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ORIGINAL ARTICLE
doi:10.1111/j.1558-5646.2011.01238.x
ANCIENT COLONIZATION PREDICTS RECENT
NATURALIZATION IN ANOLIS LIZARDS
Steven Poe,1,2J. Tomasz Giermakowski,1Ian Latella,1Eric W. Schaad,1Erik P. Hulebak,1and Mason J. Ryan1
1Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque,
New Mexico 87131
2E-mail: anolis@unm.edu
Received February 25, 2009
Accepted January 7, 2011
The distributions and characteristics of naturalized species may be explained by novel anthropogenous aspects of world biogeogra-
phy such as the creation of favorable transport environments for propagules on ships. Conversely, the unprecedented connectivity
of humans may simply accelerate omnipresent ecological and evolutionary forces, for example, ships may allow species that are
generally good dispersers to disperse more quickly. As a null hypothesis, there may be no human component to species natu-
ralization. The first hypothesis predicts that naturalized species will possess unusual characteristics specific to interactions with
humans. The latter two hypotheses predict similarity between ancient colonizers and recently naturalized species. In this article,
we present a test of the latter hypotheses and show how they may be reconciled with the former. We show that species of Anolis
lizard that are ancient solitary colonizers share characteristics of size, shape, scalation, and phylogeny with naturalized species of
Anolis. Characteristics of ancient solitary colonizers predict naturalization approximately as well as characteristics of naturalized
species themselves. These results suggest the existence of a general colonizing type of Anolis, and that contemporary patterns of
naturalization are at least partially explained by abilities that are unrelated to interactions with humans.
KEY WORDS: Evolution, invasion, natural processes, nonnative, solitary species.
Invasive species are a global concern due to resulting economic
losses and extinction of indigenous wildlife. Much of invasion
biology focuses on identifying common characteristics of inva-
sions, including intrinsic (e.g., asexual reproduction) (Rejmanek
and Richardson 1996) and extrinsic (e.g., suitable habitat for inva-
sion) (Williamson 1996) factors, with two goals in mind (Rice and
Sax 2005). First, such information may be used to erect a predic-
tive framework of likely invasive species for conservation, health,
and economic purposes. Second, knowledge of the characteristics
of recent invaders may give insight into general ecological and
evolutionary processes.
In this article, we examine whether the reverse inference, of
evolutionary biology informing invasion biology, is also possi-
ble. We studied an ancient evolutionary colonization pattern, the
so-called “solitary” Anolis lizards, to gain insight into the char-
acteristics that determine recent naturalization success. We study
naturalization—the establishment of a population outside of its
native range, rather than invasion—the spread of a naturalized
species beyond its point of introduction (Richardson et al. 2000),
because naturalization is a necessary precursor to invasion and
invasion is more difficult to demonstrate than naturalization.
Anolis lizards are an ideal system for studying naturalization.
Nineteen of 374 (5%) Anolis species include naturalized popula-
tions. For example A. sagrei is native to Cuba but has established
populations in Belize, Grenada, Guam, Jamaica, Mexico, Taiwan,
and the United States (Lever 2003). Naturalized species of Anolis
share unusual characteristics of anatomy, environment, ecology,
and phylogeny (Latella et al. 2010).
Anolis is also a model system for studies of ancient evolu-
tionary colonization (Williams 1969; Nicholson et al. 2005), that
is, nonhuman-mediated naturalizations that occurred millions of
years ago. Solitary Anolis—species historically endemic to is-
lands lacking congeners (note that this definition excludes the
dozens of Anolis species that are sole inhabitants of some islands
1195
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2011 The Author(s). Evolution C
2011 The Society for the Study of Evolution.
Evolution 65-4: 1195–1202
STEVEN POE ET AL.
but historically sympatric with congeners in other parts of their
range)—are probably all overwater colonizers. Solitary species
inhabit either oceanic islands (e.g., A. agassizi), so are neces-
sarily colonizers, or landbridge islands and are phylogenetically
recent derivatives (e.g., A. desechensis [Rodriguez-Robles et al.
2007]), indicating recent colonization rather than vestigial vicari-
ant existence.
