Evo Edu Outreach (2009) 2:248–256

DOI 10.1007/s12052-009-0133-4

ORIGINAL SCIENTIFIC ARTICLE

Downsized Dinosaurs: The Evolutionary Transition

to Modern Birds
Luis M. Chiappe

Published online: 16 April 2009

# Springer Science + Business Media, LLC 2009

Abstract Living birds are the most diverse land vertebrates chronological information about milestones within a tran-
and the heirs of a rich chapter in the evolution of life. The sition, they help us visualize the sequence of physical
origin of modern birds from animals similar to Tyranno- transformations involved in it, and they document a series
saurus rex is among the most remarkable examples of an of intermediate characteristics that are no longer present (or
evolutionary transition. A wealth of recently discovered that are highly modified) in extant organisms. Fossils also
fossils has finally settled the century-old controversy about document that the origin of any major group is accompa-
the origin of birds and it has made the evolutionary saga nied by a wide range of evolutionary experimentation in
toward modern birds one of the best documented transitions which closely related lineages—whether contemporaneous
in the history of life. This paper reviews the evidence in or not—approach to a greater or lesser degree the
support of the origin of birds from meat-eating dinosaurs, characteristic trademarks of the new group. A wealth of
and it highlights the array of fossils that connect these intermediate fossils has made the evolutionary saga toward
fearsome animals with those that fly all around us. modern birds one of the best documented transitions in the
history of life (Fig. 1).
Keywords Dinosaurs . Birds . Origin . Evolution . Mesozoic Birds have an ancient and enormously rich history. The
common ancestor of all living groups of birds can be traced
to at least the Late Cretaceous period, more than 75 million
years ago, and the earliest records of fossils widely
With nearly 10,000 living species, birds are the most accepted as birds—those of the famed Archaeopteryx from
diverse land vertebrates and are the product of a long and southern Germany—date back twice as far. Deciphering the
fascinating chapter in the evolution of life. The origin of origin of birds, namely, identifying the closest relatives to
modern birds is undoubtedly one of the most dramatic the most recent common ancestor of Archaeopteryx and
examples of an evolutionary transition—one connecting modern birds, has been a matter of scientific debate and
animals akin to the fearsome Tyrannosaurus rex with the scrutiny throughout the history of evolutionary biology
feathered marvels we now see all around us—a transfor- (Chiappe 2007; Witmer 1991; Chatterjee 1997; Shipman
mation documented by a wealth of intermediate fossils that 1998; Feduccia 1999). As early as the eighteenth century,
date back to the Mesozoic Era (Chiappe 2007), the geologic birds were generally placed immediately ahead of flying
period that spanned between 245 and 65 million years ago. fishes in the “chains of being” postulated by the naturalists
The importance of the fossil record in providing evidence of that time. With the nineteenth century's advent of
of intermediate stages in an evolutionary transition has long evolutionary thinking, especially after Darwin's theory of
been recognized (Sues and Anderson 2007). Fossils provide evolution by natural selection, more explicit hypotheses
of relationships were formulated. Post-Darwinian times
L. M. Chiappe (*) witnessed a diversity of hypotheses in which birds were
The Dinosaur Institute, considered to be most closely related to a variety of extinct
Natural History Museum of Los Angeles County,
and extant lineages of reptiles. These hypotheses related
900 Exposition Boulevard,
Los Angeles, CA 90007, USA birds to groups of animals such as turtles, crocodiles, and
e-mail: chiappe@nhm.org their relatives, various primitive Triassic fossils (245 to 208
Evo Edu Outreach (2009) 2:248–256 249

