Ecological Monographs, 74(2), 2004, pp. 261–280
q 2004 by the Ecological Society of America
RAPID EVOLUTION OF AN INVASIVE PLANT
JOHN L. MARON,1,6 MONTSERRAT VILÀ,2 RICCARDO BOMMARCO,3 SARAH ELMENDORF,4
AND PAUL BEARDSLEY 5
2
1
Division of Biological Sciences, University of Montana, Missoula, Montana 59812 USA
Centre de Recerca Ecològica i Aplicacions Forestals, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain
3Department of Ecology and Crop Production Science, Swedish University of Agricultural Sciences, Box 7043,
SE-750 07 Uppsala, Sweden
4Environmental Science and Policy Department, University of California, Davis, California 95616 USA
5Department of Botany, University of Washington, Seattle, Washington 98195 USA
Abstract. Exotic plants often face different conditions from those experienced where
they are native. The general issue of how exotics respond to unfamiliar environments within
their new range is not well understood. Phenotypic plasticity has historically been seen as
the primary mechanism enabling exotics to colonize large, environmentally diverse areas.
However, new work indicates that exotics can evolve quickly, suggesting that contemporary
evolution may be more important in invasion ecology than previously appreciated. To
determine the influence of contemporary evolution, phenotypic plasticity, and founder effects in affecting phenotypic variation among introduced plants, we compared the size,
fecundity, and leaf area of St. John’s wort (Hypericum perforatum) collected from native
European and introduced western and central North American populations in common
gardens in Washington, California, Spain, and Sweden. We also determined genetic relationships among these plants by examining variation in amplified fragment length polymorphism (AFLP) markers.
There was substantial genetic variation among introduced populations and evidence for
multiple introductions of H. perforatum into North America. Across common gardens introduced plants were neither universally larger nor more fecund than natives. However,
within common gardens, both introduced and native populations exhibited significant latitudinally based clines in size and fecundity. Clines among introduced populations broadly
converged with those among native populations. Introduced and native plants originating
from northern latitudes generally outperformed those originating from southern latitudes
when grown in northern latitude gardens of Washington and Sweden. Conversely, plants
from southern latitudes performed best in southern gardens in Spain and California. Clinal
patterns in leaf area, however, did not change between gardens; European and central North
American plants from northern latitudes had larger leaves than plants from southern latitudes
within these regions in both Washington and California, the two gardens where this trait
was measured. Introduced plants did not always occur at similar latitudes as their most
closely related native progenitor, indicating that pre-adaptation (i.e., climate matching) is
unlikely to be the sole explanation for clinal patterns among introduced populations. Instead,
results suggest that introduced plants are evolving adaptations to broad-scale environmental
conditions in their introduced range.
Key words: amplified fragment length polymorphisms (AFLPs); EICA hypothesis; founder effects;
Hypericum perforatum; introduced plants; latitudinal clines; molecular genetic variation; population
differentiation; rapid evolution; St. John’s wort.
INTRODUCTION
Exotic species can often be larger or more fecund in
their introduced range than in their native range (Elton
1958, Crawley 1987, Fowler et al. 1996, Rees and
Paynter 1997, Buckley et al. 2003, Grosholz and Ruiz
2003). Why this may be so has remained elusive, despite growing interest in this topic. Phenotypic plasticity has traditionally been seen as a key to colonization success and a likely explanation for why indiManuscript received 10 March 2003; revised 7 July 2003;
accepted 1 August 2003; final version received 10 September
2003. Corresponding Editor: S. Lavorel.
6 E-mail: john.maron@mso.umt.edu
viduals appear so robust in recipient communities
(Marshall and Jain 1968, Rice and Mack 1991, Sultan
and Bazzaz 1993, Williams et al. 1995, Kaufman and
Smouse 2001, Novak and Mack 2001, Sexton et al.
2002, Parker et al. 2003). Species introduced to new
regions may face a more benign environment from
whence they came, either because they escape from
their native competitors or specialist herbivores and
pathogens, or because they occur in locations that possess physical conditions that are more suitable for prolonged growth (Elton 1958, Gillett 1962, Crawley
1987). Introduced plants may respond flexibly to a
more benign biotic or physical environment by growing
more vigorously or devoting more resources to repro-
261
262
JOHN L. MARON ET AL.
duction. Understanding the magnitude of these changes
in phenotype is important because size and fecundity
can greatly influence interactions between natives and
exotics and thereby critically determine colonization
success.
Although phenotypic plasticity can be an important
mechanism allowing exotics to succeed in recipient
communities, so too may evolution. Early classic studies on plants highlighted the fact that exotics often have
substantial evolutionary potential (Baker and Stebbins
1965, Baker 1974, Jain and Martins 1979, Brown and
Marshall 1981). Yet, the idea that evolution could be
an important force in the ecology of invasions has been
mostly neglected in the ecological literature on exotics.
Only recently have ecologists recognized that species
introduced to new environments can evolve rapidly
(Losos et al. 1997, Reznick et al. 1997, Weber and
Schmid 1998, Yom-Tov et al. 1999, Huey et al. 2000,
Bone and Farres 2001, Lee 2002) and that rapid genetically based adaptation to novel environments might
be more important in the ecology of invasions than
previously thought.
Two distinct but not mutually exclusive classes of
selection pressures might drive contemporary evolution within exotic plant populations. First, liberation
of exotic plants from their natural enemies might lead
to the evolution of increased plant size or fecundity.
Blossey and Nötzold (1995) proposed that introduced
plants that are no longer attacked by specialist enemies
should lose costly herbivore defense and re-allocate
resources previously spent on defense to traits that enhance competitive ability, such as increased size or
fecundity. The evolution of increased competitive ability (EICA) hypothesis predicts that introduced plants
should universally be larger or more fecund than their
native conspecifics; if true, it implies that rapid evolutionary change may play a key role in invasion success.
Tests of the EICA hypothesis have been inconclusive. Both Siemann and Rogers (2001) and Blossey and
Nötzold (1995) found introduced individuals were larger or more fecund than native individuals of Chinese
tallow trees (Sapium sebiferum) and purple loosestrife
(Lythrum salicaria), respectively. Leger and Rice
(2003) found that introduced California poppies (Eschscholzia californica) from Chile were larger and
more fecund than native Californian conspecifics in
common gardens, but only in the absence of competition. On the other hand, Willis et al. (2000) grew four
species of plants collected from their native European
and introduced ranges in a common garden in Britain
and found no evidence that introduced plants had
evolved increased size. Thébold and Simberloff (2001)
similarly found no consistent evidence (based on data
in accounts of the flora of Europe and the United States)
that introduced genotypes were larger than their native
counterparts.
Ecological Monographs
Vol. 74, No. 2
Second, geographic gradients in abiotic conditions
across the introduced range could impose divergent
selection and promote genetically based differentiation
among introduced populations. A classic manifestation
of this would be the evolution of geographic clines, as
is often found among native populations occurring
across altitudinal or elevational gradients (Turreson
1930, Clausen et al. 1940, Neuffer and Hurka 1986,
Lacey 1988, Galen et al. 1991, Winn and Gross 1993,
Jonas and Geber 1999). Yet, whether introduced plant
populations rapidly evolve clines in response to environmental conditions across their introduced range is
seldom studied (but see Neuffer 1990, Weber and
Schmid 1998, Neuffer and Hurka 1999). Furthermore,
whether clines in traits among introduced plant populations broadly converge on those expressed among
native conspecifics occurring over similar latitudinal or
elevation gradients is unknown. There is certainly precedence for such clinal convergence. Introduced populations of Drosophila subobscura have rapidly
evolved clinal variation in wing shape that converges
on that found for native fruit flies occurring across a
similar latitudinal gradient (Huey et al. 2000).