The 26 species of solitary Anolis share traits of size, sexual
dimorphism, limb length, head scalation, and toe scalation, and
the similarities among solitary species in each of these traits ex-
cept toe scalation evolved earlier than the transition to solitary
existence (Schoener 1969; Poe et al. 2007; Poe unpubl. data).
That is, these traits did not evolve as adaptive responses to soli-
tary existence, but rather evolved earlier and apparently facilitated
colonization as exaptations. This lack of postcolonization evolu-
tionary change in studied traits is what allows us to consider extant
solitary species as proxies for the ancient colonizing versions of
themselves—there is no reason to reconstruct ancestral states, be-
cause ancestral states will tend to be the same as current states in
solitary species for the traits we are studying.
Naturalized species have been viewed as models for evolu-
tionary colonization at least since Darwin (1859). However, the
appropriateness of naturalized species as models to test ancient
evolutionary processes has never been tested. If this supposition
holds true, then ancient colonizers (i.e., solitary species) and natu-
ralized species would be expected to share unusual characteristics
that facilitate colonization and/or establishment. We hypothesized
that solitary and naturalized species are especially similar to each
other and differ from other Anolis in the same ways. We test this
contention using randomized contingency tests. If solitary and nat-
uralized species are found to be nonrandomly similar according
to these tests, we should be able to construct a model that predicts
naturalization based on either solitary or naturalized species, and
both solitary and naturalized parameterizations should yield good
fit to the model. We construct such models using both phylo-
genetic logistic regression (Ives and Garland 2010) and logistic
regression incorporating a parameter for phylogenetic distance to
naturalized species (Jiang et al. 2010). Our goal is to test whether
it is possible to predict naturalization using information from an-
cient evolutionary colonizers.
Materials and Methods
DATA
We measured body length from snout to vent, head length from
anterior edge of ear to tip of snout, and femoral length from ven-
tral midline to knee of 242 species of Anolis (n=1–15 specimens
per species). We recorded maximum male and female snout to
vent length, median number of head scales across the snout be-
tween the second canthals, and median number of lamellae under
the fourth toe from personal observation of 242 species of Anolis,
Williams et al. (1995), and original species descriptions. Each of
these traits has been shown or suggested to reflect performance
differences in Anolis (Losos 2009). All variables were natural-log
transformed before analyses. Maximum snout to vent length was
used as a measure of body size (henceforth: SVL). Sexual size
dimorphism was measured as maximum female SVL divided by
maximum male SVL ( =SSD). Head length, femoral length, and
lamellae number were found to be strongly correlated with snout
to vent length and so regression residuals were used in analy-
ses. Mean head length and femoral length were regressed against
mean snout to vent length measured for the same specimens of
each species. Median lamellae number was regressed against SVL
for each species. Residuals for these regressions are henceforth
abbreviated as HL (head length), FL (femoral length), and LM
(lamellae). Naturalized status of species was determined based on
Lever (2003). Solitary status of species was based on Losos and
de Queiroz (1997) and Williams et al. (1995). Data are listed in
Table S1.
PHYLOGENETICS
We performed a parsimony analysis of data from Nicholson
et al. (2005; mitochondrial DNA, nuclear ITS DNA) and Poe
(2004; morphology) and unpublished morphological data (45 ad-
ditional species scored beyond Poe [2004]) for 252 species of
Anolis and eight outgroups using the parsimony ratchet (Nixon
1999) on PAUP (Swofford 2002). Data coverage varied from all
1267 parsimony-informative characters scored to 52 characters for
some species scored only for external morphology. This analysis
resulted in 1344 most parsimonious trees. Mixed-model Bayesian
methods were attempted but convergence to optimal trees was not
obtained in spite of multiple lengthy searches (up to three months
of computer time).
To obtain branch lengths to measure phylogenetic distances
between species, we performed a separate analysis of the mito-
chondrial dataset of Nicholson et al. (2005) using the topology
obtained in parsimony analyses of the entire dataset. We used the
AIC in Modeltest (Posada and Crandall 1998) to select a model
of evolution for likelihood analysis in PAUP. The model (GTR +
G+I) was applied in a likelihood analysis of a randomly selected
optimal topology with species that were not scored for mtDNA
excluded and branch lengths constrained to enforce a molecu-
lar clock. The resulting branch lengths were grafted onto this
topology of all 252 species using the BladJ program in Phylo-
com (Webb et al. 2007), which interpolates node times by evenly
spacing undated branchpoints between dated nodes.