Fig. 1 The skeletons of the nonavian maniraptoran Velociraptor, the of bird-like nonavian maniraptorans and primitive (“dinosaur”-like)
Jurassic bird Archaeopteryx, the Early Cretaceous short-tailed bird birds have been unearthed from Mesozoic rocks worldwide—these
Sapeornis and enantiornithine Longipteryx, the Late Cretaceous discoveries have consolidated the notion that birds evolved from
Ichthyornis, and the living Gallus (chicken). In recent years, a wealth maniraptoran theropod dinosaurs. Drawings not to scale

million years ago), pterodactyls, and their kin, and the the fossils of large and small theropods. Since the 1960s, a
plant-eating ornithischians and the meat-eating theropod greater understanding of small predatory dinosaurs of the
dinosaurs. For decades, the origin of birds remained Cretaceous age, such as the dromaeosaurid Deinonychus
obscure and controversial—the fossil record was too (Ostrom 1969, 1976), has led to the idea that birds had
fragmentary to provide a clear picture. Today, however, originated from within a group of bird-like theropods called
most of the other hypothetical relationships have been maniraptorans (Gauthier 1986). Today, the skeletons of
abandoned and the theropod hypothesis has received nearly such maniraptoran theropods such as the sickle-clawed
universal acceptance (Shipman 1998; Rowe et al. 1998; dromaeosaurids (Deinonychus, Velociraptor, and their kin;
Sereno 1999; Chiappe and Witmer 2002). In fact, because Fig. 1), the lightly built troodontids (Troodon, Mei, and
birds are overwhelmingly interpreted as the descendants of their kin), the parrot-headed oviraptorids (Oviraptor and
a group of carnivorous dinosaurs, most scientists argue that relatives), and the short-armed alvarezsaurids (Mononykus
they be considered living dinosaurs. Therefore, birds are and its kin) are recognized as sharing a great deal of similarity
today interpreted as avian dinosaurs—Velociraptor, Tyran- with birds (Chiappe and Witmer 2002; Weishampel et al.
nosaurus, Brachiosaurus, and all other traditional “dino- 2004). Not only have birds retained the bipedalism,
saurs” that coexisted with a variety of primitive Mesozoic hollowed bones, and the three fully developed toes of their
birds are referred to as nonavian dinosaurs. theropod predecessors, but these animals also share a series
of air spaces connected to the ear region, unique structures
of their vertebral column and rib cage, elongate forelimbs
Birds as Living Dinosaurs with wrist bones allowing swivel-like movements of the
hand and similar structures in the pelvis and hindlimbs, as
The idea that the ancestry of birds can be traced back to a well as many other characteristics distributed over the entire
group of carnivorous dinosaurs called theropods is not new skeleton (Rowe et al. 1998; Sereno 1999; Chiappe and
(Chiappe 2007). Nearly 150 years ago, soon after the Witmer 2002; Weishampel et al. 2004; Novas and Puerta
publication of Darwin's Origin of Species, German embry- 1997; Holtz 1998). Indeed, many skeletal features previously
ologist C. Gegenbaur used similarities in the structure of thought to be exclusively avian—such as wishbones, laterally
the ankle to place the small, 150-million-year-old theropod facing wingpits, and large breastbones—have now been
Compsognathus in an intermediate position between birds discovered among nonavian maniraptorans (Padian and
and other reptiles. At about the same time, American Chiappe 1998).
paleontologist E.D. Cope compared the ankle of the In recent years, a wealth of evidence taken from
Jurassic theropod Megalosaurus to that of an ostrich, and comparisons between the skeletons of these dinosaurs and
on the basis of this and other skeletal similarities, argued those of birds has been supplemented by diverse lines of
for a close relationship of theropods and birds. Despite evidence in support of the same evolutionary relationship.
these initial considerations, it was British anatomist T.H. Paleontologists have determined that the shape and struc-
Huxley (Huxley 1868) who first popularized the idea that ture of nonavian maniraptoran eggs were similar to those of
birds had originated within theropod dinosaurs. In the living birds (Mikhailov 1992; Zelenitsky 2006; Varricchio
ensuing years, a myriad of other skeletal features support- and Jackson 2004; Grellet-Tinner et al. 2006). Some of
ing the dinosaurian origin of birds has been discovered in these features involve the presence of more than one
250 Evo Edu Outreach (2009) 2:248–256

