Zoological Journal of the Linnean Society, 2016, 176, 632–647. With 11 figures.
Patterns of morphological diversification of mainland
Anolis lizards from northwestern South America
RAFAEL A. MORENO-ARIAS* and MARTHA L. CALDERÓN-ESPINOSA
Grupo de Biodiversidad y Sistemática Molecular, Instituto de Ciencias Naturales, Universidad
Nacional de Colombia, Ciudad Universitaria, Bogotá D.C. 11001, Colombia
Received 11 February 2015; revised 30 June 2015; accepted for publication 9 July 2015
Anolis lizards are one of the most diverse vertebrate genera and are the classic example of adaptive radiation
and convergent evolution. Anoles exhibit great morphological diversity produced by the ecological opportunity to
exploit several arboreal niches. Anole radiation in the Caribbean islands is well studied, but the mainland radiation is less understood. We used a large morphological data set and a molecular phylogeny to describe the morphological diversification of anoles from northwestern South America, a region with the highest anole diversity
on a mainland. We describe morphological diversity as summarized by ten morphotypes, defined mainly by body
size, limb proportions, and subdigital lamellae. We show that some morphotypes are limited to forested lowlands
and others to Andean highlands; by contrast, Anolis assemblages from tropical rainforests are comprised of the
same four morphotypes. We demonstrate that morphological diversification followed a pattern of adaptive radiation across a landscape of adaptive peaks. Our results are consistent with the most recent hypothesis of convergence stated for Caribbean radiation, and demonstrate convergence between mainland morphotypes and Caribbean
ecomorphs, which suggests that common processes are driving both radiations.
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016
doi: 10.1111/zoj.12325
ADDITIONAL KEYWORDS: adaptive peaks – adaptive radiation – Colombia – convergent evolution –
morphology.
INTRODUCTION
Lizards of the genus Anolis comprise one of the most
diverse clades of vertebrates, with 390 described species
(Uetz & Hošek, 2014). The geographical range of anoles
includes the northern half of South America through
Central America and into tropical Mexico and the southeastern USA, including every Caribbean island and some
islands of the Pacific Ocean; anoles have also been introduced to southeastern Pacific islands (Losos, 2009).
The Anolis clade is more phenotypically diverse than
related clades and represents a classic example of adaptive radiation (Losos & Miles, 2002). Anolis radiated
extensively in the Caribbean islands as well as in mainland Central and South America. The Caribbean island
radiations have been widely studied and the adaptive basis of this diversification is well understood (Losos,
*Corresponding author. E-mail: [email protected]
632
2009). In Cuba, Hispaniola, Puerto Rico, and Jamaica,
anole lizards diversified into a set of species adapted
morphologically to particular microhabitats, with these
microhabitat specialists known as ecomorphs (Williams,
1972).
Six ecomorphs are recognized and are named according their microhabitat use: crown-giant, grassbush, trunk, trunk-crown, trunk-ground, and twig (Rand
& Williams, 1969; Williams, 1983). The Caribbean anole
radiation is also significant because it shows independent evolution of these ecomorphs – each ecomorph
has evolved at least twice independently on each of
the Greater Antilles, indicating convergent adaptation amongst islands (Williams, 1983; Losos et al., 1998;
Mahler et al., 2013). In addition, the mechanistic basis
of the relationship between morphology and ecology
is well supported by ecomorphological and functional
studies (Losos, 1990a, b, c; Losos & Irschick, 1996).