We also obtained a tree from analysis of the mtDNA data
alone. We added a sequence from A. apletophallus to the dataset
of Nicholson et al. (2005) and performed a Bayesian phyloge-
netic analysis of 187 Anolis species and two outgroups using
1196 EVOLUTION APRIL 2011
ANCIENT COLONIZATION PREDICTS RECENT NATURALIZATION
MrBayes (Huelsenbeck and Ronquist 2001) under the following
parameter/Markov Chain Monte Carlo values: GTR +I+gamma,
two runs of four heated chains, heating temp =0.1 (a value ob-
tained by trial and error while attempting to reach the acceptance
rate of the Metropolis proposals recommended by the authors,
i.e., 10–70%), 10,00,000 generations, sampling every 500 gener-
ations, 1000 burnin trees. We confirmed postburnin convergence
between runs by comparing plots of likelihood values for stabil-
ity and examining the standard deviation of split frequencies. We
obtained clocklike branch lengths on the most probable tree using
penalized likelihood in r8s (Sanderson 2003).
SIMILARITY OF SOLITARY AND NATURALIZED
SPECIES
We tested whether solitary and naturalized species are signifi-
cantly similar and unrepresentative of Anolis in SVL, SSD, HL,
FL, HS, and LM using a contingency metric:
G=(xsol.i−xall.i)×(xnat.i−xall.i),(1)
where xrefers to mean for i=SVL, SSD, HL, FL, HS, or LM for
solitary (xsol), naturalized (xnat ), or all (xall)Anolis species. Gis
large and positive if solitary and naturalized species are similar to
each other and unrepresentative of Anolis and small or negative
if they are each representative of Anolis or differ from Anolis in
different ways. We compared the test statistics from solitary and
naturalized means to a null distribution of values calculated for
999 random samples of 26 (corresponding to solitary) and 19 (cor-
responding to naturalized) species selected without replacement
from the total pool of species.
We tested whether naturalized species tend to come from
the same clades as solitary species using Webb et al’s (2007)
COMDIST approaches. These methods test whether the mean
(COMDIST) or nearest neighbor (COMDISTNT) phylogenetic
distances between sets of species are significantly smaller (or
greater) than the distribution of such distances from randomly
selected sets of species.
NATURALIZATION MODELS
We wanted to test whether naturalization was predictable based on
a model that is independently parameterized to predict evolution-
ary colonization to a solitary environment. We performed logistic
regression analyses using naturalization as the dependent variable
and, in separate analyses, using solitary existence as the depen-
dent variable. If naturalization can be predicted based on species
traits, then models based on naturalized species are expected to
have maximal predictive ability for naturalization, as such models
are parameterized using those species that have actually become
naturalized. However if solitary characteristics are good predic-
tors of naturalization, then models predicting naturalization and
models predicting solitary existence should be correlated. That is,
they should both identify the same species as likely invaders.
We used two logistic regression approaches, stepwise elimi-
nation of parameters incorporating a parameter for phylogenetic
distance between taxa (Jiang et al. 2010) and phylogenetic logis-
tic regression (Ives and Garland 2010), which explicitly accounts
for shared phylogenetic history via a variance–covariance matrix.
For the former approach, we started with a model including all
independent variables (SVL, SSD, HL, FL, LM, HS; and PHY,
defined below) and reduced this model in a stepwise fashion by
sequentially removing the variable that had the least effect on the
likelihood of the model. Phylogenetic distance (PHY) was mea-
sured as the branch length connecting a species to its closest natu-
ralized relative. Our stopping rule was to obtain a model wherein
all remaining variables were significant at P<0.05. These anal-
yses produced models that predicted naturalization and solitary
existence. For the phylogenetic logistic regression (which cur-
rently does not allow stepwise procedures), we constructed mod-
els using the same parameters identified in the stepwise procedure
(excluding PHY), and also using all parameters that were found
to be individually significant under separate univariate phyloge-
netic logistic regression analyses. Our use of phylogenetic logis-
tic regression followed the implementation of Ives and Garland
(2010).