distinct crystalline layer in the eggshell (distinguished by a probably took several days for a nonavian maniraptoran
differential disposition of eggshell crystals), reduction in female to lay its egg clutch (Varricchio and Jackson 2004;
the number of airholes perforating the eggshell, a relative Grellet-Tinner et al. 2006), a condition shared with birds.
increase in the volume of the egg (with respect to the adult's Other extraordinary discoveries have shed light on the
size), and the development of asymmetrical eggs in which nesting behavior of these dinosaurs. Skeletons of oviraptor-
one pole is narrower than the other (Fig. 2). Snapshots of ids (Norell et al. 1995; Clark et al. 1999) and troodontids
ancient behavior revealed by a handful of exceptional (Varricchio and Jackson 2004) have been discovered on top
fossils have also provided support to the hypothesis that of their clutches of eggs. The fossils show evidence that
birds evolved from maniraptoran dinosaurs. The discovery these animals adopted a posture similar to that of brooding
of a “gravid” oviraptorid female containing a pair of shelled birds. In oviraptorids, the adult tucked its legs inside an
eggs inside her pelvic canal (Sato et al. 2005) has open space at the center of the egg-clutch and hugged the
confirmed previous interpretations based on the spatial periphery of the clutch with its long forelimbs; in the more
arrangement of eggs within clutches of nonavian manir- lightly built troodontids, the adult sat on top of the
aptorans. These clutches—particularly well known among vertically buried eggs. These discoveries suggest that,
oviraptorids—show that the eggs were arranged in pairs, as regardless of its specific role (protection, incubation),
opposed to typical reptilian clutches (turtles, crocodiles, and typical avian nesting behaviors (adults sitting on top of
other dinosaurs), in which the eggs lack any spatial their nests) were widespread among nonavian maniraptor-
arrangement (Grellet-Tinner et al. 2006) (Fig. 2). This ans. Additional evidence further documents behavioral
evidence indicates that, as with birds, nonavian maniraptor- similarities with birds. Fossils of troodontids with their
ans laid their eggs sequentially, at discrete time intervals. It skeleton arranged such that the hindlimbs are flexed

Fig. 2 Characteristics of the

eggs and clutches of several
nonavian maniraptorans support
the inclusion of birds within
these theropod dinosaurs. For
example, the presence of at least
two distinct crystalline layers in
the eggshell and the existence of
an asymmetric egg (less asym-
metric among oviraptorids) can
be traced back to as far as the
maniraptoran divergence. The
distribution of the eggs within a
clutch in oviraptorids indicates
that these dinosaurs laid their
eggs sequentially (other evi-
dence also indicates that, as in
the case of birds, they also
brooded their clutch)
Evo Edu Outreach (2009) 2:248–256 251

beneath the belly, the neck is turned backwards, and the birds more than the realization that true feathers—the
head is tucked between the wing and the body have quintessential avian feature—may have covered the bodies
documented that at least some of the maniraptoran of a variety of nonavian dinosaurs (Norell and Xu 2005).
precursors of birds had already evolved stereotypical The enormous significance of these fossils notwithstanding,
resting poses familiar to many birds (Xu and Norell 2004). the documented existence of feathers in nonavian dinosaurs
More specific fields of research have made their own has, thus far, been limited to a dozen or so species, all of
empirical contributions in support of the dinosaurian legacy them circumscribed to the Cretaceous deposits of East Asia.
of birds. Studies of dinosaurian growth rates, based on Some of these dinosaurs exhibit feathers that are filament-
details preserved in the fossilized tissue of their bones, have like, with a minimal degree of branching, but a number of
documented that these animals, once believed to be slow- others display pennaceous feathers with distinct shafts and
growing, actually grew at speeds comparable to many vanes. In certain nonavian maniraptorans, long pennaceous
living birds (Erickson et al. 2001), and special bone tissues, feathers attach to the distal part of the tail, either in a fan-
such as the medullary bone characteristic of ovulating birds, like fashion or giving the tail the frond-like appearance
have been documented in a female T. rex (Schweitzer et al. common to primitive birds such as Archaeopteryx (Fig. 1a).
2005). Evidence in support of the evolutionary transition Long pennaceous feathers also attach to the tip of the
between nonavian dinosaurs and birds has also been forelimbs of some of these maniraptorans, and in the case
uncovered from disciplines as far-off from classic paleon- of the peculiar dromaeosaurid Microraptor (Norell and Xu
tology as genetics. Studies correlating the sizes of bone 2005), they form a wing of essentially modern design.
cells and genomes (the entire genetic material of an Despite the evidence of plumage being restricted to a
organism) have revealed that the mighty T. rex and its handful of nonavian dinosaurs, the fact that these fossils
fearsome kin had the small genomes typical of modern span a large portion of the family tree of theropods and
birds (Organ et al. 2007), and putative protein sequences display a great diversity of sizes, appearances, and life-
from soft tissues of this dinosaur have also highlighted its styles, hints at a much larger and yet undocumented
evolutionary closeness to birds (Organ et al. 2008, although diversity (Fig. 3)—even the colossal T. rex may have been
for a different interpretation of this evidence, see Dalton covered with a cloak of feathers at some early stage of its
2008). life. It is an amazing experience to gaze at the entirely
Yet, despite the multiplicity of this extensive body of modern feathers of animals, whereas their skeletal charac-
evidence, nothing has cemented the dinosaurian pedigree of teristics are so unquestionable dinosaurian.