Adaptive radiation in Anolis also occurred on the mainland, with more species distributed in Central and South
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DIVERSIFICATION OF SOUTH
America than in the Caribbean. However, mainland
anoles exhibit different patterns of radiation compared with those seen in the Caribbean, possibly because
of differences in food resources, competitors, predators, and selective pressures (Irschick et al., 1997; Losos,
2009; Schaad & Poe, 2010). In general, mainland anoles
occupy a different morphospace than Caribbean anoles,
although most Caribbean ecomorphs (e.g. crowngiant, grass-bush, trunk-crow, trunk-ground, twig) are
represented by a few mainland species (Irschick et al.,
1997; Velasco & Herrel, 2007; Pinto et al., 2008; Schaad
& Poe, 2010); however, in these cases, mainland species
differ in their ecology from Caribbean ones (Irschick
et al., 1997; Schaad & Poe, 2010). Additionally, some
clades of mainland anoles have greater diversification
rates than those in the Caribbean (Pinto et al., 2008).
Therefore, the differences between mainland and Caribbean anoles suggest the possibility that other ecomorphs
could occur on the mainland (Schaad & Poe, 2010).
Colombia has the greatest diversity of Anolis, with
76 species (71 mainland restricted) of the 120 registered to northwestern South America – Brazil, Colombia, Ecuador, Perú, and Venezuela (Uetz & Hošek, 2014).
Therefore, we used anoles distributed in mainland Colombia as a model with which to analyse the morphological diversity of the mainland radiation in
northwestern South America. We combined a large morphological data set of Colombian Anolis, multivariate
analyses, and phylogenetic comparative methods with
the following aims: (1) to characterize the morphological diversity, (2) to identify morphotypes and describe their geographical distribution and natural history
features, (3) to test patterns of morphological evolution of Anolis from northwestern South America, and
(4) to compare morphological similarity between mainland and Caribbean species.
MATERIAL AND METHODS
MORPHOLOGICAL DATA
To describe the morphological diversity we measured
778 male lizards of 59 species of Colombian mainland anoles (N = 1–77 specimens/species), representing 83.1% of Colombian mainland species and 52.2%
of northwestern South American mainland species (Supporting Information Table S1). These consisted of 717
specimens from the Reptile Collection of Instituto de
Ciencias Naturales (ICN-R), Universidad Nacional de
Colombia, and 61 specimens measured in the field and
subsequently released. We only measured adult male
lizards because they exhibit the greatest morphological variation in anoles (Losos, 2009). We sexed individuals by the presence of a hemipenis, dewlap, or
enlarged postanal scales, depending upon which characters occur in that species. For each individual we
633
recorded the snout–vent length (SVL), tail length only
for specimens with no regenerated or broken tails (TLL),
foreleg length (FLL), hindleg length (HLL), trunk length
(LTR), head width (HW), head height (HH), and head
length (HL) in mm. We used digital callipers with an
accuracy of ±0.01 mm. We also counted the number
of subdigital lamellae under the third and fourth phalanges of the fourth toe (LN).
MORPHOLOGICAL
DATA ANALYSES
We calculated the mean value of each morphological
trait per species. We log-transformed all data and corrected for the body size effect through regression analyses of SVL against each trait. The variables employed
in subsequent statistical analyses corresponded to SVL
and the residuals of each trait against SVL.
To identify species with similar morphology, we performed a polythetic hierarchical divisive clustering method
in an ordination space (Legendre & Legendre, 1998).
This method is based on a principal components analysis, followed by a division of objects (species) into groups
(morphotypes) according to whether their value for the
first principal component was positive or negative. The
same procedure was applied subsequently to each new
group (Williams, 1976) until we obtained groups with
at least two species with the same value for the first
component. We evaluated the groups identified by previous analysis using a discriminant function analysis
(DFA). We used the first significant functions to assess
morphological differences amongst species and to classify them into morphotypes. Morphotypes were defined
as the species group that showed the same sign in their
punctuations to each significant function.
Finally, we performed a second DFA to corroborate
the morphotypes from the first DFA. The structure matrix
from a DFA shows the most relevant variables for each
function each function, so we used the matrix obtained
in the last DFA to describe the morphotypes. We performed analyses of covariance with morphotypes as treatments and SVL as the covariate to find differences
between morphotypes for each trait individually. It is
important to mention that some species were poorly
represented in our sample and so could be classified in
other groups when more data are acquired.