Here, by means of common garden experiments in
the native and introduced range and genetic analyses
of plants, we explore whether the widespread exotic
plant, St. John’s wort (Hypericum perforatum), has undergone contemporary adaptive evolution (sensu
Stockwell et al. 2003) in its introduced range. Specifically, we ask: (1) whether introduced St. John’s wort
populations have evolved latitudinally based clines in
size, fecundity, leaf area, or survival, as might be expected if abiotic conditions drive adaptation, (2) whether native populations of St. John’s wort also exhibit
clinal variation in traits in common gardens, and if so,
how clines in the native and introduced range compare,
and (3) whether introduced H. perforatum has evolved
larger size or fecundity in response to an enemy-free
environment, as predicted by the EICA hypothesis. Because of St. John’s wort’s history of introduction,
spread, and subsequent control, our study provides a
unique test of the EICA hypothesis. In western North
America, St. John’s wort has been exposed to biocontrol for over 50 years, whereas introduced plants in
central North America have either never been exposed
to biocontrol or in a few localities have had a much
more recent exposure to biocontrol (Julien and Griffiths
1998). Although many factors besides exposure to biocontrol (for example, climate) potentially contribute
toward selecting for particular traits in western and
central North American populations, if the EICA hypothesis is correct, plants liberated from specialist herbivores that reside in central North America should
tend to be larger or more fecund than plants from European populations when grown in common gardens.
Additionally, EICA predicts that plants from western
North American populations should be intermediary in
EXOTIC PLANT ADAPTATION
May 2004
size between central North American and European
plants as a result of their biocontrol history.
While comparison of traits in common gardens provides insight into whether there has been genetically
based differentiation among introduced populations,
evidence for clinal differentiation does not, in itself,
necessarily imply contemporary evolution. Multiple introductions from a genetically diverse source pool
could produce a good match between the set of conditions a genotype is adapted to and the conditions it
experiences where introduced (Neuffer and Hurka
1999). If this is the case, no evolution has occurred;
rather, introduced genotypes only persist in areas where
they are pre-adapted. Alternatively, clinal patterns in
traits within common gardens could result from adaptive evolution within the introduced range. This could
occur either as a result of adaptive radiation from a
limited number of founding genotypes, or from multiple introductions that provide sufficient genetic variability on which selection can act. To differentiate between these alternatives, we used amplified fragment
length polymorphism (AFLP) markers to examine genetic relationships between native and introduced
plants, and thereby infer the invasion history of St.
John’s wort.
METHODS
St. John’s wort natural history
St. John’s wort is a short-lived rhizomatous perennial
native to Europe, North Africa, and Asia. These plants
inhabit old fields, overgrazed, or otherwise disturbed
grasslands, forest clearings, gravel river banks, and
road sides. Individuals grow as prostrate mats in winter,
then bolt, flower, and set seed in summer. After seed
set, plants senesce aboveground until winter rains initiate new procumbent growth.
As an introduced weed, St. John’s wort is widely
distributed. It has been introduced into Australia, New
Zealand, South Africa, and North and South America.
In the United States, St. John’s wort was first found in
1793, in Lancaster, Pennsylvania. St. John’s wort was
found in some portions of the Midwest in the mid1800s (Sampson and Parker 1930, Voss 1985) and on
the West Coast, in Oregon, between 1840 and 1850.
By the early 1900s, St. John’s wort was found in California (Campbell and Delfosse 1984, Voss 1985). Biological control of St. John’s wort in western North
America was first initiated in 1945, with the introduction of a chrysomelid beetle, Chrysolina quadrigemina
(Huffaker and Holloway 1949, Holloway and Huffaker
1951). Beetles established and killed many plants;
within five years of introduction in California, H. perforatum was reduced to ,1% of its former abundance
(Holloway 1957). Whether biocontrol in the West is
currently as efficacious as it was initially is not well
documented. In central North America, St. John’s wort
never reached the densities observed in the West, likely
263
because cropland habitat is not ideal for St. John’s wort.
Biocontrol introductions in eastern North America occurred much later than in western North America (in
1969 vs. 1945); biocontrol beetles have only recently
spread to several eastern states and Minnesota (Harris
and Maw 1984, Fields et al. 1988, Hoebeke 1993, Julien and Griffiths 1998). Thus, throughout central North
America, St. John’s wort has either never been exposed
to biocontrol or plants have had a much more limited
history of herbivore exposure than have plants in western North America. Censuses of multiple introduced
populations indicate that in the absence of biocontrol
agents, St. John’s wort receives minimal herbivore
pressure by native generalists (J. L. Maron and M. Vilà,
unpublished data). Plants we out planted into common
gardens received little or no herbivore damage.
Seed collection
In late summer 1998 and 1999, we collected mature
seed capsules of H. perforatum from three distinct regions: Europe, western North America, and central
North America (N.A.). We collected seeds from 18 native populations (17 in Europe plus one population in
Kyrgyzstan; for simplicity we collectively refer to all
18 populations as European), 18 introduced western
North American populations, and 14 introduced central
North American populations (see Appendix for additional information on seed source populations and collection methods). Seed capsules were collected from
10–14 haphazardly chosen individuals per population,
except European populations 5, 10, 12, and 13 (see
Appendix for location of populations), where we collected a pooled sample of capsules from .10 individuals.
Common garden experiments
We established two large common gardens in Snohomish, Washington, USA, and at the Mas Badia Experimental Field Station (IRTA) near Girona, Spain, in
spring 2000. In 2001, we established two additional
smaller common gardens, on the Wantrup Preserve in
Pope Valley, California, USA, and near Sörby on the
island of Öland, Sweden (see Table 1 for information
on common garden sites, dates of transplant, number
of individuals, and populations used in each garden,
etc.) In each garden, individuals from each population
were maternal sibs of those planted in other gardens.
Since St. John’s wort produces upwards of 90% of its
seed apomictically, maternal sibs planted in all gardens
were likely clones (Robson 1968, Arnholdt-Schmitt
2000). To ensure that transplants were not overtopped
by surrounding grasses, we periodically mowed between plots and/or hand-clipped grasses immediately
surrounding experimental plants. St. John’s wort occurred naturally near each garden site. Plot spacing and
the layout of plants among gardens differed due to
space and other logistical considerations. The com-
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Vol. 74, No. 2
JOHN L. MARON ET AL.
264
TABLE 1. Comparison of the four common garden sites with respect to physical conditions and timing of plant propagation,
outplanting, and measurement.
