microbial Classification,
such as a new metabolic
such as a new metabolic capability capability within andand between
between genetic-ecological
genetic-ecological 3. M. Achtman, M. Wagner, Nat. Rev. Microbiol.
12th Symposium of the Society for General
genome,
or a new
or amode
new mode composed
of transmission of genes
of transmission for afor ashown shownhereherein two
in two dimensions,
dimensions,and anda amobile
mobilegene gene common
common to to all
all three.
three. clusters rating both
clusters (Fig.
(Fig. “clonal”
1).1).It Itisandis “sexual”
stillstill unclear
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Microbiology, G. C. Ainsworth, P. H. A.
and operons The The
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are shown
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as solid
solid lines in
in red,
red, blue,
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pathogen—may
pathogen—may bethatofbe may or may
of enormous
enormous im- im- and green. The part of the ecological space where the shared mobile gene populations
whether these
these into a single
patterns
patterns areare theo-
main- main- will be useful in dissecting the roles of the aux- Sneath, Eds. (Cambridge Univ. Press,
notinbetermspresent and green. The part of the ecological space where the shared mobile gene tained (2002).
portance
portance of in
in terms all isolates. It
of speciation.
speciation. is selected in each species
reticalby
tained framework?
by gene gene flowflowOne
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5. W. F. Doolittle, R. T. Papke, Genome Biol. 7,
Cambridge, 1962), pp. 433–455.
seems likelymore that more
such striking
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shownbybyaadashed dashedpurple
purple line
line and
and overlaps
overlaps theoretical
Perhaps Perhaps
even even striking is theis the all three species ranges. Examples of (circular) genomes from each species and andwhat whattheconcept
theeffecteffect is
of to consider
population
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33. S. K. Sheppard, N. D. McCarthy, D. Falush,
ryof genes ofhelp toindetermine the all three species ranges. Examples of (circular) genomes from each species structure species as
is. the
The arena
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amountamount variation variation genein genecontent content with and without the purple mobile element are also illustrated. Note
with and without the purple mobile element are also illustrated. Note that genetic that structure is. The joint distribution 6. D. Gevers et al., Nat. Rev. Microbiol. 3, 733
34. A. C. Retchless, J. G. Lawrence, Science 317,
specific
revealed
revealed by multipleecological
by multiple genomes properties
genomes fromfromfor each for each species, the locus is not selected for all isolates, and its evolu- individuals
genetic and and are
ecological similar
ecological data enough,
datacancan be be different study systems, these would inevitably (2005).
1093 (2007).
of the organism.
species, For implies that tionaryspecies,
example, the locus is not selected for all isolates, and its evolu- or interbreed enough,
above that 7. M. F. Polz, D. E. Hunt, S. P. Preheim, D. M.
the
the same same
species, whichwhich implies that tionary fatefate is
is uncoupled from that of each host species, because if one used,
uncoupled from that of each host species, because if one species used,asasdescribeddescribed above forindi-
for Vibrio
Vibrio form a good basis for identifying fundamental
Weinreich, Philos. Trans. R. Soc. London Ser.
35. K. Vetsigian, N. Goldenfeld, Proc. Natl. Acad.
a group
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define compete
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gene acquisition occurs at a sur- undergoes a selective sweep or goes extinct, the mobile gene may be species (13), to define populations B 361, 2009 (2006).
lum has recently
prisingly been hypoth-
high frequency. It is now reintroduced from one of the other species. Examples of such distributed without rectly for making reproductive
a strong success. theoret- In the foregoing we have emphasized eco- 8. D. B. Rusch et al., PLoS Biol. 5, e77 (2007).
36. A. Tuanyok et al., BMC Genomics 9, 566
prisingly high frequency. It ofisthe now “core”reintroduced without makingto aeither strong theoret-
esized to adapt
commonplace to different
to speak loci includefrom drugone of the determinants
resistance other species.inExamples
pathogensof(e.g., suchb-lactamase
distributed ical Practical
commitment advances building of these on type and metapopulation models, but there are 9. C. Darwin, The Origin of Species (Penguin
(2008).
commonplace to speak of thefundamental
“core” loci genes) include drug resistance determinants in pathogens (e.g., b-lactamase ical commitment to either of these 37. U. Dobrindt, B. Hochhut, U. Hentschel, J.
areas of an acid mine drainage
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alternatives. One clear result from others that deserve consideration—notably the Classics, London, 1985).
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system byshared
functions shuffling
by allof chro- of agenes)
members genes andmayheavy metal resistance
be transferred among strains in environmental
and species by organisms.
conjugative These plas- allwill of the onlystudiescome discussedwhen these hereare is epidemic clonal model (42) and the impact of 10. E. Stackebrandt et al., Int. J. Syst. Evol.
38. P. Wilmes, S. L. Simmons, V. J. Denef, J.
functions shared
mosome(and,
species by
segments
all members
enriched
it should ofin
go without a genes may be transferred among strains
mids or other mobile elements (including transducing phage). and species by conjugative plas- all of
developed
that the
the underlying studies discussed
into theoretical
explicit models ques- is
here phage epidemics causing classic Lotka-Volterra Microbiol. 52, 1043 (2002).
F. Banfield, FEMS Microbiol. Rev. 33, 109
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noncore genes (38, 39). We
other related species), onto tions concerning
and model-based algorithms that species will not be boom-bust dynamics (43) illustrated in Fig. (2009).
tions (2002).
saying,which
other is related
bolted
should, however, be aware species),
the “auxiliary” onto or “accessory” habitat to which each host strain is adapted. In answered in are tested and refined on a wide be
the concerning
absence of more species
detailed will
genetic- not 2D—and it is possible, even likely, that more 12. J. C. Arbique et al., J. Clin. Microbiol. 42,
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which genome,
is bolted
that changes thein“auxiliary”
composed coreof genes genesormay and“accessory”
operons
also leadthatto habitat
the
tic of todifferent
case which
of very each host
mobile
levels strain is adapted.
elements—for
of ecological exam-
specificity, answered
In environmental
range of data.in the absenceMoreover,
mapping.
Alternatively, of more
it maydetailed
some
be sensible genetic-
guide- than one of these mechanisms may be relevant (2008).
4686 (2004).
genome,may or may
composed not be
of present
genes in
and all isolates.
operons It seems
that the ple,
caseplasmids
of very encoding
mobile resistance
elements—for to antibiotics
exam- or lines for
environmental the types of
mapping. ecological Moreover,studies that
some will
guide- 40. E. Bantinaki et al., Genetics 176, 441 (2007).