GEOGRAPHICAL
DISTRIBUTION AND NATURAL HISTORY
OF MORPHOTYPES
To describe the distribution of morphotypes, we quantified the occurrence of each morphotype in
ecogeographical regions (Fig. 1). These regions were
defined by two criteria (1) geographical trans-Andean
regions (below 1000 m a.s.l. for western and eastern
slopes of Central and Western Andes Cordillera and
western slope of Eastern Andes Cordillera), cis-
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 632–647
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
Figure 1. Distribution of species richness and morphotype (MT) diversity across 13 ecogeographical regions, altitude
range, and main regions based on life zones and predominant vegetation types for 59 Anolis species of Colombia. Bar
size for each colour indicates number of species. ARF, Cis-Andean tropical rain forests in the Amazonas; CA, central
Andes; CP, Caribbean Plains; EA, eastern Andes; LCV, Lower Cauca River Valley; LS, Cis-Andean savannahs in Los
Llanos; MBC, Middle Biogeographical Chocó; MMV, Middle Magdalena River Valley; NBC, Northern Biogeographical
Chocó; SBC, Southern Biogeographical Chocó; SNSM, Sierra Nevada de Santa Marta; UMV, Upper Magdalena River
Valley; WA, western Andes.
Andean regions (below 1000 m a.s.l. for eastern slopes
of Eastern Andes Cordillera to Orinoco Llanos and
Amazonas), and Andean regions (above 1000 m a.s.l.
in the Andes system and Sierra Nevada de Santa
Marta); (2) predominant life zone and vegetation types
of Colombia (Rangel, 1997, 2004). This second criterion divides the country into tropical rain forest, tropical dry forest, cloud forests, Andean forest, scrubland,
savannah, and Paramo.
Integrating both criteria we identified 13 geographical regions for this study: trans-Andean tropical rain
forests in Northern Biogeographical Chocó (NBC),
Middle Biogeographical Chocó (MBC), Southern Biogeographical Chocó (SBC), Lower Cauca River Valley
(LCV), Middle Magdalena River Valley (MMV), TransAndean dry forests in Upper Magdalena River Valley
(UMV), and Caribbean Plains (CP). We grouped Andean
cloud forests (altitude range > 1000 < 2300 m a.s.l.),
Andean forests and scrublands (Altitude range > 2300–
3000 m a.s.l.), and Paramo vegetation of each mountain range into western (WA), central (CA), and eastern
Andes (EA), and Sierra Nevada de Santa Marta
(SNSM). Cis-Andean savannahs in Los Llanos (LS),
and Cis-Andean tropical rain forests in the Amazonas
(ARF) were regions in eastern Andes (Fig. 1).
The occurrence of species across ecogeographical
regions was defined by collection and literature data.
We corroborated identifications of all specimens and
their collection locality, and complemented locality data
with reports of Colombian inventories of reptiles (Lamar,
1987; Bernal-Carlo, 1991; Hernández-Ruz et al., 2001;
Castaño-Mora et al., 2004; Carvajal-Cogollo &
Urbina-Cardona, 2008; Moreno-Arias, Medina-Rangel
& Castaño-Mora, 2008; Moreno-Arias et al., 2009;
Medina-Rangel, 2011). In order to describe differences in species composition between ecogeographical
regions we calculated Whittaker’s diversity beta index
(Whittaker, 1972). Microhabitat and vegetation strata
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 632–647
DIVERSIFICATION OF SOUTH
were obtained from natural history literature for each
species (Table S1).