Location
Snohomish, Washington
Pope Valley, California
Sörby, Sweden
Girona, Spain
Latitude
478529
388369
568509
428199
N
N
N
N
Mean annual
Mean daily
precipitation
maximum
(cm)
temperature (8C)
123
106
42
62
22.8
30.8
27.6
31.0
Mean daily
Dates plants
minimum
propagated in
temperature (8C)
greenhouse
0.7
2.9
27.7
10.0
March 2000
January 2001
April 2001
March 2000
Individuals
used per
population
10
9
9
14
Note: Plants were propagated in greenhouses at the University of Washington (for Washington and California), the University
of Barcelona (for Spain), and the Swedish University of Agricultural Sciences (for Sweden).
petitive environment across gardens was roughly similar.
Washington common garden.—We established 10
replicate, 8.5 3 12 m blocks composed of six 1.5 3
12 m plots separated by 2 m. Plants in three of these
plots were exposed to herbivory by Chrysolina quadrigemina as part of a separate experiment and not discussed here. One individual from each population within a given region was randomly assigned to the same
plot within blocks. Thus, each plot within a block contained plants from a different region. Across blocks,
plots contained a unique individual from each population. Plots consisted of two rows of nine individuals
(spaced 1.5 m apart) from each of 18 populations. Since
we only collected seed from 14 central North American
populations, we added four randomly selected replicate
plants to each central North American plot to maintain
plant density at 18 in each plot. No data were collected
from these replicate plants.
In September 2000, 2001, and 2002, we estimated
plant fecundity: in 2000 by clipping and counting the
seed capsules on each plant (n), and in 2001 and 2002
by harvesting, drying, and weighing seed capsules
since plants had too many capsules to count individually. On a subset of plants in 2001 and 2002, we both
counted and weighed seed capsules to determine the
relationship between capsule mass (M ) and capsule
number (N ). We used these regressions (2001 regression, N 5 44.45M 2 3.71, R2 5 0.93, P , 0.0001, n
5 43; 2002 regression, N 5 43.5M 1 22.2, R2 5 0.97,
P , 0.0001, n 5 85) to convert capsule mass into
capsule number each year.
We censused all plants in July 2001 and 2002. We
estimated plant size by treating each plant as a cylinder
and calculating cylindrical volume (V). To do this, we
measured the width of each plant in perpendicular directions (W1 and W2) and then measured the height of
the tallest stem (H ); thus, V 5 p[(W1 1 W2)/4]2 3 H.
In July 2002, we randomly chose one of two opposite
leaves at the sixth node on the tallest stem on each
plant and measured the length and maximum width of
this leaf on all plants. These leaves were similar in size
to those sampled at other nodes on the same plant (Pearson r 5 0.74). We calculated the relationship between
leaf length (L) 3 maximum width (W ) and leaf area
(LA) by measuring leaf length and width of greenhouse-grown plants and then estimating their area by
using image analysis performed on a Macintosh computer using public-domain NIH image program version
1.62 (developed at the U.S. National Institute of Health;
available online)7 to analyze digitally scanned images
of these leaves when dried and flattened. We then applied the equation LA 5 [(W 3 L) 3 0.785] 1 0.002
(R2 5 0.99, n 5 500) to field-measured leaves to convert leaf size to leaf area.
California common garden.—We established nine
replicate blocks composed of six plots (three of which
were used for a separate experiment and not discussed
here). Plants from a given region were all assigned to
the same randomly chosen plot within blocks. Plots
consisted of two rows of six plants from the same region but from different populations within that region,
except for central North American plots that contained
two rows of five plants. Plants within plots were separated by 1 m, plots were separated from each other
by 1.5 m, and blocks were separated from each other
by 2 m.
In April 2002, we censused all plants and estimated
plant size, as described in Methods: Common garden
experiments, Washington common garden. We also
measured the length and width of one randomly chosen
leaf at the fourth node on the tallest stem of each plant.
We then converted leaf size to leaf area, as described
above. We censused all plants and estimated plant fecundity in late July 2001. Only six plants produced
seed capsules, and these plants produced no more than
a few capsules each. In mid-July 2002, we again censused plants and estimated fecundity, as we did in
Washington in 2002.
Spain common garden.—We randomly assigned one
individual from each population within a region to one
of 14 4 3 4 m plots (42 plots total). Individuals within
plots were separated by 1 m, and plots were separated
by 2.5 m.
In September 2000, we censused all plants and estimated fecundity by counting seed capsules on plants.
In April 2001, after plants had been in the field for 11
months, we censused and measured all plants. At this
7
URL: ^http://rsb.info.nih.gov/nih-image/&
EXOTIC PLANT ADAPTATION
May 2004
TABLE 1.
265
Extended.
Populations used per region
Europe
Western
North
America
Central
North
America
Field preparation
prior to transplant
Transplant
date
Dates plant
size measured
18
12
10
16
18
12
9
16
14
10
9
13
mowed and tilled
mowed and tilled
mowed
mowed and tilled
April 2000
March 2001
April 2001
June 2000
July 2001, 2002
April 2002
June 2002
April 2001
time, most individuals had not yet bolted and grew as
prostrate mats that were roughly circular. We estimated
mat area (MA) by measuring the diameter of each mat
in two perpendicular directions (L1 and L2) and converting these values to area (where MA 5 ((L1 1 L2/
4)2 3 p). Mat area prior to bolting is correlated to
plant size after bolting (Pearson r 5 0.65, P , 0.0001).
In late October 2001, we again censused all plants and
estimated fecundity by harvesting, drying, and weighing seed capsules. We converted capsule mass into capsule number, as was done for plants grown in Washington in 2001.
Sweden common garden.—We established nine replicate blocks composed of three plots, with each plot
containing plants from a single region. Regions were
randomly assigned to plots within blocks. Plants were
spaced 1.2 m apart within a plot, plots within blocks
were separated by 1.5 m, and blocks were separated
from each other by 3–4 m.
In mid-June 2002, we censused all plants and counted the number of shoots on each individual. In midSeptember 2002, we harvested, dried, and weighed
seed capsules from each plant, as described in Methods:
Common garden experiments, Washington common
garden.
Analysis of common garden data
Within each garden, we determined whether there
was significant differentiation in plant size, fecundity,
or leaf area based on latitude of population origin. Latitudinally based differentiation within a common garden is classic evidence for a geographic cline, and suggests that plants have adapted to the broad-scale environmental conditions experienced across their home
environment (i.e., Europe for native genotypes and
North America for introduced genotypes). After statistically controlling for latitude, we explored whether
plant size or fecundity varied based on region of population origin, as predicted by the EICA hypothesis.
To make these comparisons, in the PROC GLM module
within SAS (2001) we performed an ANCOVA with
Type I sum of squares, using the following model: response variable 5 block (except for Spain where plants
were not blocked in the field) 1 latitude of population
origin 1 region of population origin 1 latitude 3 region 1 population nested within region 1 error. Block
Dates fecundity
estimated
September
July 2001,
September
September
2000, 2001, 2002
2002
2002
2000, October 2001
and population nested within region were random factors, region was a fixed factor, and latitude was a covariate. A significant population within region effect
indicates that there is population differentiation and
that this differentiation is not due to latitude of origin
(since variation among populations due to latitude is
removed before testing the population with region effect). We used Type I rather than Type III sum of
squares because most populations had unique latitudes
of origin (Table 1) and there were insufficient degrees
of freedom to simultaneously use latitude and population nested with region within a Type III sum of
squares model. Response variables in these analyses
were plant volume (log-transformed to meet assumptions of the ANCOVA), fecundity (or cumulative fecundity across two and three years for plants grown in
Spain and Washington, respectively), and leaf area. We
performed Bonferroni post hoc comparisons to examine pairwise differences between regions in mean size
or fecundity. To determine how mortality varied based
on latitude of population origin, we calculated mortality within each population in a given garden and
regressed these population mortality values on latitude
of population origin. To examine clinal patterns among
introduced plants in isolation, we combined data from
western and central N.A. and performed Type I sum
of squares ANCOVAs on these data from each garden.