ecological differentiation, a phenomenon well ranging from highly conserved core functions to suggest an ad hoc application of principles to any given problem in speciation and cluster 13. D. E. Hunt et al., Science 320, 1081 (2008).
41. R. A. Welch et al., Proc. Natl. Acad. Sci.
may orlikely
may that
not such
be auxiliary
present in genes
all help
isolates. to
It determine
seems ple, heavy
plasmidsmetals—the
encoding ecological
resistance specificity
documented in experimental studies of bacteria that are essential for growth in all environments to different genera on the basis of their specificwill
to antibiotics deter-
or be most
lines forinformative
the types ofare emerging.
ecological Most
studies impor-
that formation. Distinguishing among these mecha- 14. See supplementary information in (16) for a
U.S.A. 99, 17020 (2002).
linka tant, the ecological dataarecollected statistical comparison of the ecotype model
the
likely that specific
growing ecological
suchinauxiliary
structured genesproperties
help toofdetermine
environments the(40).
organism. heavy mined
to loci by
that
metals—thethese
are accessory
involved
ecological loci may have no
withspecificity
adaptation to
deter- characteristics,
be most informative including the extentmust
emerging. ofMost be impor-
variation rel- nisms is the bacterial species challenge (Table 42. J. Maynard Smith, N. H. Smith, M. O’Rourke,
For example, a group of related Leptospirillum to the sequence clusters we observe using house- evant to the niche boundaries of the populations with an effective neutral model and an
the specific Estimates
ecological vary, depending
properties of the on organism.
the genomes mined specific
by thesehabitat. Some loci
accessory narrowmayniche-specific
have no link in gene
tant, thecontent
ecological and recombination.
data collected In must
any case, be rel- 1), described in 1991 by John Maynard Smith B. G. Spratt, Proc. Natl. Acad. Sci. U.S.A. 90,
implicit estimate of Ne.
has recently
that are available,
For example, a group been of hypothesized
butrelated
to adapt to dif- keeping
as littleLeptospirillum
as 40% of genes to the genes
genes (Fig. 4).we observe using house- studied.
may beclusters
sequence distributed across species, being no toAnd
biologist
evant thewould if genetic
niche deny
groups do
the importance
boundaries of not map ex-
of ecol-
the populations as follows: “Ecotypic structure, hitch-hiking, 4384 (1993).
15. C. Fraser, W. P. Hanage, B. G. Spratt, Science
43. K. H. Hoffmann et al., FEMS Microbiol. Lett.
has recently in all sequenced
hypothesized to adapt to dif-of a transferred between them by mobile elements. clusively
ferent areas of an acid mine drainage system by keeping genes (Fig. 4).
may bebeen present genomes ogy to what
studied. onto sampling categories (as is likely
And weifobserve,
geneticbut it maydonot
groups notbemap easy ex- and localized recombination can explain the 315, 476 (2007).
273, 224 (2007).
shuffling of chromosome segments enriched in Identifying Mechanisms and to be the case), more complex statistical models 16. A. Koeppel et al., Proc. Natl. Acad. Sci.
ferent named
areas ofspecies an acid(41). mineWe may consider
drainage system by genes Delineating
The evolutionary Species fate of such genes may hence to incorporate
clusively onto it in a
sampling fashion that
categories is convenient
(as is likely observed patterns of variation. The difficulty, of 44. We thank T. Connor and S. Deeny for
noncore genes (38, 39). We should, however, be Identifying Mechanisms will be needed to identify and describe the under- U.S.A. 105, 2504 (2008).
within a named species as being characteris- be only loosely coupledand with that of any par- for taxonomists. Nonetheless, population ge- course, is that the model is sufficiently flexible
shuffling
noncore
Speciation
of chromosome segments enriched in
aware that changes in core genes may also lead to What do we want from bacterial species? Do we lying niche structure. Longitudinal studies that
genes (38, 39). We should, however, bewell Delineating Species
to be
neticists
the
will be needed
case),
may have
more complex
little choice
to identify
statistical
but to tackle
and describe
models
the the
under- to explain almost anything. To test the hypoth-
17. J. Maynard Smith, Proc. R. Soc. London Ser. useful discussions. Supported by University
Research Fellowships from the Royal Society
ecological differentiation, a phenomenon need theoretical consistency even at the expense measure the dynamics of ecological associations B 245, 37 (1991).
question of defining bacterial species (C.F. and W.P.H.), a program grant from the
aware documented
that changes
Table 1. A proposed in core genes
in experimental strategy may also lead
for developing
studies to What do
of bacteria andofvalidating we
taxonomic wantmodelsfrom bacterial
of bacterial
practicality, species? Do
evolution both
incorporating we
that over lying
18. H.timeniche
Ochman, structure.
willA.also C. Wilson,
be helpful Longitudinal
in Escherichia coli andathow
to determine or,
studies thethat esis of ecotypic structure, we need to know the 18. H. Ochman, A. C. Wilson, in Escherichia
very least, populations. Wellcome Trust (B.G.S.), grants from the
ecological
mightdifferentiation,
growing eventually
in structured be used a phenomenon
environmentsto classify (40). well diversity
genetic need theoretical
“clonal”dataand consistency
and“sexual” evenfoundation
provide populations
a firm at into
the expense measure
for a transient
a single the
Salmonella
natural habitatsWhether
dynamics
typhimurium: Cellular
are, andandwe
of ecological are
Molecular
thus how estimat-
associations
Biology,
likely distribution of electrophoretic types [i.e., geno- coli and Salmonella typhimurium: Cellular
U.S. Department of Energy Genomes to Life
ing and Molecular Biology, F. C. Neidhart, Ed.
documented
bacterial in species
Estimates experimental
vary,concept.
dependingstudiesonofthe bacteria
genomes of theoretical
taxonomicframework? practicality, Oneincorporating
unifying theoretical overeffective
both bottlenecks F. C. Neidhart,
time arepopulation
will Ed. (ASM Press,
also
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helpful from
Finally, toneutral
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whole-genome
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sity pp. 1649–1654.
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available,environments
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is to“sexual” species as theinto arena a within transient
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 is admitted and accepted as a member of a host by testsmall is higherlarger
thaninthethe other
central species because of the
critical assessment of the scenarios produced of forest
which refugia in the southernmost range by of magnitude
7. K. Schönrogge et al., J. Chem. Ecol. 30, 91 (2004). Audio S1 to S4
phylogeographic approach is a powerful documents a replacement of forests (Bahia) refugium
society, it mimics adult ant acoustics (particu- 8. T. Akino, J. J. Knapp, J. A. Thomas, G. W. Elmes, Proc. R. 22 July 2008; accepted 28 November 2008 modeling of species’ distributions
assemblage-scale responses under to palaeo-
former environ- grasslands in the southern Atlantic forest during relative to the less stable (southern) portion of the
larly queens) to advance its seniority toward the Soc. London Ser. B 266, 1419 (1999). 10.1126/science.1163583 climates (7). mental change and thereby provides a means for the LGM (14, 18) and suggests the occurrence of forest. Diversity of H. faber in this southern area
REPORTS