PHYLOGENETIC
COMPARATIVE ANALYSIS
We used the same traits as in the DFA above (SVL
and residuals of traits vs. SVL) but in this case residuals were calculated using phylogenetic size correction (Revell, 2009) with the phyl.resid function of
the phytools R package (Revell, 2012). We built a phylogeny of 28 species based on DNA sequences from
GenBank (Table S2), utilizing sequences fragments from
mitochondrial regions of nicotinamide adenine
dinucleotide dehydrogenase subunit II (ND2, 1038 bp),
five transfer-RNA (tRNATrp, tRNAAla, tRNAAsn,
tRNACys, tRNATyr, 398 bp), and a small fragment of
cytochrome c oxidase subunit I (COI, 30 bp). As consequence our inferences are about a gene tree instead
of a species tree; however, several studies show that
mitochondrial trees not only reconstruct nearly the
phylogenetic history of anoles as trees builded with
several data types (nuclear sequences and morphology) but also are adequate to make inferences about
the evolution of other biological attributes (i.e. Castañeda
& de Queiroz, 2011; Nicholson et al. 2012; Gamble et al.,
2013). We aligned sequences using default values of
gap costs from CLUSTAL X v. 2 (Larkin et al., 2007),
and tRNAs were aligned based on secondary structure information from Kumazawa & Nishida (1993).
We used three data sets: a data set without partitions, a data set partitioned by gene (three partitions: ND2, tRNA, and COI), and a data set partitioned
by codon position for ND2 and gene identity for the
other two fragments (three partitions: ND2 by codon,
tRNA, and COI). We selected the model of evolution
for each partition with Akaike’s information criterion
(AIC) using JModeltest 2 (Darriba et al., 2012), and
performed phylogenetic analysis with MrBayes 3.2
(Ronquist et al., 2012). We verified convergence visually with TRACER v. 1.5 (Rambaut & Drummond, 2007)
and evaluated each partition strategy with Bayes factors
(BF). This method compares two models (two partition strategies) by their ratios of marginal likelihood
(BF), then, if BF values larger than 10 indicate strong
support of a model over other. Conditions for these
analyses were as follows: four independent runs with
four Markov chains per run, 30 000 000 generations
with a random starting tree, a temperature of 0.15,
and trees sampled every 1000 generations.
For all phylogenetic comparative analyses we used
the strict consensus tree (Fig. 4) which was ultrametric
transformed with the function chronos from the ape
R package (Paradis, Claude & Strimmer, 2004). To
explore if related species are more similar morphologically than expected by chance (phylogenetic signal:
Blomberg & Garland, 2002), we calculated and tested
Blomberg et al.’s K statistic (Blomberg, Garland & Ives,
635
2003) for each continuous trait, using the function
phylosig from the phytools R package (Revell, 2012).
K statistic tests phylogenetic signal as the ratio of the
mean of squared error from the data measured and
the proposed phylogeny vs. the mean of squared error
of data randomly permuted across the tips of the tree.
Blomberg et al.’s K values fluctuate from zero when
phylogenetic independence exists in data, to one or more
than one when data are distributed as expected under
Brownian motion. As the significant values of
phylogenetic signal also can be result from different
evolutionary processes and rates (Revell, Harmon &
Collar, 2008), we explored some evolutionary models
that could explain the morphological diversification patterns in Colombian mainland anoles. We calculated the
evolutionary scenarios with the surface R package and
tested them with ΔAICc – Akaikes’s information criterion, c: corrected to small sample size (Burnham &
Anderson, 2004); the AICc values were obtained using
the approach suggested by Ingram & Mahler (2013).
We tested the following models:
1. Brownian Motion (BM; Felsenstein, 1973), which
indicates that the distribution of data follows a
pattern related to the shared ancestry of species.
In this case phenotypes change through time but
the most closely related species are phenotypically more similar to each other than they are to
others because of their shared history.
2. Early Burst (EB; Harmon et al., 2010) is a timedependent model that exponentially transforms evolutionary rates under the model R(t) = R(0) * exp(a*t),
where R is the evolutionary rate, a is the rate change
parameter, and t is time. We transformed the tree
with a value of a = −3. This model tests if trait evolution has slowed over time from the root to the
tips, by transforming the topology as if the evolutionary rate near the root is faster than near the
tips of the tree. This model suggests that major
changes in traits occur early in history and the phenotypic similarity between closest species is lower
than expected by BM, which is a pattern that corresponds to adaptive radiations.