We tested for effects of block, latitude, and population,
with population and block as random factors and latitude as a covariate.
Finally, we compared the total phenotypic variation
among European and western North American populations in each garden, respectively. If there had been
a large founder effect and a limited number of genotypes introduced into North America, one might expect
phenotypic variation to be greatly reduced among introduced plants compared to natives. To examine this,
we calculated the percentage of the total among-population phenotypic variance (based on adjusted population means from the ANCOVA) that was accounted
for by native and introduced populations. This test requires roughly balanced numbers of individuals and
populations from each region, since differences in sample size can bias variance estimates. In cases where the
number of populations sampled was unequal between
regions (fecundity in Sweden), we randomly chose an
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Vol. 74, No. 2
JOHN L. MARON ET AL.
266
equal number of populations from each region. We excluded populations from central N.A. from this analysis
since the number of populations sampled was smaller
and therefore not comparable to those sampled in Europe and western N.A. We omitted data from Spain, as
high mortality in that garden made for an extremely
unbalanced design.
Genetic relations between native
and introduced plants
We used amplified fragment length polymorphisms
(AFLPs; Vos et al. 1995, Mueller and Wolfenbarger
1999) to determine genetic relationships between individuals and populations. We clipped leaves from
four randomly chosen individuals from each population within the Washington common garden. We extracted total genomic DNA from either fresh, green
leaves or leaves that had been frozen using standard
procedures (Vos et al. 1995) to produce AFLPs with
the following modifications. We digested 400–500 ng
of DNA from each plant and ligated adaptors (MseI
and EcoRI) to the ends in a reaction mixture that contained 5 m L 10 3 RL buffer (100 mmol/L Tris-Acetate
pH 7.6, 100 mmol/L Mg-Acetate, 500 mmol/L K-Acetate, 50 mmol/L dithiothreitol), 50 pmol/L EcoRI
adapter, 50 pmol/L MseI adapter, 1 m mol/L 10 mmol/
L ATP, 1 unit of T4-DNA ligase, and water to a final
volume of 50 m L. Adapter sequences are the same as
those described by Xu et al. (2000). After digestion
and ligation, products were diluted 1:4 with water.
Digestion/ligation products were amplified with one
selective nucleotide using polymerase cahin reaction
(PCR) as described in Vos et al. (1995). In the second
round of PCR, products were amplified with primers
(EcoRI and MseI) labeled using LICOR IRD-800 or
LICOR IRD-700 dyes (LI-COR Biosciences, Lincoln,
Nebraska, USA). In total, 25 primer pairs were used.
Amplification products were visualized using gel electrophoresis on a LI-COR Long ReadIR DNA sequencer. Digital AFLP gel images were scored using AFLPQuantar scoring software (Keygene products B.V.,
Wageningen, The Netherlands) and also carefully
checked by eye to ensure Quantar scoring was accurate. Prior to analysis, we eliminated one individual
from populations Spain 1, France 7, Czech 14, Ontario
10, and Michigan 14, because these plants had anomalously low numbers of AFLP fragments. It is likely
that methodological problems during sample preparation led to these anomalies.
Analysis of genetic data
We recorded AFLP band presence or absence for
each sample as a binary character. We then analyzed
this data matrix in two ways. First, using PAUP* 4.0
(Swofford 1998), we determined relationships among
H. perforatum individuals and populations using neighbor-joining, a distance-based analysis. Estimates of
similarity were calculated using the index of Nei and
Li (1979). We also constructed trees based on parsimony analyses, but these analyses produced qualitatively very similar trees that recovered the same wellsupported clades as those based on neighbor-joining.
We arbitrarily picked population 16 from England as
the out group because relationships are more easily visualized using rooted trees. Using other out groups yielded qualitatively similar results. Bootstrap values (Felsenstein 1985) for the neighbor-joining tree were calculated using 1000 replicate neighbor-joining searches.
Second, we used analysis of molecular variance
(AMOVA; ARLEQUIN software version 2.0, Schneider et al. 2000) to determine how total neutral molecular genetic variation was partitioned between regions
and among populations within regions. AMOVA calculates pairwise squared Euclidean distances among
AFLP phenotypes, and from these estimates Fst, the
percentage of total molecular variation that is due to
differences among specified hierarchical groups (in our
case, between regions of population origin, among populations within regions, and within populations). We
first used AMOVA to determine how genetic variation
was partitioned between regions and among populations within regions. We then asked, within a given
region, how the percent of total molecular genetic variation was partitioned within and among populations.
For both of these analyses, we used only data from
European and western North American genotypes,
since an equal number of populations within these regions were sampled.
RESULTS
Genetic relationships between native
and introduced plants
Together, 25 AFLP primer pairs generated 302 polymorphic markers across all samples analyzed. Among
195 individuals, we detected 195 unique AFLP phenotypes. When examined together, individuals from introduced and native populations clustered in several
well-supported clades (Fig. 1). The fact that individuals
from the introduced range cluster in multiple clades
indicates that there have likely been repeated introductions of St. John’s wort into North America (Fig.
1). One well-supported clade contains individuals from
multiple populations collected in Spain, France, and
California, while other well-supported clades contain
individuals from populations originating from western
and central N.A., as well as individuals from Europe.
As was the case for European populations, plants from
the same North American populations usually clustered
together (see Fig. 1, exceptions: Wisconsin 2–1, Wisconsin 2–3, Michigan 6–10, Ontario 10–5, California
2–4, California 9–7, Oregon 12–8, Oregon 14–14,
Oregon 18–10).
Analysis of molecular variance revealed that only
10.42% of the total molecular genetic variation among
European and western North American samples was
EXOTIC PLANT ADAPTATION
May 2004
accounted for by region of origin (i.e., Europe vs. western N.A.). The majority of molecular variation (65.6%)
was partitioned among populations within regions, with
the remaining molecular variation (23.91%) partitioned
within populations. For European samples in isolation,
65.67% of the variation in AFLP haplotypes was due
to differences in diversity among populations, whereas
34.33% of the molecular genetic variation was contained within populations. For western North American
genotypes, 78.2% of the molecular genetic variation
was contained among populations, and 21.88% was
contained within populations. Thus, for both native and
introduced plants, greater genetic variability was preserved among vs. within populations.