Results of a logistic regression analysis may be summarized
as continuous values from the linear model (i.e., a “naturalization
score”) or as discrete classifications of those values (i.e., predic-
tion of naturalized if model score is positive, or nonnaturalized
if negative). The absolute fit of the model is generally evaluated
with a Classification Table, which summarizes the percentage of
species that are correctly classified by the model. Interpretation
of logistic regression results for our analysis using naturalization
as the dependent variable is clear—results show the ability of the
model to predict naturalization and which parameters are the best
predictors of naturalization. But a comparison of these results to
the performance of solitary species as naturalization predictors is
not straightforward. To compare results from the analysis using
solitary existence as the dependent variable to the naturalization
results, we interpreted the values of the linear solitary model as
naturalization scores rather than solitary scores. Thus, a positive
model score was interpreted to indicate classification as natural-
ized rather than as solitary, and fit of the model was evaluated by
whether the scores for the solitary colonization model accurately
predicted naturalization rather than solitary existence.
We compared continuous scores of these models (natural-
ization, solitary) using a bivariate plot, the Spearman’s signed
ranks correlation test, and simple linear regression. A significant
result suggests that these models are describing similar phenom-
ena; that is, that ancient solitary colonization can predict recent
naturalization.
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STEVEN POE ET AL.
We compared logistic regression results predicting solitary
and naturalized species using five approaches: (1) All 242 species,
including all 19 naturalized and 26 solitary species, using the phy-
logenetic tree obtained with parsimony analysis and Phylocom
branch lengths and stepwise regression including PHY as a pa-
rameter; (2) 237 species, including only statistically independent
solitary (n=21) and naturalized (n=14) species (i.e., exclud-
ing the five species that are both solitary and naturalized), using
the parsimony tree with phylocom branch lengths and stepwise
regression using PHY as a parameter; (3) 187 species, including
only those species scored for mtDNA (20 solitary, 19 natural-
ized), using the Bayesian mtDNA tree and stepwise regression
including PHY as a parameter.; (4) all 242 species, using the
parsimony tree with phylocom branch lengths and phylogenetic
logistic regression using the parameters chosen in (1), excluding
PHY; (5) all 242 species, using the parsimony tree with phylocom
branch lengths and phylogenetic logistic regression under models
incorporating all parameters that are individually significant in
univariate phylogenetic logistic regression, excluding PHY.
Results
SIMILARITY OF SOLITARY AND NATURALIZED
SPECIES
Solitary and naturalized species of Anolis are significantly similar
and differ from other Anolis in SVL (P=0.001), SSD (P=0.001),
HL (P=0.024), HS (P=0.002), and LM (P=0.001) (Table 1).
Figure 1 shows phylogenetic clustering of solitary and naturalized
species (P=0.001).
Tab l e 1 . Means and standard deviations (in parentheses) of traits.
For each set of entries, first row shows raw values (measure-
ments in millimeters unless otherwise noted), second row shows
ln-transformed and/or size-corrected values used in analyses.
Solitary Naturalized
All Anolis Anolis Anolis
(n=242) (n=26) (n=19)
Body size 72.1 (32.5) 76.3 (19.2) 91.2 (32.8)
(SVL) 4.20 (0.38) 4.31 (0.25) 4.46 (0.31)
Sexual size 0.89 (0.12) 0.77 (0.11) 0.75 (0.11)
dimorphism −0.13 (0.14) −0.27 (0.14) −0.30 (0.15)
(SSD)
No. headscales 8.6 (3.0) 7.3 (1.6) 7.1 (1.5)
(HS) 2.10 (0.33) 2.00 (0.21) 1.94 (0.19)
No. lamellae 20.4 (5.6) 23.6 (4.0) 24.5 (4.4)
(LM) 0.00 (0.16) 0.11 (0.09) 0.07 (0.13)
Femoral length 17.5 (7.6) 19.0 (3.3) 20.4 (6.9)
(FL) 0.00 (0.14) 0.03 (0.07) 0.01 (0.07)
Head length 17.3 (8.2) 18.8 (3.6) 21.0 (7.8)
(HL) 0.00 (0.09) 0.02 (0.08) 0.03 (0.10)
Figure 1. Similarity of phylogenetic position for solitary and nat-
uralized species of Anolis. Dark branches show solitary (left) and
naturalized (right) species. Tree is one of the optimal trees from
phylogenetic analyses.