Fig. 3 Genealogical relation-

ships of feathered nonavian
theropods. Current evidence
supports the hypothesis that fil-
amentous and vaned feathers
evolved with the divergence of
coelurosaurs and maniraptorans,
respectively
252 Evo Edu Outreach (2009) 2:248–256

An important corollary of these discoveries is that in support of the idea that birds evolved from maniraptoran
feathers did not evolve in the context of flight. With the theropods. Current evidence highlights the fact that many
sole exception of Microraptor, it is certain that none of features previously thought to be exclusively avian—from
these feathered dinosaurs were able to take to the air. The feathers to a wishbone—have now been discovered in the
forelimbs and their feathers are both much shorter than in immediate dinosaur predecessor of birds. The origin of birds
flying birds and their bodies are larger. The evolutionary was also preceded by a substantial reduction in body size—
transition toward birds and the origin of their flight the most primitive members of groups such as troodontids
involved a dramatic reduction in body size. These feathered and dromaeosaurids are smaller than one meter long (Turner
dinosaurs indicate that, at their onset, feathers must have et al. 2007). This notable reduction in the size of the
had a different function, perhaps insulating the bodies of forebears of birds was an important prerequisite of flight;
animals that had metabolically diverged from their cold- even this most characteristic avian attribute is likely to have
blooded, reptilian ancestors. My research has suggested that been inherited by birds from their dinosaurian predecessors.
vaned feathers may have originated in the context of thrust, The comparative studies that have been the building
evolving in running nonavian theropods that by flapping blocks of these important evolutionary conclusions have
their feathered arms were able to increase their running been greatly assisted by many newly discovered Mesozoic-
speed (Burgers and Chiappe 1999). In the end, however, we aged birds (Chiappe 2007), which by possessing many
simply do not have an answer for what was the original skeletal features that are only slightly modified from the
function of feathers; nonetheless, we have been able to ancestral maniraptoran condition, fill a critical gap in the
eliminate flight as an option. evolutionary transition toward modern birds (Figs. 1, 4, and
Today, the century-old debate on bird ancestry has 5). This newly-discovered fossil menagerie has unveiled an
largely been resolved. The uncertainties that led to this unexpected diversity of archaic birds that would take
long controversy—both empirical and methodological— birding to another dimension. These new discoveries are
have been clarified and there is an overwhelming consensus reviewed next.

Fig. 4 Cladogram or diagram

depicting the genealogical rela-
tionships among the main line-
ages of premodern birds and
some lineages of nonavian
maniraptoran dinosaurs. The
known fossil record of these
groups is also highlighted. The
concept of a dove as a living
dinosaur—because they share a
common descent—may seem
bizarre, but, in reality, it is just
as logical as the argument that
humans are primates because we
evolved from primates
Evo Edu Outreach (2009) 2:248–256 253