Differences between native and introduced plants
in size and fecundity
There were significant differences in size between
native and introduced plants within Spain and Washington common gardens but not within California and
Sweden gardens (Table 2). In Spain, plants from European populations were larger (84 650 cm3 6 23 498
[unadjusted mean volumes 6 1 SE]) than those from
either central (45 779 cm3 6 25 241) or western (47 139
cm3 6 22 752) North American populations (post hoc
comparison, P , 0.05). In Washington, the same was
true (191 322 cm3 6 40 352, 169 257 cm3 6 27 966,
and 122 199 cm3 6 26 979 for European, central and
western North American plants, respectively; post hoc
comparison, P , 0.05).
Cumulatively, western North American plants produced more seed capsules over three years (unadjusted
mean 5 2748 6 237) than did European (2368 6 266)
and central North American (2430 6 160) plants in
Washington (Table 3; post hoc comparison, P , 0.05).
In Sweden, western North American plants also produced more seed capsules (unadjusted mean 5 468 6
42) than did central North American (453 6 42) or
European (405 6 40) plants (post hoc comparison, P
, 0.05). However, in California, European plants produced more seed capsules (unadjusted mean 5 783 6
250) than did either central or western North American
individuals (unadjusted means 5 115 6 54 and 683 6
225 for central and western North American populations, respectively; post-hoc comparison, P , 0.05;
Table 3). In Spain, there was no significant difference
in fecundity based on region of origin (Table 3). Thus,
in contrast to the prediction of the EICA hypothesis,
introduced plants were neither consistently larger nor
more fecund than natives across all gardens.
Clinal variation
Plant size.—St. John’s wort from diverse native European and introduced North American populations exhibited significant latitudinally based clines in size in
California, Sweden, and Washington, and marginally
significant clines in size in Spain (Figs. 2 and 3, Table
2). In relatively northerly common gardens in Sweden
267
and Washington, plants from populations originating
at northern latitudes grew larger than plants from southern latitudes (Fig. 2). In more southern latitude common gardens in California and Spain, the opposite pattern prevailed; plants originating from southern latitudes were larger than plants originating from northern
latitudes (Fig. 3). When introduced North American
plants were analyzed separately, there were significant
clinal patterns in size in common gardens in California
(F1,20 5 8.5, P , 0.008), Sweden (F1,22 5 10.1, P ,
0.005), and Washington (F1,30 5 16.4, P , 0.003) and
a marginally significant cline in Spain (F1,27 5 3.7, P
5 0.07).
Plant fecundity.—Both introduced and native plants
produced abundant seed capsules in their first summer
in Washington and Spain. In Sweden and California,
plants did not flower and set seed until their second
summer (with the exception of six individuals in California that each produced fewer than 10 seed capsules). Among all populations, fecundity varied in a
strong clinal pattern in all common gardens except
Spain, where there was a marginally significant effect
of latitude on fecundity (Figs. 4 and 5, Table 3). As
was the case for size, plants from northern latitudes
outperformed plants from southern latitudes in northern
common gardens in Sweden and Washington (Fig. 4),
but performed less well than plants from southern latitudes when grown in southern common gardens in
California and Spain (Fig. 5).
In Washington, clinal patterns in fecundity switched
dramatically between years. Mean cumulative fecundity (across years one and two) among populations was
negatively related to latitude of population origin (Fig.
4). Plants from southern latitudes performed better than
those from northern latitudes despite the fact that the
Washington garden was at a more northerly latitude.
However, in their third year (2002), fecundity was higher for plants from northern latitudes than those from
southern sites (Fig. 4). This clinal shift coincided with
large differences between years in rainfall. The winter
of year two (2001) was unusually dry (mean cumulative
rainfall from January to May 5 38.7 cm) and significantly drier than the 20-year rainfall average for this
period (57.4 cm [one-sample t test, t 5 7.4, P ,
0.0001]). This created conditions more similar to what
typically would be found at a more southerly locale.
Since seed capsule production in year two made up the
lion’s share of the cumulative two-year total, the environmental conditions during year two had a predominant impact on cumulative fecundity in the first two
years. However, in year three (2002), cumulative rainfall during January–May was 58.5 cm, not significantly
different from the long-term average (one-sample t test,
t 5 0.05, P 5 0.95).
Introduced populations, when analyzed alone, exhibited significant clines in fecundity in California
(F1,20 5 11.3, P , 0.003), Sweden (F1,17 5 11.3, P ,
0.003), and Washington (cumulative fecundity across
268
JOHN L. MARON ET AL.
Ecological Monographs
Vol. 74, No. 2
FIG. 1. Neighbor-joining tree of 195 Hypericum perforatum genotypes from 50 populations across Europe and North
America. The first number after the country or state name is the population number, followed by the individual number (see
the Appendix for the specific geographic location that corresponds to each population number). Numbers at nodes represent
confidence levels for clades with .49% bootstrap support based on 1000 replicates. At right, colored bars represent latitudinal
ranges encompassing the latitude at which each individual was collected. Please note that the bottom of Fig. 1a (left) continues
at the top of Fig. 1b (right).
May 2004
EXOTIC PLANT ADAPTATION
FIG. 1.
two years, F1,30 5 9.7, P , 0.004), but not in Spain (P
5 0.27). Because of the switch in plant fecundity between the first two years (2000 and 2001) and the third
(2002), there was no significant clinal pattern in cumulatively three-year fecundity in Washington (P 5
0.88).
269
Continued.
Leaf size.—Plants exhibited significant clinal variation in leaf area in Washington and California (Table
4). Unlike for size and fecundity, however, populations
did not change rank between the northern and southern
common gardens. Instead, individuals from northern
latitude populations had larger leaves than those from
Ecological Monographs
Vol. 74, No. 2
JOHN L. MARON ET AL.
270
TABLE 2. Results from ANCOVAs testing for the effect of block (except in Spain), latitude of population origin, region
of population origin, latitude 3 region interaction, and population nested within region on plant size in California (CA),
Sweden (SW), Spain (SP), and Washington (in the third year [2002]; WA).
CA
SW
Source
df
MS
F
P
df
MS
F
P
Block
Latitude
Region
Latitude 3 region
Population(region)
Error
8
1
2
2
28
252
8.4
6.4
0.8
0.2
14.1
47.7
5.5
12.7
0.8
0.2
2.7
0.0001
0.001
0.47
0.81
0.0001
8
1
2
2
23
186
112.9
434
42.1
9.5
258.8
1262
2.1
37.2
1.9
0.4
1.7
0.04
0.0001
0.18
0.64
0.03
southern latitude populations in both gardens (Fig. 6).
When introduced plants were analyzed in isolation, we
found no significant effect of latitude on leaf area, in
either the Washington (F1,30 5 0.4, P 5 0.53) or California gardens (F1,20 5 1.9, P 5 0.19).
Other components of variation in size and fecundity
among introduced and native plants
In all gardens, there were significant differences in
size and fecundity among individuals from different
populations, even after variation due to latitude of origin was removed (Tables 2 and 3). This was true not
only for introduced and native populations combined,
but also in analyses using only introduced plants (P ,
0.02 in all gardens). Thus, introduced plants from divergent populations were genetically differentiated,
with this differentiation based both on latitude as well
as other unknown factors that varied between populations.
Introduced plants from western North American populations exhibited almost as much, or in some cases
even greater, phenotypic variation in size and fecundity
as did natives. For example, in Washington, western
North American populations accounted for almost 61%
of the total among population variation in size. In Sweden, introduced populations accounted for over 71% of
the total among population variation in fecundity (Table 5). For size in California and Sweden, and fecundity
in California and Washington, total phenotypic variation was relatively equally partitioned among introduced and native populations (Table 5).