Distribution
critical assessment
The palaeomodeling method of the scenarios pre-
intersects produced by small forest refugia inSpecies the southernmost rangeMap of ofispredicted
higher than the otherCurrent
species&because of the

Modeling
Diversity
’s hier- 9. J. A. Thomas, G. W. Elmes, J. C. Wardlaw, Proc. R. Soc. dicted species’modeling
distributionsof species’
underdistributions
current condi- under palaeo- occurrence stable areas historical climate
in persistence
tropical biomesandhavehence diversity,
usefully employedtheypost
leadhoc
to niches. H. albomarginatus
Inclimatic climates (7). andLate H. Quaternary
faber, the data (putative refugia) data
mimicry
Stability Predicts Genetic Diversity in
London Ser. B 265, 1895 (1998). tions and extremes of the

Distribution
phylogeographic predictions for both individual extension
(6000 yearsofbeforethe The palaeomodeling method intersects pre-
predicted São Paulo refugium

Modeling
10. G. W. Elmes, J. C. Wardlaw, K. Schönrogge, J. A. Thomas, Species Map of predicted Current &
palaeoclimate models of species and habitats to

Diversity
lack the present, or 6 kybp, and 21 kybp)
dicted species’ distributions under current condi- occurrence stable areas historical climate
and of-
Entomol. Exp. Appl. 110, 53 (2004).
provide and assemblages
species insights about processes(codistributed taxa;
shaping genetic westward
to predict into areas theofand
tions neighboring
stability Cerrado
(regions
climatic extremes thebiome
of in which
Late Quaternary data (putative refugia) data

. the Brazilian Atlantic Forest Hotspot

11. Materials and methods are available as supporting
material on Science Online. Fig.
and 1).
predictions
Field
species sampling
diversity
to cover
(5, 7).is driven
Building by
on the
both predictedofrefugia
model
them, we
and
reflects
species model
Models
overprediction
are predicted
period)ofand
(6000
habitat
years tobefore
occupy
stability
(fig.irrespective
present,
ofthrough
S2)or 6(14).
kybp, and
(7, 14). fluctuat-
of21 kybp) Spatially explicit hypotheses Re:

Formulation
first map the palaeodistribution endemic time to predict
unstable areas
areas stability (regions
Becausein which

Hypothesis
species 12. P. J. DeVries, R. B. Cocroft, J. A. Thomas, Biol. J. Linn.
Soc. 49, 229 (1993). 1 2 unstableto(recently
species identify colonized)
temporallyareas,stableparticularly
(refugial) ing climatesmaps
the stability correctly
species predict
raiseare patterns
predicted
specific to occupy
hypotheses of phylo-
irrespective of
about Spatially explicit hypotheses Re:
li (12): Ana
13. F.Carolina Carnaval, Michael
J. Acoust.*Soc. Am. 109,J.3080
Hickerson, Célio F. B. Haddad,3

Formulation
in time
the period) and unstable areas (7, 14). Because

Hypothesis
Roces, J. Tautz, (2001).
studied Miguel T. Rodrigues, 4 1 and unstable previously
emphasizing undersampled
(recently colonized) areas.for
regions If geography
regional differences Brazilian
in Atlantic
persistence and rainforest
hence di-
14. R. Hickling, R. L. Brown, Craig
J. Acoust.Moritz
Soc. Am. 108, 1920 the stability maps raise specific hypotheses about spatial-temporal patterns
nsals or (2000). the approach
species correctly
occurrence, which are thencurrent
predicts patterns
validated with (Fig. 2 and
versity, theyfigs.
lead S3 todifferences
S5). In all
to phylogeographic
regional species,
predictions
in persistence high
and hence di- distribution of
of colonization
congruence
with ants 15. H. Markl, B. Hölldobler, Behav. Ecol. Sociobiol. 4, 183 of biodiversity
multispecies at the data.
molecular regional
Going scale,
beyondspecies
the levels
for bothof individual
divergence and
species population
and structure
assemblages
versity, they lead to phylogeographic predictions are
(co- genetic diversity
distribution of
spatial-temporal patterns
and/or vicariance
across taxa
congruence
Biodiversity hotspots, representing regions with high species endemism and conservation threat, of colonization
e acous- (1978). should consistently
traditional show (i) approach,
species-by-species higher genetic di-
the mo- observed
distributedacross
taxa; refugia
forFig.
both1). (Tamura-Nei
Field
individual sampling
species and corrected
isassemblages
driven (co- genetic diversity
and/or vicariance
across taxa
have
16. H.been
Markl,mapped globally.
Z. Vgl. Physiol. 60, 103Yet, biodiversity distribution data from within hotspots are too sparse
(1968).
lthough for
17. effective conservation
H. Markl, Science 149, 1392in(1965).the face of rapid environmental change. Using frogs as indicators, versity
lecular within
analyses and among
contrast populations
the in refugia
fit of assemblage- distances
by the model (20):predictions
4 to 7% between
distributed to coverBahia
taxa; Fig. 1). Field and Per-
sampling
both predicted is driven
by the model predictions to coverareas,
both predicted
and simultaneous Bayesian analyses of multispecies relative to unstable areas, because of long-term nambuco refugia, 1% (recently
between the nearby Bahia
s attracts 18. D. A. Grasso,
level data to the spatially explicit demographic refugia and unstable colonized) Sampling across predicted stable and unstable areas
ecological nicheA. models
Mori, F. Leunder
Moli, M.paleoclimates,
Giovannotti, refugia and unstable (recently colonized) areas, Sampling across predicted stable and unstable areas
A. Fanfani, Ital. J. Zool. 65, 167 (1998). persistence
scenarios and population
suggested by the climate-based genetic
structure; (ii)models. and São Paulo
particularly refugia
emphasizing in H. faber).
previously Similarly,
undersam- in

Validation
s to sig- molecular data, we compare alternative hypotheses of assemblage-scale response to late particularly emphasizing previously undersam-

Validation
We apply
signature of this approachexpansion
population to one of in theunstable
world’s all taxa thereIfare multiple, divergent
approachclades with-

Model
19. T. C. Scott-Phillips, J. Evol. Biol. 21, 387 (2008). pled areas. the approach correctly predicts cur-
a basal