and in time. In the last few decades, however, our

understanding of the origin and ancient divergences of
birds has advanced at an unparalleled rate. This rapid
increase in discoveries has not only filled much of the
anatomical and temporal gaps that existed previously, but
has also made the study of early birds one of the most
dynamic fields of vertebrate paleontology.
New information highlights the fact that the enormous
diversity of living birds is just a remnant of an archaic
evolutionary radiation that can be traced back to Archae-
opteryx (Mayr et al. 2005) (Figs. 1 and 4). Few physical
features set this most ancient bird apart from its theropod
dinosaur predecessors. However, Archaeopteryx gives us
paramount clues to the beginning of one of the most
dramatic evolutionary events in the history of vertebrates—
the development of powered flight in birds. This 150-
million-year-old jay-sized bird with toothed jaws, clawed
wings, and a long bony tail stands alone in the fossil record
of birds of the end of the Jurassic period. Yet, in the last
decade, a large number and variety of birds have been
found in early Cretaceous rocks ranging from 130 to 115
million years ago (Chiappe 2007; Zhou 2004). These fossils
reveal that a great diversity of birds with long bony tails
preceded the evolution of birds with an abbreviated bony
tail (Forster et al. 1998; Zhou and Zhang 2003), one
composed of fewer vertebrae ending in a bony stump called
a pygostyle (the structure that supports the “parson's nose”).
Characteristics of the plumage, the large wing size, and
specific features of their brain all suggest that Archaeop-
teryx and the remaining long-tailed birds were fliers, even if
these birds probably required a take-off run to become
airborne (Burgers and Chiappe 1999).
A rich diversity of more advanced birds is also recorded
in these early Cretaceous rocks. In fact, the differing design
of skulls, teeth, wings, and feet indicate that, even at this
early phase of their evolutionary history, birds had
specialized into a variety of ecological niches, including
seed-feeders, insect-feeders, fish-eaters, and meat-eaters
(Chiappe 2007). At the same time, a host of novel features
Fig. 5 Photographs of the Berlin specimen of the Late Jurassic of the wings, shoulders, and tails suggests that, soon after
Archaeopteryx (a), the Early Cretaceous short-tailed bird Confuciu- Archaeopteryx, birds evolved flying abilities not very
sornis (b), long-tailed bird Jeholornis (c), enantiornithine Eoenantior-
nis (d), and primitive ornithuromorph Yanornis (e). Photographs not to different from the ones that amaze us today, a feat that
scale was most likely the recipe for their dramatic diversification
during the Cretaceous. Paramount among these transforma-
tions is the abbreviation of the tail and the consequent
The Long March Toward Modern Birds development of a pygostyle. Yet, the details of this
evolutionary transition are far from clear. One recent fossil
Research on the early history of birds and the development that has shed some light onto this transition is the tiny, 125-
of flight has been at the forefront of paleontology since the million-year-old Zhongornis (Gao et al. 2008) from
advent of evolutionary thought. For most of this time, northeastern China. Zhongornis is the first bird discovered
however, the available evidence was limited to a small that has a short tail and a corresponding reduced number of
number of fossils largely restricted to near-shore and marine tail vertebrae, yet lacks the pygostyle that is present in all
environments and was greatly separated both anatomically other short-tailed birds. Therefore, Zhongornis represents
254 Evo Edu Outreach (2009) 2:248–256