Patterns of mortality
Across all populations, mortality in common gardens
in California, Washington, and Sweden was remarkably
low, despite the fact that common gardens contained
plants originating from widely disparate localities. In
California, only 6% (out of 300) of all plants died after
16 months in the field. In Washington, after 29 months
in the field, 4.6% (out of 500) of plants died (excluding
an entire block of 50 plants from all regions that were
overgrown by grasses and killed during late spring of
their second year). In Sweden, 9.7% (out of 248) of
plants died in the 14 months they were in the field. In
all of these gardens, the percentage mortality of indi-
viduals within each population was significantly correlated with latitude of population origin (R2 5 0.18,
F1,32 5 7.1, P , 0.01 for California, R2 5 0.16, F1,26
5 4.8, P , 0.037 for Sweden, and R2 5 0.08, F1,48 5
4.3, P , 0.05 for Washington). For these three gardens,
mortality was always lowest within populations that
originated from latitudes closest to that of the common
garden and highest within populations that originated
at more distant latitudes from that of the common garden.
In Spain, mortality was substantially higher than in
the other gardens. Fifty-three percent of all individuals
(of 630) initially planted in the common garden died
throughout the 16 months of the study. Mortality was
high in part due to pathogen attack. Plants were attacked in their second spring by three conspicuous fungal pathogens (Colletotrichum spp., Fusarium spp., and
Gliocladium spp.). Pathogens killed more plants from
western N.A. than from the other two regions (Pearson
chi-squared test, x2 5 24.0, P , 0.001; percentage of
plants from each region killed 5 21%, 22%, and 43%
for Europe, central, and western N.A., respectively).
We compared the average fecundity (from the first year
in 2000) of western North American plants that were
later killed by pathogens in the second year and those
that survived. Plants killed by pathogens in 2001 produced significantly more seed capsules in 2000 than
did those plants that survived pathogen attack (500 vs.
290 seed capsules for plants that died later or survived,
respectively; ANOVA, F1, 172 5 7.9, P , 0.006). In
contrast, there was no difference in seed capsule production in 2000 between European plants that (in 2001)
were killed by pathogens and those that survived to
produce seeds (ANOVA, F1, 170 5 0.08, P 5 0.72).
Thus, there was differential mortality of the most fecund western North American plants, leaving behind
those individuals that produced low numbers of seed
capsules. Since introduced populations in their first
year of reproduction (2000) exhibited significant clinal
variation in fecundity (F1,24 5 6.9, P , 0.01), differential mortality before reproduction in year two likely
explains why there were no clinal patterns in cumulative fecundity across both years in Spain (Fig. 5).
DISCUSSION
Exotic species often are introduced into diverse recipient communities. To succeed, these species must
EXOTIC PLANT ADAPTATION
May 2004
TABLE 2.
271
Extended.
SP
WA
df
MS
F
P
df
MS
F
P
1
2
2
39
260
6.8
22
0.7
68.9
146
3.2
5.2
0.2
3.2
0.085
0.01
0.84
0.0001
8
1
2
2
44
374
37.1
65.8
26.8
6.5
66.8
204
4.6
42.7
8.8
2.1
2.8
0.0001
0.0001
0.0006
0.13
0.0001
cope with different environmental conditions than what
they have experienced in their native site of origin.
How introduced species respond to novel environmental challenges in their new range remains unclear. We
compared molecular genetic variation and the phenotypes of native and introduced St. John’s wort in reciprocal common gardens in order to infer the role of
rapid adaptive evolution, phenotypic plasticity, and
founder effects in influencing colonization ability of a
widespread exotic. While common garden experiments
and molecular analysis of genetic variation are increasingly used in studies of exotics, these two approaches
are seldom combined to explore the evolutionary biology of introduced species.
Differences between native and introduced plants
in size and fecundity
Both plants and marine invertebrates can be larger
in their introduced range than in their native range
(Pritchard 1960, Crawley 1987, Fowler et al. 1996,
Rees and Paynter 1997, Buckley et al. 2003, Grosholtz
and Ruiz 2003). Yet, whether this is due to plasticity
in response to benign recipient environments or evolutionary change brought about by unique selection
pressures in the introduced range is not well understood. Pritchard (1960) was the first to provide limited
evidence that increased stature in an exotic plant could
be due to evolution. Based on measurements from a
limited number of genotypes of St. John’s wort in a
single common garden he asserted ‘‘. . . data obtained
from various populations indicate that those collected
from habitats where the species is a weed are much
taller than those collected from natural or semi-natural
habitats.’’
In our study, we found no evidence to support Pritchard’s (1960) assertion. Plants from central N.A. were
neither universally larger nor more fecund that natives
across gardens. Furthermore, western North American
plants were not smaller than those from central N.A.,
which one might expect if increased biocontrol pressure affects allocation of resources to defense, at the
expense of size or fecundity. Although we only estimated the aboveground size of plants in common gardens, in greenhouse experiments we have found no
difference in shoot:root ratios between native and in-
troduced genotypes (S. Elmendorf, J. L. Maron, and
M. Vilà, unpublished manuscript).
In general, evidence for the evolution of increased
size within introduced plant populations has been
mixed. However, comparisons have mostly involved
plants from a limited number of native and introduced
populations grown in only one common garden (Pritchard 1960, Blossey and Nötzold 1995, Willis et al.
2000, Siemann and Rogers 2001, but see Willis and
Blossey 1999) or two common gardens placed in relatively close proximity within the introduced range
(Leger and Rice 2003). While these experiments have
been valuable first steps in testing predictions of the
EICA hypothesis, positive results from a single common garden at best only evaluate the evolutionary potential of introduced genotypes. An unambiguous demonstration of genetically based changes in phenotype
requires reciprocal transplant experiments in the field.
Our results serve to highlight this fact. Results from
one or even two gardens were not necessarily mirrored
across all gardens. For example, there were strong differences in fecundity between western North American
plants and European plants in common gardens in
Washington and Sweden, but not in California and
Spain. Had we only established one common garden,
for instance in Washington, we would have come to
the erroneous conclusion that introduced plants had
evolved higher fecundity than natives.
Clinal variation
Although we found no support for the EICA hypothesis, we did find latitudinally based clines in fitness
in almost all gardens. This suggests that both native
and introduced St. John’s wort have adapted to the
broad-scale abiotic conditions experienced across their
current range. Since trait values were significantly different among populations even after the effects of latitude had been statistically removed, at least for native
populations, it is likely that genetic drift and/or other
sources of selection in addition to broad-scale climate
have driven genetic differentiation. In addition to genetically fixed differences in traits, both native and
introduced plants exhibited substantial phenotypic
plasticity, as evidenced by the dramatic change in the
slope of clines in northern vs. southern common gar-
Ecological Monographs
Vol. 74, No. 2
JOHN L. MARON ET AL.
272
TABLE 3. Results from ANCOVAs testing for the effect of block (except in Spain), latitude of population origin, region
of population origin, latitude 3 region interaction, and population nested within region on number of seed capsules (or
cumulative seed capsules produced across two or three years in Spain and Washington, respectively) in California (CA),
Sweden (SW), Spain (SP), and Washington (WA).