COLONIZATION MODEL
The final logistic regression model for the analysis of all 242
species using stepwise regression incorporating the PHY param-
eter, with naturalization as dependent variable, is:
N=−6.23 (SSD) −3.03 (PHY) −2.43.(2)
This model accurately classifies 92.2% of species. Model scores
for naturalized species (mean =−1.54) are significantly greater
than scores for nonnaturalized species (mean =−3.35; P<
0.0001, Mann–Whitney U test).
The final logistic regression model for the analysis of all 242
species, with solitary existence as dependent variable, is:
S=−4.07 (SSD) +5.77 (FL) +5.72 (LM) −4.01 (PHY) −1.65.
(3)
This model accurately classifies 89.8% of species as natu-
ralized or nonnaturalized. Model scores for naturalized species
1198 EVOLUTION APRIL 2011
ANCIENT COLONIZATION PREDICTS RECENT NATURALIZATION
Figure 2. Similarity of scores from models predicting natural-
ization under parameterizations using solitary and naturalized
species of Anolis. Inset graph shows a comparison of scores for
the 19 naturalized species.
(mean =−1.24) are significantly greater than scores for nonnat-
uralized species (mean =−3.39; P<0.0001, Mann–Whitney
Utest).
Scores for these two models are strongly correlated (Fig. 2;
P<0.0001, Spearmann’s signed ranks test). Solitary model score
explains 69% of the variance in naturalized model score (R2,sim-
ple regression). The correlation is strong among the 19 naturalized
species (Fig. 2, inset; R2=0.74).
Results using subsets of statistically independent taxa, phy-
logenetic logistic regression, and the mtDNA phylogenetic tree
are qualitatively identical to those shown here (Figs. S1–S4). In all
cases, naturalization and solitary models both significantly predict
naturalization and are strongly correlated with each other (P<
0.0001 for each comparison; Spearmann’s signed ranks test).
Discussion
Solitary anoles share several unusual characteristics with natural-
ized species (Table 1). These results reflect the close phylogenetic
relationship of solitary and naturalized species (Fig. 1) and sug-
gest the potential utility of these traits for demonstrating similarity
between these groups using the phylogenetically corrected mod-
eling procedures discussed below. See Latella et al. (2010) for a
discussion of how each of these traits may function in dispersal
and establishment of species.
Models based on solitary parameterization predict naturaliza-
tion approximately as well as models based on naturalized species
themselves (Fig. 2, Figs. S1–S4). The correlation of model scores
among naturalized species (Fig. 2, inset) is especially telling, as
it indicates that naturalization and solitary models consider the
same species to be typical (e.g., A. carolinensis) and surprising
(e.g., A. equestris) invaders. Both naturalized and solitary models
display good absolute predictability of naturalization as evidenced
by high classification percentages (Analysis 1: 89.8, 92.2), signif-
icantly greater model scores in naturalized versus nonnaturalized
species (P<0.0001 in each case), and significant variables in all
models.
The consistency of the modeling results across five analyses
including four combinations of taxa, two phylogenetic estimates,
and two statistical techniques (Fig. 2, Figs. S1–S4) suggests ro-
bustness of these results within this dataset. The full dataset in-
cludes five species that are both solitary and naturalized as well
as several naturalized and solitary species that share recent phy-
logenetic history with other naturalized or solitary species. Al-
though these issues invite obvious statistical complications, we
prefer results from the full dataset because we believe the poten-
tial statistical issues are outweighed by biological considerations.