Model
Quaternary climate change. pled areas. If the correctly predicts cur-
20. K. G. Schurian, K. Fiedler, Nachr.This reveals
Entomol. a Apollo
Vereins hotspot within the Brazilian Atlantic forest hotspot.
most species-rich, yet notoriously endangered and
the southern Atlantic forest was climatically unstable relative to the central region, areas, reflecting multispecies colonization from in the Bahia region, agreeing with model-based scale,
t expect rent patterns of biodiversity
rent patterns of at the
biodiversityregional
at the scale,
regional
We show
14, 339 that
(1994). Genetic testsof of Assemblage-scale
understudied ecosystems: the Brazilian Atlantic Genetic tests Assemblage-scale
which served as a large climatic refugium for neotropical species in the late Pleistocene. This sets adjacent refugial regions after the Last Glacial predictions of species
a large refugium
nea. 21. C. J. Hill, J. Aust. Entomol. Soc. 32, 283 (1993). species should consistently
should show
consistently this
showarea.
(i)inhigher geneticIn genetic
(i) higher Descriptive
Descriptive
stability/expansion, hypothesis testingtesting
diversity within populations
and among populations in refugia phylogeography stability/expansion, hypothesis
ecies of 22. D. R. Nash, T. D. Als, R. Maile, G. R. Jones, J. J. Boomsma,
new priorities for conservation in Brazil and establishes a validated approach to biodiversity Maximum (LGM, 21 kybp); (iii) absence of H. faber, divergent clades are also represented
diversity within and among in refugia phylogeography divergence times
divergence times (HABC)
(HABC)
Science 319, 88 (2008). relative to unstable areas, because of long-term per-
genetic
Museum patterns of isolation-by-distance in un- in the São
relative Paulo
to unstable region,andmatching
population predictions
areas, because of long-term per- of
1
icularly prediction in other understudied, species-rich regions. of Vertebrate Zoology, University of California,
23. P. J. DeVries, Am. Mus. Nov. 3025, 1 (1991). 2 sistence structure; (ii) genetic sig-
Diptera, Berkeley,
stable CA 94720–3160,
areas, given that USA. Biology Department,
colonization has been asistence
mid-sized andrefugium
population in structure;
this area. (ii)
Allgenetic
taxain show sig-
24. K. Fiedler, B. Hölldobler, P. Seufert, Experientia 52, 14 Queens College, City University of New York, Flushing, NY nature of population expansion unstable areas, Fig. 1. Proposed method of biodiversity prediction. Three stages are involved: biodiversity dis-
naturegenetic
of population
reflectingexpansion incolonization
unstable areas,

L
ays the (1996). too recent to3 permit restoration of equilibrium low diversity across the
multispecies southernmost Proposed
Fig. 1.tribution
from adjacent method
modeling of model-based
(top), biodiversityhypothesis
prediction. Three stages
formulation (middle),arehypothesis
involved:testing
biodiversity
and dis-
25. M. ate Quaternary N. E. climate fluctuations 60, helped refugia models have been dismissed because of 11367, USA. Departamento de Zoologia, Instituto de

L
nt’s hi- A.ate Quaternary
Travassos, Pierce,climate
Anim. fluctuations
Behav. 13 being described (8, 9). Our ultimate goal is to Biociências,
between migration
UNESP, Rioand genetic
Claro, drift (15);Brazil.
SP 3526-4100, and reflecting multispecies colonization
range of the forest, an area predicted to be less
refugial regions after the from
Last adjacent
Glacial Maximumtribution modeling
model validation(top),
(bottom).model-based hypothesis formulation (middle), hypothesis testing and
to shape present-day diversity in temper- conflicting evidence (2, 3) or circularity in iden- 4Departamento de Zoologia, Instituto de Biociências,
cue has (2000).
26. N. ate
helpedettoal.,shape
E. Pierce
present-day diversity
47, 733
in pinpoint regions for inventory work and habitat (iv) strong phylogeographic structure between
(2002).
refugialbyregions
stable after the LastFurthermore,
the palaeomodels. Glacial Maximum mito- model validation (bottom).
and boreal systems (1), providing a tifying putative refugia (4), but historical pro- Universidade de São Paulo, SP 055008-090, Brazil.
Annu. Rev. Entomol.
27. J. C.temperate C.and boreal systems (1),
14, pro- protection before we lose a substantial fraction refugia, reflecting assemblage-wide, long-term chondrial786 DNA (mtDNA) lineages found in this
ate and Downey, 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
general contextA.for Allyn, Bull. Mus.
understanding Entomol.
current pat- cesses must be invoked to explain regions of
viding a general context for understanding cur- of described and undocumented diversity. The *To
1 (1973). whom correspondence
population persistence should be addressed.
in isolated areas. E-mail: 786 region are shared with adjacent refugia (one
6 FEBRUARY in scale,
2009long-term
VOL 323 persistence
SCIENCE of populations in and E). Using Bayes factor (25), we also detect
www.sciencemag.org
terns ofthank
endemism. In
andthe tropics, forPleistocene high endemism (5, 6). Recent studies from sub- carnaval@berkeley.edu
rent
28. Wepatterns N.ofElfferich
endemism. P. J.In the tropics,
DeVries Pleis- approach differs from previous methods by di-
introducing Distribution models developed under current H. albomarginatus and H. semilineatus, two in isolated refugial areas, as opposed to post-LGM evidence for stability in both areas under the no-
us to ant-butterfly acoustics; G. W. Elmes, J. C. Wardlaw,
Berlin,
tocene refugia models have been dismissed be- rectly modeling historical processes, as opposed climatic conditions accurately predict distribu-
V. La Morgia, M. B. Bonsall, and referees for
H. faber). colonization of refugial regions. migration model [B(Z2 = 0, Z2 > 0) = 4.89], as
cause of conflicting
comments and advice; evidence (2, 3)for
and M. Charles ordesigning
circularity to observed biodiversity
www.sciencemag.org SCIENCE patterns
VOL 323(10), with the tions2009
6 FEBRUARY of each of the target species along the At- 785 Metrics of genetic diversity confirm the To test for assemblage-wide colonization well as under a postisolation migration model
nu. Rev. the acousticalputative
in identifying equipment. refugia (4), but historical aim of informing conservation. lantic rainforest domain [area-under-the-curve above patterns (Table 1). In H. albomarginatus of predicted unstable areas, we group mtDNA [B(Z2 = 0, Z2 > 0) = 4.84].
processes
Supporting must invoked to explain regions
OnlinebeMaterial We use molecular genetic data from multiple, (AUC) values (16) 0.968, 0.989, and 0.994; and H. semilineatus, genetic diversity (21) is an sequences from the southernmost refugial sites Relative to nuclear loci, mtDNA data are
9).
nández, of high endemism (5, 6). Recent studies from
www.sciencemag.org/cgi/content/full/323/5915/782/DC1 largely codistributed species to test whether spa- maximum Kappa (17) 0.81, 0.925, and 0.94 in H. order of magnitude larger in the central (Bahia) [population 1 (Fig. 3A)] and from localities in more variable and readily collected and often
Materials and Methods
subtropical biomes have usefully employed post tial modeling of species-specific Late Quaterna- albomarginatus, H. faber, and H. semilineatus, refugium relative to the less stable (southern) unstable areas south of the refugium [population provide key insights into biological response
SOM Text
4). hoc palaeoclimate
Figs. S1 and S2 models of species and habi- ry refugia sheds light on historical processes and respectively (fig. S2)]. Stability maps, depict- portion of the forest. Diversity of H. faber in 2 (Fig. 3A)] to contrast two alternative historical to environmental modification (1). Although
nsect
y, J. Rolff, tats S1 provide insights about processes shaping
Table to hence improves prediction of genetic endemism ing the intersection of distribution models for this southern area is higher than the other spe- models across the three codistributed species, single-locus inference can be imprecise in the
18. References and species diversity (5, 7). Building
genetic and diversity in tropical Brazil (11). We focus each taxon under current, 6 kybp, and 21 kybp cies because of the presence of two lineages that while allowing the taxon-specific demographic face of coalescent variance and the possibility of
Audio S1 to S4
004). on them, we first map the palaeodistribution of on three common species of tree frogs that are climates, predict for all species a large central co-occur in the adjacent refugia. In all species, parameters to vary. In H1, the long-term persis- selection (26), our method benefits from a mul-
, Proc. R. endemic
22 July 2008;species
accepted to
28 identify temporally stable
November 2008 widely distributed along the Brazilian Atlantic refugium throughout the Late Quaternary (“Ba- average net nucleotide differences across locali- tence model, two contemporary populations split titaxon approach, while explicitly accounting
10.1126/science.1163583
(refugial) and unstable (recently colonized) forest: Hypsiboas albomarginatus, H. semi- hia refugium”) (Fig. 2). A second, much smaller ties (22) reflects high geographic structure with- from an ancestral population prior to the LGM for the stochasticity of a single-locus coalescent
regions for species occurrence, which are then lineatus, and H. faber. Given their life history refugium is predicted in the northeasternmost in refugia (2.6 to 6.2% divergence). In contrast, (120,000 to 1.2 million years before present, or across taxa. Combining data sets from several
tropical with multispecies
validatedbiomes have usefullymolecular
employeddata.post Go-
hoc traits, amphibians are useful indicators of envi- portion of the forest (“Pernambuco refugium”). sites located outside (south of) the refugia are Mybp, Fig. 3A). In H2, the recent colonization codistributed groups into a single hierarchical
in ing beyond
approach,
provide
the traditional
the molecular
insights
species-by-species
palaeoclimate models of species and habitats to
analyses
about processes contrast
shaping the
genetic
ronmental changes through time (12). Whereas
H. albomarginatus and H. semilineatus occur in
In H. faber, a third, southeastern refugium of in-
termediate size is also predicted (“São Paulo ref-
genetically more similar to each other, although model, population 2 is modeled as being colo- Bayesian analysis allowed us to estimate con-
to a lesser extent in H. faber (0.1 to 1.6%). Sig- nized from refugial population 1 subsequent to gruence across species, while borrowing strength