CA
SW
Source
df
SS
F
P
df
SS
F
P
Block
Latitude
Region
Latitude 3 region
Population(region)
Error
8
1
2
2
28
258
516 613
44 270 556
42 415 934
3 339 885
66 744 214
101 528 193
1.6
18.3
8.9
0.7
6.1
0.11
0.002
0.001
0.50
0.0001
8
1
2
2
23
186
690 764
457 111
882 002
33 557
2 363 376
12 277 293
1.3
4.3
4.2
0.16
1.6
0.25
0.05
0.03
0.85
0.057
dens. Although we cannot completely rule out the possibility that maternal effects influenced our results, this
seems unlikely. We found no significant difference in
seed mass based on region of origin, nor was there a
significant relationship between latitude of origin and
seed mass within or among regions (J. L. Maron, unpublished). Moreover, plants were measured after at
least a year in the field, a time period sufficient for any
initial maternal effect to diminish.
For natives, genetically based clinal variation in size
and fecundity is not surprising. St. John’s wort occurs
across a large latitudinal range in Europe and latitudinal
or elevational clines are often found in species that
occur over steep environmental gradients (Turreson
1930, Clausen et al. 1940, Neuffer and Hurka 1986,
Galen et al. 1991, Winn and Gross 1993, Jonas and
Geber 1999). Clinal variation among introduced populations, however, is particularly noteworthy because
it may indicate that exotics are rapidly evolving adaptations to conditions in recipient communities. Indeed, the study of clinal variation in adaptive traits has
been a classic approach to understanding how organisms adapt to their environment (Clausen et al. 1940,
Endler 1977). Although other studies have shown that
exotic plant populations can be genetically differentiated with respect to particular traits (Jain and Martins
1979, Potvin 1986, Warwick 1990, Rice and Mack
1991, Linde et al. 2001), we know of no other study
that has documented both broad-scale differentiation
in adaptive traits among exotic populations based on
latitude, and strong convergence between introduced
and native plant populations in geographic clines for
fitness.
For introduced plants, several alternative mechanisms could produce clines in traits such as those we
have observed. Clines could evolve as a result of adaptive radiation from a limited number of genotypes that
were introduced into North America. Alternatively,
multiple introductions could result in genetically diverse populations with sufficient variation on which
selection could act. In this instance, there could be
genetically based adaptation among the diverse genotypes that were originally introduced or selection could
simply filter out genotypes not already adapted to conditions in the recipient community. If filtering has taken
place, there is no adaptive evolution. Rather, surviving
plants are those that are already pre-adapted to the climatic conditions in recipient communities. Since these
mechanisms have different implications regarding the
importance and mode of adaptive evolution, distinguishing among them is essential if we are to fully
understand the role of rapid evolution in the invasion
process.
Our genetic data suggest that there have been multiple introductions of St. John’s wort into North America. Plants sorted into several well-supported clades
(Fig. 1), which would not be the case if there had been
a massive genetic bottleneck caused by only a few
founding individuals. Thus, unlike many exotic plants
that show little genetic differentiation across geographic gradients (Baker 1974, Morgan and Marshall 1978,
Barrett and Richardson 1986, Warwick and Black 1986,
Rapson and Wilson 1988, Wang et al. 1995, Williams
et al. 1995), we found substantial molecular genetic
variation among introduced St. John’s wort. Most of
this variation was partitioned among populations; only
10% of the total variation in AFLP haplotypes was due
to region of population origin (i.e., introduced vs. native). This is consistent with what has been found for
other apomictic or highly selfing plants, where substantial genetic variation is often preserved among genetically differentiated populations (Widén et al. 1994,
Wang et al. 1995, Bergelson et al. 1998, Miyashita et
al. 1999, Auge et al. 2001).
Not only were introduced plants genetically diverse,
but they were phenotypically variable as well. Introduced populations expressed as much, or in some cases
more phenotypic variation in size and fecundity within
any given common garden than did individuals from
native populations, despite the fact that introduced populations spanned a narrower latitudinal range than did
the natives.
Given that there have been multiple introductions of
St. John’s wort, are clines among introduced populations the result of adaptive evolution or entirely the
result of plants having been introduced into areas that
are climatologically similar from whence they came?
Several lines of evidence suggest that St. John’s wort
did not universally establish at latitudes similar to their
European site of origin. We found multiple cases in
EXOTIC PLANT ADAPTATION
May 2004
TABLE 3.
273
Extended.
SP
WA (cumulative across first two years)
WA (cumulative across three years)
df
SS
F
P
df
SS
F
P
df
SS
F
P
1
2
2
39
250
1 383 719
2 048 447
531 811
15 933 275
37 226 630
3.1
2.4
0.57
2.7
0.08
0.10
0.57
0.0001
9
1
2
2
44
406
98 751 567
15 716 958
15 673 251
10 034 411
89 652 986
319 442 031
13.8
7.6
3.8
2.4
2.6
0.0001
0.008
0.03
0.1
0.0001
9
1
2
1
44
404
216 864 022
21 745 730
36 039 543
19 934 584
232 111 881
749 315 733
12.8
4.1
3.4
1.8
2.8
0.0001
0.05
0.04
0.17
0.0001
FIG. 2. (A, B) Mean size (number of shoots) produced by 14-month-old H. perforatum plants in the Sweden common
garden, and (C, D) mean size (volume) of 28-month-old plants in the Washington common garden (open circles, central
North American populations; filled circles, western North American populations; triangles, European populations). Lines
through points indicate significant effect of latitude. Arrows indicate the latitudes of the common gardens.
274
JOHN L. MARON ET AL.
Ecological Monographs
Vol. 74, No. 2
FIG. 3. (A, B) Mean size (volume) of 14-month-old H. perforatum plants in the California common garden, and (C, D)
mean size (volume) of 12-month-old plants in the Spain common garden (open circles, central North American populations;
filled circles, western North American populations; triangles, European populations). Lines through points indicate significant
effect of latitude. Arrows indicate the latitudes of the common gardens. Note that one point from central North America is
totally obscured by a western North American data point.
which particular introduced genotypes share as their
closest native relative individuals originating from different latitudes than themselves (Fig. 1). For example,
individuals from California populations 1 and 2, from
latitudes 38.558 and 38.668 N, respectively, have as
their closest European relative plants from France population 7, which originate from latitude 44.18 N. Plants
from California populations 3 and 4 (latitudes 398 and
39.258 N, respectively) are most closely related to
plants from Germany population 15, which were from
latitude 50.738 N. Furthermore, some clades contain
plants from both western and central North American
populations, implying that plants from one portion of
North America were founded by plants from another
latitudinally distinct portion of North America, or that
European genotypes were simultaneously introduced
into very different recipient locales.