Rather than being problematic, the existence of species that are
both solitary and naturalized actually supports the conclusions of
this article. Consider the hypothetical extreme case of statistical
nonindependence where all solitary species produced naturalized
populations and all naturalized species invaded from solitary lo-
calities. In such a case, the conclusion of this article of similarity
between solitary and naturalized species would be obvious and
the statistical analyses presented here would be superfluous. Re-
gardless, though, the analysis using only unshared species obtains
the same results as the full dataset (compare Fig. 2 and Fig. S1).
The different analyses included two logistic regression ap-
proaches, one explicitly correcting for phylogeny (Ives and
Garland 2010; Figs. S3 and S4) and one that incorporated phy-
logeny through an additional regression parameter (Jiang et al.
2010; Fig. 2, Figs. S1 and S2). We view the Jiang et al. (2010)
approach of allowing phylogeny to compete with other explana-
tory parameters roughly equally via the PHY parameter as a best
attempt at fulfilling the human goal of prediction of naturaliza-
tion. Conversely, we interpret the Ives and Garland (2010) phy-
logenetic correction as an attempt at biological explanation for
naturalization ability. Although we wish to point out that, unlike
typically analyzed traits in comparative biology (i.e., morpholog-
ical, ecological), all instances of species naturalization are in fact
nonhomologous—they occurred after each species had achieved
phylogenetic independence from sister species—and therefore
the phylogenetic correction is accounting for inertial tendency
rather than homologous similarity. Regardless of one’s preferred
interpretation, for our purposes of comparing prediction of natu-
ralization using solitary versus naturalized species, results using
the Jiang et al. (2010) and Ives and Garland (2010) approaches are
qualitatively identical (compare Fig. 2, Figs. S1, S2 to Figs. S3,
S4). That is, all analyses show a significant positive relationship
between naturalized and solitary parameterizations and thus that
naturalization can be predicted using solitary species.
EVOLUTION APRIL 2011 1199
STEVEN POE ET AL.
The similarities between solitary and naturalized species sug-
gest reciprocal insight. Recent invasions have long been consid-
ered a model for natural evolutionary colonization (Darwin 1859).
Our use of evolutionarily solitary species as a model system al-
lows the first test of this assumption. The shared characteristics
of solitary and naturalized species indicate that this assumption is
warranted, at least in this case.
The recent naturalization success of species with solitary
characteristics may be explained by these same characteristics be-
ing favored in solitary environments where successful and failed
colonization attempts are ubiquitous throughout evolutionary his-
tory. Islands with solitary species are environmentally homoge-
neous, not large enough to support multiple species, and geo-
graphically close to source islands so attempted invasions are
likely to be common (MacArthur and Wilson 1967; Rand 1969).
The solitary species that inhabit these islands probably possess
characteristics that favor competitive ability over congeners (to
repel attempted invaders or replace previous inhabitants), persis-
tence in a volatile (i.e., hurricane affected), homogeneous, spa-
tially limited environment, and initial colonizing ability into such
environments. These same characteristics contribute to modern
invasive success. Williams (1969) presents an early exposition of
this idea of a “colonizing type.”
The evolution of a colonizing type of Anolis is supported
by at least two contemporary patterns of naturalization. First,
among 41 instances of establishment for 19 naturalized species,
only one of these involves invasion from the mainland to an is-
land (Lever 2003). Most of the approximately 200 species of
mainland Anolis evolved in situ (Nicholson et al. 2005) within
multispecies communities (K¨
ohler 2003). Thus, mainland diver-
sification has been shaped by evolutionary forces of vicariance,
adaptation to complex environments, and community competi-
tion rather than of colonization and direct competition for limited
homogeneous space as in solitary species. The characteristics
of mainland species allow coexistence in multispecies commu-
nities but apparently are not conducive to naturalization. That is,
there are no colonizing types found among the vicariantly evolved
mainland communities.