ot fit of assemblage-level data to the spatially

and species diversity (5, 7). Building on them, we
plicit
first mapdemographic scenarios suggested
the palaeodistribution
ex-
by the
of endemic
low and mid altitudes and are mostly restricted
to the evergreen or semideciduous components
ugium”). This is not surprising, given that this
species occupies a broader environmental niche.
natures of population expansion (23) are found the LGM (0 to 20 kybp; Fig. 3A). The results from the full comparative phylogeographic sam-
in the unstable area for H. albomarginatus and indicate that all three species colonized the ple (24). This can translate into higher analytical
climate-based
species to identify models. temporally stable (refugial) of the Atlantic Forest in eastern Brazil, H. faber In contrast to the central and northern regions, H. faber, as well as in the Bahia refugium area southern (unstable) areas after the LGM (Z2 = 3, power and be more informative than qualitative
andWe apply this
unstable approach
(recently to one of regions
colonized) the world’s
for has a broader altitudinal range and also inhabits populations south of the Bahia or São Paulo for H. faber and H. semilineatus. The lack of the number of species evolved under H2), even comparisons of species-specific analyses. By
most
speciesspecies-rich, yet notoriously
occurrence, which endangered
are then validated with mixed and deciduous areas, occupying interior refugia appear much less stable, despite the signature of population expansion in the south- when allowing for postisolation migration (Fig. capturing the historical signal that emerges from
and understudied
multispecies molecular ecosystems:
data. GoingthebeyondBrazilian
the and coastal sites in the Atlantic Forest south to more extensive (preclearing) range of the for- ernmost localities of H. semilineatus may reflect 3, B and C). When Bayes factor is used (25), larger, combined multispecies molecular data
hreat, Atlantic
traditionalrainforest. Originally
species-by-species extending
approach, for
the mo- Paraguay and Argentina (figs. S1 and S2) (13). est in southern and southeastern Brazil. We hy- low statistical power because of the exception- there is strong support for recent colonization in sets, HABC will offer the possibility of looking
sparse 1,300,000 km2 along thetheBrazilian coast and The comparative phylogeographic approach is pothesize that these areas received a significant ally low levels of diversity observed in this spe- all three species (Z2 = 3) under the no-migration at patterns of historical community assembly in
lecular analyses contrast fit of assemblage-
ators, reaching cies. As predicted, isolation by distance is not model [B(Z2 = 3, Z2 < 3) = 35.16], and moderate codistributed nonmodel organisms for which
level datainto to Paraguay and Argentina,
the spatially this biome
explicit demographic a powerful test of assemblage-scale responses influx of migrants from adjacent, large refugial
species has been reduced to by
lessthe
than 8% of its range (8). to former environmental change and thereby populations after the LGM. These palaeomodel observed in unstable regions, but is detected support under a postisolation migration model barcode-type DNA sequence information (e.g.,
scenarios suggested climate-based models.
Today’s fragments
We apply harbor one
this approach of the
to one of largest per-
the world’s provides a means for critical assessment of the results are congruent with the fossil pollen re- within refugial areas for H. albomarginatus and [B(Z2 = 3, Z2 < 3) = 5.70]. mtDNA data) can be feasibly collected.
pot. centages of endemic species in the world, with scenarios produced by modeling of species’ dis- cord, which documents a replacement of forests H. faber. Using the same framework to test for long- Collectively, the results identify the central
most species-rich, yet notoriously endangered and
region,
many
understudied and even genera
species ecosystems: the of vertebrates
Brazilian still
Atlantic tributions under palaeoclimates (7). by grasslands in the southern Atlantic forest dur- The hierarchical approximate Bayesian com- term persistence of refugial populations, we region as a hotspot within the Atlantic rainforest
his sets
The palaeomodeling method intersects ing the LGM (14, 18) and suggests the occur- putation (HABC) method (24) allows us to use compare mtDNA sequences between the pre- hotspot and a refuge for biodiversity during
ty 1
Museum of Vertebrate Zoology, University of California, predicted species’ distributions under current rence of small forest refugia in the southernmost data from all three species at once to test for dicted Pernambuco refugium [population 1 (Fig. climatic extremes of the Late Pleistocene.
Berkeley, CA 94720–3160, USA. 2Biology Department, conditions and climatic extremes of the Late range of the putative Bahia refugium (19). The assemblage-wide responses to Late Quaternary 3A)] and adjacent (northern) populations from This is not to say that southern areas entirely
Queens College, City University of New York, Flushing, NY Quaternary (6000 years before present, or 6 results also agree generally with forest models climate change. These analyses support both the Bahia refugium [population 2 (Fig. 3A)] to lacked forested habitats in the late Pleistocene:
11367, USA. 3Departamento de Zoologia, Instituto de
ause of
Biociências, UNESP, Rio Claro, SP 3526-4100, Brazil. kybp, and 21 kybp) to predict areas of stability published previously (14), although the central model-driven hypotheses of (i) simultaneous, contrast alternative historical models H1 and H2. The existence of species and genera endemic
n iden- 4
Departamento de Zoologia, Instituto de Biociências, (regions in which species are predicted to oc- refugium extends farther south in the frog-based multispecies colonization of unstable areas from In this case, the HABC results infer long-term to the southern forests (27), as well as some
al pro- Universidade de São Paulo, SP 055008-090, Brazil. cupy irrespective of time period) and unstable models. Such differences are expected because adjacent refugial populations since the LGM, persistence of populations in isolated refugia for palaeoecological and genetic evidence (28),
ions of *To whom correspondence should be addressed. E-mail: areas (7, 14). Because the stability maps raise the forest and its associated species may differ as opposed to long-term persistence of popu- all three species (Z2 = 0, i.e., Z1 = 3), even when offer evidence to the contrary. Rather, the
m sub- carnaval@berkeley.edu specific hypotheses about regional differences slightly in their climatic tolerances and realized lations in unstable areas, and (ii) assemblage- allowing for postisolation migration (Fig. 3, D phylogeographically validated palaeomodels