Patterns of leaf size variation among native and introduced plants also support the notion that plants introduced into particular latitudes did not necessarily
originate from similar latitudes. For natives, leaf size
is diagnostic for whether plants reside in northern or
southern Europe. In native communities, plants from
northern Europe have wider leaves than plants from
May 2004
EXOTIC PLANT ADAPTATION
275
FIG. 4. (A, B) Mean number of seed capsules produced by 17-month-old H. perforatum plants in the Sweden common
garden, and (C) mean cumulative number of seed capsules produced across their first and second years by plants in the
Washington common garden (open circles, central North American populations; filled circles, western North American
populations; triangles, European populations). (D, E) Mean number of seed capsules produced by 31-month-old plants in the
Washington common garden. Lines through points indicate significant effect of latitude. Arrows indicate the latitudes of the
common gardens.
the south, and in fact, northern and southern European
plants are treated as different varieties (var. perforatum
in the north and var. angustifolia and var. microphyllum
in the south; Robson 1968). In contrast to these clear
differences in leaf size among European plants (both
in natural populations and in our common gardens),
western North American plants did not exhibit clinal
variation in leaf size in common gardens. Because this
Ecological Monographs
Vol. 74, No. 2
JOHN L. MARON ET AL.
276
FIG. 5. (A, B) Mean number of seed capsules produced by 17-month-old H. perforatum plants in the California common
garden, and (C, D) mean cumulative number of seed capsules produced across two years by plants in the Spain common
garden (open circles, central North American populations; filled circles, western North American populations; triangles,
European populations). Lines through points indicate significant effect of latitude. Arrows indicate the latitudes of the common
gardens.
TABLE 4. Results from ANCOVA testing for the effect of block, latitude of population origin,
region of population origin, latitude 3 region interaction, and population nested within region
on leaf area in Washington (WA), and California (CA).
WA
CA
Source
df
SS
F
P
df
SS
F
P
Block
Latitude
Region
Latitude 3 region
Population(region)
Error
8
1
2
2
44
363
1.6
5.5
1.9
6.1
57.3
89.5
0.79
4.1
0.73
2.37
5.28
0.61
0.05
0.49
0.10
0.001
8
1
2
2
28
255
2.2
3.8
3.8
1.62
23.7
44.8
1.3
4.4
2.3
0.96
4.26
0.25
0.04
0.12
0.39
0.0001
EXOTIC PLANT ADAPTATION
May 2004
277
FIG. 6. (A, B) Mean leaf area of H. perforatum plants in the Washington common garden, and (C, D) mean leaf area of
plants in the California common garden (open circles, central North American populations; solid circles, western North
American populations; triangles, European populations). Lines through points indicate significant effect of latitude. Arrows
indicate the latitudes of the common gardens.
TABLE 5. Percentage of total phenotypic variation in size
or fecundity partitioned among European and western
North American (N.A.) populations in common gardens in
California (CA), Sweden (SW), and Washington (WA).
Population
CA
SW
WA
Size
Native
Western N.A.
51.5
48.5
52.8
47.2
39.3
60.7
Fecundity
Native
Western N.A.
53.5
46.5
29.6
70.4
40.6
59.4
trait appears not to have yet responded to conditions
in the introduced range, leaf size may be a reasonable
proxy for the latitude that western North American
plants originated from in Europe. Since some largeleaved populations were found at southern latitudes in
western N.A., it appears that southern latitude populations in western N.A. likely originated from more
northern latitudes in Europe.
Taken together, genetic and common garden data
suggest the following scenario. Multiple introductions
of St. John’s wort into North America provided sufficient phenotypic (and underlying genetic) variation on
JOHN L. MARON ET AL.
278
which selection could act. Some introduced genotypes
undoubtedly originated from regions that shared a similar abiotic regime as that experienced in their recipient
community, and therefore were pre-adapted to particular conditions experienced in North America. However, given the patterns discussed above, it also seems
likely that many populations were founded by individuals that were not pre-adapted to the latitude (and hence
climatic conditions) of introduction. Plants within these
populations appear to be evolving in response to current conditions experienced in their recipient community. Since the earliest arriving genotypes of St.
John’s wort have only been in North America for ;150
years (and likely less time in California), or perhaps
12–15 plant generations, this evolutionary adaptation
is occurring quite rapidly.
Concluding remarks
Exotic plant introductions represent a grand, if unfortunate, experiment in evolutionary ecology. This
was first recognized over 35 years ago by evolutionary
biologists who were among the first to explore the evolutionary potential of introduced plants (Baker and
Stebbins 1965, Baker 1974). However, this evolutionary perspective has mostly been ignored in the burgeoning ecological literature on invasion biology
(Parker et al. 2003).
Our results generally support the contention that introduced plants can undergo contemporary evolution
(Bone and Farres 2001), and that adaptive evolution
may be one of several key mechanisms enabling exotics
to succeed in recipient communities. Hopefully, increasing awareness of the importance of contemporary
evolution in the ecology of invasions will catalyze a
greater fusion of ecological and evolutionary perspectives in future studies of exotic plants (Thompson 1998,
Bone and Farres 2001, Lee 2002). Melding of these
often disparate approaches offers tremendous potential
to crack the mystery of why exotic species are able to
attain such staggeringly high densities in recipient
communities, while their native counterparts virtually
never do.
ACKNOWLEDGMENTS
This work benefited from early discussions with Richard
Root and Doug Schemske. We thank D. Ewing and the rest
of the staff in the Botany greenhouse at the University of
Washington for their help in propagating plants. T. Bradshaw
graciously allowed us to work in his laboratory, and B. Frewen, J. Pijoan, and D. Grosenbacher ably performed AFLP
analyses. Paul Spruell helped with analyzing molecular data.
Thanks to B. Clifton, D. Grosenbacher, J. Jones, T. Hirsch,
T. Huettner, J. Pijoan, and M. Wolven for helping establish
and maintain the Washington common garden and to K. Parker for allowing the use of her land in Washington for our
common garden. The Napa Land Trust permitted us to establish our garden on their property in California, and L.
Amsberry, J. Calizo, and S. Harrison helped with logistics
and/or fieldwork in establishing this common garden. In
Spain, we thank P. Matas from the Universitat de Barcelona
greenhouse for assistance in propagating plants and J. Serra
Ecological Monographs
Vol. 74, No. 2
and the staff in Mas Badia (IRTA), as well as I. Gimeno, L.
Marco, and F. Debicki for their assistance maintaining the
common garden in Spain. In Sweden, we thank the Folkesson
family for kindly allowing us to establish our experiment on
their land and for the use of their machinery. S. Lagergren,
A. Bommarco, and S. Öberg provided help in the field. The
manuscript was improved by comments from L. Amsberry,
J. Brodie, E. Crone, J. Robertson, and J. Williams. We are
tremendously grateful to A. Angert, D. Ayers, J. Combs, U.
Gamper, S. Gardner, D. Greiling, F. Grevstad, J. Hess, R.
Keller, P. Kittelson, E. Knapp, E. Ogheri, P. Pysek, A. Sears,
R. Sobhian, A. Stanley, J. Taft, E. Weber, A. Weis, and A.
Wolf for collecting H. perforatum seeds for us. This work
was supported by grants to J. L. Maron from the University
of Washington Royalty Research Fund and from NSF grant
DEB-0296175 and to M. Vilà by a grant from DURSI (Generalitat de Catalunya).
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APPENDIX
A table of the locations of seed source populations is available at ESA’s Electronic Data Archive: Ecological Archives
M074-005-A1.