Second, the two ecological types (“ecomorphs”; Williams
1983, Losos et al. 1998) that are predominant among both solitary
and naturalized species, trunk-crown and trunk-ground (Losos and
de Queiroz 1997), are also the most abundant types around hu-
man habitations where other types are nearly absent (Schwartz and
Henderson 1991; Lever 2003; a contingency test similar to equa-
tion (1) with ecomorph type as a dependent variable is significant
at P=0.001, n=107). As in other exotic species (Elton 1958),
naturalized Anolis are often most abundant, or even restricted to,
human-altered environments (Lever 2003). If disturbed environ-
ments are the only available habitats for invasion (due to, e.g.,
niche-packing [MacArthur and Levins 1967]), then those species
that are exapted for such environments will be the most success-
ful invaders (Lozon and Isaac 1997). Species with trunk-ground
and trunk-crown ecologies such as solitary and naturalized Anolis
appear to be so exapted. That is, trunk-ground and trunk-crown
species fit the colonizing type.
The similarities between historical colonizers and recent in-
vaders suggest that the success or failure of particular introduced
species may not be attributable to the peculiarities of humans
(Brown and Sax 2005). For example, the specialized morpholo-
gies of naturalized Anolis are unlikely to be due to these traits
being exaptations for stowage in ship or airplane cargo because
solitary species possess the same morphologies, and they became
established long before ships and planes existed. More likely is
the possibility that species that are especially good dispersers
anyway are fortuitously able to disperse more efficiently due to
the speed and scope of modern human travel. Similarly, human
habitations may be amenable to invasion because they imitate
ancient invadable environments, perhaps as areas that are unsuit-
able for specialized local species and/or lack competing species
due to eradication of natural habitat. Disturbed habitats thus may
allow only modern invaders that are similar to ancient invaders.
Colonizations may be proceeding more frequently now due to
the greater connectivity of humans, but the colonization ability of
particular species appears unrelated to human influence, at least
in the case of Anolis.
Conclusions
Recently naturalized species of Anolis lizard share unusual char-
acteristics with solitary species that colonized environments be-
fore human history. Logistic regression models based on solitary
species predict naturalization with similar effectiveness to those
based on naturalized species themselves (Fig. 2, Figs. S1–S4).
These results suggest that invasions occurring during modern hu-
man history are similar to ancient prehuman colonizations. There
is no need to invoke special interactions with humans to explain
which species will become naturalized, as the same colonizing
“type” of Anolis occurs anciently and in modern times.
Naturalized species have been considered model systems to
test general ecological and evolutionary principles at least since
Darwin (1859). The results presented here validate this assump-
tion in the case of characteristics that are correlated with colo-
nization, as naturalized species appear to be recent incarnations
of forms that have been successful colonizers over evolutionary
time. Future work is likely to forge additional links between an-
cient natural processes and recent phenomena we view as human-
mediated. Humans clearly are altering the global environment at
a rapid rate, sometimes with catastrophic consequences. But such
alterations may simply change the tempo, rather than the essence,
of omnipresent natural processes.
1200 EVOLUTION APRIL 2011
ANCIENT COLONIZATION PREDICTS RECENT NATURALIZATION
ACKNOWLEDGMENTS
We thank C. Webb for help with Phylocom, and A. Ives and T. Garland
for providing the PLogReg program. J. Brown and T. Lowrey reviewed
earlier versions of this manuscript and provided useful comments. This
research was funded by NSF grant DEB 0844624 to SP.
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Associate Editor: J. Vamosi
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Supporting Information
The following supporting information is available for this article:
Figure S1. Plot of prediction of naturalized model score by solitary model score using only statistically independent species, with
phylogenetic distances from parsimony tree with Phylocom branch lengths (i.e., analysis 2).
Figure S2. Plot of prediction of naturalized model score by solitary model score using only species scored for mtDNA, with
phylogenetic distances from Bayesian mtDNA analysis (i.e., analysis 3).
Figure S3. Plot of prediction of naturalized model score by solitary model score using all species and phylogenetic logistic
regression with models incorporating parameters determined to be significant in stepwise analysis (i.e., analysis 4).
Figure S4. Plot of prediction of naturalized model score by solitary model score using all species and phylogenetic logistic
regression with models incorporating all parameters that were individually significant (i.e., analysis 5).
Tabl e S 1 . Data.
Supporting Information may be found in the online version of this article.
Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting information supplied by the
authors. Any queries (other than missing material) should be directed to the corresponding author for the article.
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