36 37
6 FEBRUARY 2009 785
 presence of two lineages that co-occur inAthe ad- B sites located
6.2% divergence). In contrast, C
population expansion (23) are found in the
refugial (stable)
jacent refugia.
jacent Inversus
refugia. unstable
all species,
In areasaverage
average
all species, net nucle- outside
net nucle- outside(south
(south of)
of) the refugiaare
the refugia aregenetically unstable
geneticallyunstable area
area for H. for H. albomarginatus
albomarginatus and H. faber,
and H. faber, Mybp, Fig. 3A). In H2, the recent colonization coalescent variance and the possibility of selec- southern regions. This reassures us that the pro-
in thedifferences
otide Brazilian Atlantic
across across
otide differences rainforest.
localities (22) (22)
localities reflects more
reflects moresimilar
similartotoeach
each other, althoughto to
other, although a lesser as well
a lesseras well as in
as in the the refugium
Bahia Bahia refugium area
area for H. for H. faber
faber model, population 2 is modeled as being colo- tion (26), our method benefits from a multitaxon cesses uncovered by the amphibian data may be
(Top) Species-specific
high geographic structure
high geographic stability
within
structure maps;
refugia
within refugia to to extent
(2.6 (2.6 faber (0.1
ininH.H.faber
extent to 1.6%).
(0.1 to 1.6%).Signatures
Signatures of ofand and H. semilineatus.
H. semilineatus. The lackTheof lack of signature
signature of of nized from refugial population 1 subsequent to approach, while explicitly accounting for the generalized to and help to explain patterns of
modeled refugia in black. (A) H. Pernambuco
albomarginatus, (B) H. semilineatus, refugium
Fig. 2. diversity
Fig.H.2.faber.
Genetic Genetic diversity in putative
in putative A B C Fig. 3. HABC analyses.
(C) Note the absence of large
refugial (stable) versus unstable areas A B C
refugialregions
stable (stable)
in theinversus unstable
the southern
Brazilian areas
portion
Atlantic rainforest.
Bahia refugium (A) Simulated models
in the
of the forest
Brazilian
(Top)(south Atlantic
of the Bahia
Species-specific rainforest.andmaps;
stability * * H1 (long-term persist-
(Top)Paulo
São Species-specific
refugia)
modeled stability
relative
refugia tomaps;
in black. the(A) H. Pernambuco ence) and H2 (recent
modeled
central and refugia
albomarginatus,
northern in areas.
black.
(B) H. (A) H.
semilineatus,
Asterisks refugium Pernambuco colonization). In both
(C) H. faber. Sã o Paulo refugium cases, each species was
albomarginatus,
denote refugia (B) Note
inferred the absencethe
H. semilineatus,
beyond of large refugium
stable regions in the southern portion Bahia refugium
(C) H. faber.
current Note
ranges of the
the absence
target of large
species. modeled as two con-
of theinforest (south of the Bahia and * 5.4% * Bahia refugium temporary populations
stable regions
Symbols indicate the southern
localities sampledportion
São Paulo refugia) relativeforto the *
of the forest
molecularcentral (south
analysis.
andScaleof the
northern Bahia
bar, areas.
400 km. and
Asterisks * with mutation-drift pa-
São PauloThe refugia) relative Sã o Paulo refugium rameters q1 and q2 that
(Bottom) denote50% inferredtobeyond
majority-rule
refugia the the
con-
central and
sensus Bayesian northern areas.
phylogenetic
current ranges Asterisks
of the target trees,species. 5.4%
split from an ancestral
7% Sã o Paulo refugium
denote with
rooted refugia
Symbols inferred
indicatefrom
sequences beyond
localities the for
thesampled
oth- 7.8% population at a time t in
current
er two rangesmolecular
congenericof analysis.
thespecies
target Scale bar, 400 km.
species.
studied 5.4% the past. Ancestral pop-
Symbols (Bottom)localities
The 50%sampled majority-rule
for con- ulation sizes are repre-
(root notindicate
shown). Thick internodes
sensus Bayesian phylogenetic trees,
de- 5.3 –
molecular
note clades analysis.
withwith Scale bar,
posterior 400 km.
probability 7%
5.8% 7.8% 4% sented by (qt)1 and (qt)2;
rooted sequences from the oth-
(Bottom)
greater The
than 50%
er 90%.
two majority-rule
Percentages
congeneric con-
indicate
species studied
ybp, years before pres-
sensus
Tamura-NeiBayesian not phylogenetic
corrected
(root distances
shown). trees, de-
Thick between
internodes 7% ent. (B to E) Hyperposte-
5.3 – 7.8%
rooted(20).
clades with
notesequences
clades withfrom the probability
posterior oth- 5.8% 4% rior (bars) and hyperprior
er two congeneric
greater than 90%. species studied
Percentages indicate 5.6% (dashed) densities of Z2
Tamura-Nei
(root not shown). corrected
Thick distancesde-
internodes between (number of species evolved
5.3 –
note clades clades
with(20).
posterior probability 4% under H2) given data from
5.6% 5.8%
greater than 90%. Percentages indicate three codistributed frog
Tamura-Nei corrected distances between species. (B) and (C) Mod-
clades (20). els of refugial sites (pop-
5.6% ulation 1) and unstable,
southern areas (popula-
tion 2). (D) and (E) Models
of Pernambuco refugium
(population 1) and Bahia
refugium (population 2). (B) and (D) Postisolation migration not included in model; (C) and (E) postisolation migration included in model.