an intermediate stage between the primitive long-tailed Witmer 2002; Zhou 2004; Zhou and Zhang 2005) resemble
birds and those with a bony stump at the end of the tail. the enantiornithines, but their skeletons show, for the first
Evidence from the skeleton of Zhongornis suggests that a time, clear trademarks of their living counterparts. The
short tail with a reduced number of vertebrae evolved majority of these primitive ornithuromorphs were lightly
earlier in birds than did the pygostyle. built, flying birds, whose sizes tend to be larger than those
Very early in their evolutionary history, short bony-tailed of their contemporaneous enantiornithines. Like the latter,
birds blossomed in a range of shapes and sizes. Hundreds both their skeletons and plumage show clear evidence of
of specimens of the stout-beaked Confuciusornis, many enhanced aerodynamic capabilities. It is within these birds
surrounded by a halo of dark feathers, have been unearthed that we witness the origin of the extremely fast rates of
from the 125-million-year-old deposits of northeastern body maturation characteristic of modern birds (Chiappe
China (Chiappe et al. 1999) (Fig. 5). This crow-sized bird and Witmer 2002), which reach their full body size within a
sported long hands with enormous claws and long and year after hatching.
tapering wings. Growth series of Confuciusornis spanning a As the rocks of the Cretaceous period become younger, a
large spectrum of sizes suggest that, unlike modern birds, series of other lineages of ornithuromorphs make their
this and other archaic birds required multiple years to reach debut. The hesperornithiforms—large, flightless, foot-
adult size (Chiappe 2007). The contemporaneous and much propelled divers—first appear around 100 million years
larger Sapeornis had longer and narrower wings, superfi- ago (Chiappe 2007; Chiappe and Witmer 2002). Albeit
cially resembling those of albatrosses (Zhou and Zhang entirely restricted to the aquatic realm, the hesperornithi-
2002) (Fig. 1). Albeit bearing stout teeth and a very forms exhibit a rich and diverse evolutionary history
primitive shoulder, the anatomy of this bird suggests a spanning over 35 million years—their last representatives
closer relationship to modern birds than Confuciusornis. may have disappeared with the latest Cretaceous mass
Combined, however, these fossils best illustrate the anato- extinction that wiped out the last of the nonavian dinosaurs.
my and appearance of the most primitive short-tailed birds, Despite the fact that their earliest records represent birds the
which, by virtue of their proportionally larger wings, were size of a loon, millions of years later, these supreme fish-
likely better fliers than their long-tailed predecessors. eaters would be crowned kings of the aquatic birds with a
Fossils of more advanced birds are also first recorded at number of large forms such as the tiny-winged, four-foot
around 130 million years ago. Among these are the long Hesperornis and Asiahesperornis. The hesperornithi-
enantiornithines (Chiappe 2007; Chiappe and Witmer forms swam the waters of tropical seas that, during the late
2002), a group that constitutes the most important evolu- Cretaceous, divided in half both North America and
tionary radiation of premodern birds. Like most early birds, Eurasia. On the shore of these shallow seas, over herds of
the majority of enantiornithines had toothed jaws and duck-billed and other kinds of dinosaurs, soared the tern-
partially clawed wings (Figs. 1 and 5). Yet their skeletons sized Ichthyornis (Clarke 2004) (Fig. 1). In most respects,
show a series of key transformations that approach those of this bird represents a step closer to modern birds, yet it had
today's birds. Some of these include the shortening of the sharply toothed jaws designed to catch fish. Ichthyornis is
hand and fingers as well as changes in the proportions of perhaps the best-known, closest relative of modern birds;
the wing bones and the anatomy of the shoulder. Further- other late Cretaceous fossils seemingly close to the latter
more, these birds evolved important innovations in their are known by much more fragmentary remains.
plumage, namely, a safety device called the alula (a small Not all the birds that lived during the Mesozoic may
tuft of feathers also known as the “bastard wing”), which have looked as unfamiliar as Archaeopteryx, Confuciusor-
assists modern birds during their take-off and landing (Sanz nis, and Hesperornis. The early representatives of today's
et al. 1996). The significant transformations of the skeleton lineages of birds can also be traced back to this remote era
and plumage of these birds suggest that, even at the onset of of our geological past. In several continents, rocks from the
their evolutionary history, enantiornithines were able to last part of the Cretaceous period—75 to 65 million years
take-off from a standstill position and maneuver in ways ago—reveal the remains of early shorebirds, ducks, and
similar to those seen among living birds. It is most likely other familiar birds (Kurochkin et al. 2002; Clarke et al.
that the evolution of these enhanced flying capabilities 2005). These discoveries indicate that a number of modern
played a key role in the evolutionary success of the lineages had their origins prior to the end of the Mesozoic.
enantiornithines, which by about 120 million years ago It is unclear how these early representatives of modern
seem to have risen to dominance. birds managed to survive the devastating mass extinction of
Rocks from the early Cretaceous also record a number of the end of the Cretaceous, but these survivors diversified
transitional fossils that herald the evolution of the closest soon after into a myriad of forms, which today carry the
relatives of modern birds (Fig. 1). In some respects, these legacy of the magnificent dinosaurs that ruled the earth tens
primitive ornithuromorphs (Chiappe 2007; Chiappe and of millions of years ago.
Evo Edu Outreach (2009) 2:248–256 255

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