At a broader level, the congruence between An Online Reference, version 5.2, 15 July (2000).
788 model-based demographic hypotheses
6 FEBRUARY
and 2008 (American
2009 VOL 323Museum
SCIENCE History, 32. We thank U. Caramaschi and H. Zaher for
of Naturalwww.sciencemag.org
New York, 2008); electronic database providing access to collections MNRJ and
Table 1. Population genetic summary metrics used in model validation. n, q, and average D values of the former were obtained not only from the total
a joint, multispecies analyses of mtDNA diversity
Table 1. Population genetic summary metrics used in model validation. n, q, and average Da values of the former were obtained not only from the total accessible at http://research.amnh.org/ MZUSP; O. Peixoto, M. Gomes, A. Muri, R.
Sample size; S, number
Sample of segregating
size; S, number sites. sites.
of segregating The diversity parameter
The diversity parameterq qand
andmean
mean
numberofofsamples,
number samples,but but
also also
from from all possible
all possible combinations
combinations of spatiallyof spatially shows that palaeoclimatic niche models and herpetology/amphibia/index.php. Kautskyi, S. Lima, E. Santos, J. S. Filho, J.
Da across Dlocalities are given per base pair (bp). Hs test (23) is used to detect contiguouslocalities
localities distributed
withinwithin the geographic
extensionextension of the unstable assemblage-scale molecular genetic analyses V. Filho, G. Barros, J. Queiroz, R. Araújo, L.
a across localities are given per base pair (bp). Hs test (23) is used to detect contiguous distributed the geographic of the unstable 14. A. C. Carnaval, C. Moritz, J. Biogeogr. 35,
populationpopulation
expansion. BA, Bahia;
expansion. SP, São
BA, Bahia; SP, Paulo refugia.
São Paulo Because
refugia. Becausepredicted
predicted area.Parentheses
area. Parentheses encompass
encompass minimum
minimum and maximum
and maximum values
values from from subsamples.
subsamples. can be used to forecast spatial patterns of 1187 (2008). Japp, H. Japp, J. Giovanelli, J. Alexandrino,
refugia were oftenwere
refugia larger
oftenthan predicted
larger unstable
than predicted (recently
unstable colonized)
(recently colonized)areas,
areas,n,
n, S,
S, valuesininbold
PPvalues bold highlight
highlight statistical
statistical significance
significance at 0.05 at 0.05 probability
probability level. level. diversity in poorly explored, highly threatened 15. M. Slatkin, Evolution 47, 264 (1993). L. Toledo, O. Araújo, G. Egito, J. Zina, D.
ecosystems. In a world of ever-accelerating 16. J. A. Hanley, B. J. McNeil, Radiology 143, 29 Loebmann, D. Pavan, R. Amaro, V. Verdade,
Table 1. Population genetic summary metrics usednin nmodel validation.
SS n, qq
q, and average Mean
Da values ofDthe
Mean Dformer Hs Hs Mantel’s
were obtained corr.
onlycoef.
notMantel’s
from the coef.
corr. total F. Curcio, M. Dixo, and J. Cassimiro for field
Species Species Area Area
a
a (1982).
(min.;
Sample size; S, number of segregating sites. The diversity
(min.; max.) (min.;
parameter
max.) q(min.; max.)
and mean
max.) (min.;
(min.;max.)
number samples,(min.;
ofmax.) but max.) from(Pall
alsomax.)
(min.; value)
possible (P value) (P value)
(P value)combinations of spatially environmental changes, this approach can help 17. J. Cohen, Ed. Psych. Meas. 20, 37 (1960). work assistance; W. Monahan and R. Hijmans
D across H.
localities are given per Stable
albomarginatus base pair
(BA) (bp). Hs test 36
(23) is used to 207
detect contiguous
0.076 localities distributed
0.062 within–20.546the geographic extension
0.499 of the unstable to guide research and conservation in other 18. H. Behling, R. R. B. Negrelle, Quat. Res. 56, for discussions about the modeling work; L.
H.a albomarginatus Stable (BA) 36 207155) 0.076 0.062 –20.546 (0.001) 0.499 global hotspots or similarly complex tropical Smith and D. Turong for DNA-sequencing
(970 bp)
population expansion. BA, Bahia; SP, São Paulo refugia.(13; 23) (81;
Because predicted area. Parentheses
(0.034; 0.072) encompass minimum(0.141)
(0.020; 0.082) and maximum values from subsamples. 383 (2001).
(970 bp) Unstable (13; 23) (81; 155) (0.034;in0.072) (0.020; 0.082) –11.498(0.141) (0.001) ecosystems. 19. H. Behling, H. W. Arz, J. Pätzold, G. Wefer, assistance; R. Pereira, R. Damasceno, S.
refugia were often larger than predicted unstable (recently27colonized) areas,22n, S, 0.003
P values 0.001
bold highlight statistical significance at 0.05–0.140
probability level.
Unstable(south of BA) 27 22 0.003 0.001 (0.004)–11.498 (0.580) –0.140 Palaeogeogr. Palaeoclimatol. Palaeoecol. Rovito, J. Kolbe, S. Singhal, R. Puschendorf,
H. semilineatus (south of BA)
Stable (BA) n 28 S71 0.031
q 0.036
Mean Da –17.778 (0.004)
Hs 0.054 (0.580)
Mantel’s corr. coef. References and Notes 179, 227 (2002). and A. Pounds for discussions about earlier
Species (718 bp) Area (6; 13) (14; 58) (0.009; 0.034) 1. G. Hewitt, Nature 405, 907 (2000). [CrossRef] 20. K. Tamura, M. Nei, Mol. Biol. Evol. 9, 678 versions of the manuscript. Funding was
H. semilineatus Stable (BA) (min.;28 max.) (min.;71max.) 0.031
(min.; max.) (0.007; 0.041)
max.) (0.029)
0.036
(min.; (P value) (0.460) (P0.054
–17.778 value)
(718 bp) Unstable (6; 13)15 (14; 958) 0.0030.034)
(0.009; 0.004 0.041) 0.114(0.029)
(0.007; 0.436 (0.460) 2. F. E. Mayle, D. J. Beerling, W. D. Gosling, M. (1993). provided by the NSF (awards DBI 0512013
H. albomarginatus Stable (BA)
(south of BA) 36 207 0.076 0.062 (0.357)–20.546 (0.248) 0.499 B. Bush, Philos. Trans. R. Soc. London B Biol. 21. F. Tajima, Genetics 143, 1457 (1996). to A.C.C., DEB 0743648 to M.J.H., DEB
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(970 bp)H. faber Stable (BA) (13; 23)28 (81; 94155) 0.0180.072)
(0.034; 0.026 0.082)–38.111(0.141)
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(771 bp) Unstable 27(13; 23) (42;
22 80) (0.012; 0.022)
0.003 (0.001; 0.044)
0.001 (0.003) 3. E. P. Lessa, J. A. Cook, J. L. Patton, Proc.
and Conselho Nacional de Desenvolvimento
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(BA) (SP) 28 15 9448 0.018
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(771 bp) (13; 23) (42; 80) (0.012; 0.022) (0.001; 0.044) (0.115)(0.003) (0.221) (0.0003) 4. B. W. Nelson, C. A. C. Ferreira, M. F. da 24. M. J. Hickerson, C. P. Meyer, BMC Evol. Biol.
H. semilineatus Stable (BA) 28 71 0.031 0.036 0.054 8, 322 (2008). and M.T.R.). Sequences are deposited in
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–17.778
Stable Unstable
(SP) 15 18 4840 0.023
0.015 0.0160.028 –13.255–5.981 0.0001 0.305
(718 bp) (south of SP) (6; 13) (14; 58) (0.009; 0.034) (0.007; 0.041)(0.014)(0.029) (0.456) (0.460)
(0.115) (0.221) (1990). 25. R. E. Kass, A. E. Raftery, J. Am. Stat. Assoc. GenBank (FJ502639-FJ502822). A.C.C. and
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Unstable 18 40 0.015 0.016 0.0001 and M.T.R. collected the data; A.C.C., C.M.
26. J. W. O. Ballard, M. Kreitman, Genetics 138,
–13.255
(south of BA)
(south of SP)
(0.357)
(0.014)
(0.248)
(0.456) Proc. Natl. Acad. Sci. U.S.A. 103, 632 (2006).
H. faber Stable (BA) 28
www.sciencemag.org 94
SCIENCE 0.018 6 FEBRUARY 0.026
VOL 323 2009 –38.111 0.803
787 6. W. Jetz, C. Rahbek, R. K. Colwell, Ecol. Lett. 757 (1994). and M.J.H. analyzed the data; A.C.C. wrote
7, 1180 (2004). 27. C. F. B. Haddad, L. F. Toledo, C. P. A. Prado, the paper. All authors discussed the results
(771 bp) (13; 23) (42; 80) (0.012; 0.022) (0.001; 0.044) (0.003) (0.0003) and commented on earlier versions of
7. A. Hugall, C. Moritz, A. Moussalli, J. Stanisic, Anfibios da Mata Atlântica (Atlantic Forest
presented here show that the (SP)
Stable central region 15 much more distantly
www.sciencemag.org
48 related groups
SCIENCE VOL 323of Atlantic
0.023
6 FEBRUARY estation
0.028 in this region
2009
–5.981relative to the more ex- 787
0.305
Proc. Natl. Acad. Sci. U.S.A. 99, 6112 (2002). Amphibians) (Editora Neotropica, São Paulo, the manuscript.
had much higher stability relative to the south. forest endemics. tensive forests in São Paulo and southern Brazil
(0.115) (0.221) 8. L. P. C. Morellato, C. F. B. Haddad, Brazil, 2008).
28. M.-P. Ledru et al., Divers. Distrib. 13, 761 Supporting Online Material
Forest lizards (14, 29) andUnstable
birds (30) also show 18 Because collection 40 efforts, molecular
0.015 studies, (9, 0.016
31). Not only 0.0001
could much unique
–13.255 diversity Biotropica 32, 786 (2000).
www.sciencemag.org/cgi/content/
(south ofofSP)
high diversity in the central portion the biome and conservation priorities have been heavily be lost, but ongoing (0.014) (0.456)could
habitat destruction 9. M. T. Rodrigues, Conserv. Biol. 19, 659 (2007).
full/323/5915/785/DC1
(2005). 29. K. C. M. Pellegrino et al., Biol. J. Linn. Soc.
relative to southern areas, and provide evidence biased toward southern and southeastern Brazil quickly erase the signature of the historical Materials and Methods
10. C. Kremen et al., Science 320, 222 (2008). London 85, 13 (2005). Figs. S1 to S6
for population expansion in southern regions. (8, 9, 31), we predict that genetic diversity and processes that led to it, preventing a full under- 11. Materials and methods are available as 30. G. S. Cabanne, F. M. d’Horta, E. H. R. Sari, Tables S1 and S2
www.sciencemag.org
This reassures us that the processes uncovered SCIENCE
narrow endemism VOL corridor
in the central 323 6ofFEBRUARY
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2009 supporting material on Science Online. F. R. Santos, C. Y. Miyaki, Mol. Phylogenet. References
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and help to explain patterns of diversity in other, This is serious, given the higher rate of defor- conservation measures. 13. D. R. Frost, Amphibian Species of the World: 31. J. M. C. da Silva, M. Tabarelli, Nature 404, 72 10.1126/science.1166955

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