3. Ornstein–Uhlenbeck (OU) Process. Stabilizing selection under evolution model based on the OU
Process (Table S2), which exemplifies trait evolution towards an unique adaptive peak, where trait
X changes according to two factors through time
(t): a deterministic – selection force (selection force),
and a stochastic (random drift), according to the
formula dX(t) = α[θ − X(t)]dt − σdB(t) where α is the
selection force, θ is the adaptive optimum, and dB
is white noise. White noise indicates independent
and normally distributed random variables, and σ
is the intensity of the random fluctuations in the
evolutionary process (Butler & King, 2004).
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
4. Surface Regimes (SURF; Table S2). This is a method
to test convergent phenotypic evolution based on
OU under the adaptive landscape framework. The
method, known as surface (Ingram & Mahler, 2013),
adds regimes of phenotypic shifts step by step and
calculates their respective likelihoods after comparing all calculated regimes according to their AIC
values to choose the best regime shifts of phenotypic shifts (forward phase). Surface searches which
regimes can be collapsed, again with maximum likelihood, and step by step calculates convergent regimes
a posteriori. Finally, surface finds the best convergent regime of phenotypic shifts by comparing the
AIC values of the calculated convergent regimes
(backward phase).
5. Morphotype Regimes (MORPH fwd). We assigned
a corresponding morphotype to each species and the
most probable morphotype to each node. To do this
we estimated an ancestral reconstruction of
morphotype states with a maximum likelihood approach. To test morphotype regimes we used the ace
function from the ape R package (Paradis et al.,
2004). We tested the MORPH fwd performance model
with the startingModel function of the surface R
package (Ingram & Mahler, 2013). This model tested
if morphological evolution followed stabilizing selection under ten adaptive peaks.
6. Morphotype Regimes Collapsed (MORPH bwd). We
collapsed all MORPH fwd regimes with the
surfaceBackward function of the surface R package
(Ingram & Mahler, 2013). This model tested if the
morphological evolution occurred toward less of the
morphotypes defined by MORPHfwd.
COMPARISONS
BETWEEN MAINLAND MORPHOTYPES
AND
CARIBBEAN
ECOMORPHS
To compare anole species morphologically, we used SVL
and size-corrected values of TLL, FLL, HLL, and LN.
Morphological data for Caribbean anoles were taken
from Losos (1990a) and Losos (1992). To detect morphological differences between mainland morphotypes
and Caribbean ecomorphs, we used two approaches.
First, we conducted a DFA without phylogenetic correction with our 59 species and 27 Caribbean anoles
(which represented six Caribbean ecomorphs), using
morphotype as a grouping variable to classify Caribbean species into the mainland morphotypes. Then, we
analysed the data with a phylogenetic correction. To
do this, we calculated a phylogenetic size correction
with the phyl.resid function (Revell, 2009) using the
topology of Gamble et al. (2013), which we pruned and
kept the species for which morphological data were
available (54 species). Finally, we carried out a
surfaceBackward analysis for these data and this topology to find convergent regimes in 54 species classified according to their morphotype or ecomorph.
RESULTS
MORPHOLOGICAL
DIVERSITY
We obtained 21 species groups using polythetic hierarchical divisive clustering that were collapsed by the
DFA into ten groups that represent ten morphotypes
(Fig. 2). The most diverse morphotypes were morphotype
1 (MT1) and MT3, with eight species each, and the
least diverse were MT7 and MT9 with four and three
species, respectively. The remaining morphotypes contained between five and seven species.
DFA allowed the differentiation of morphotypes based
on four significant discriminant functions (DF1
ΛWilks = 0.001, P < 0.01; DF2 ΛWilks = 0.08, P < 0.01;
DF3 ΛWilks = 0.069, P < 0.01; DF4 ΛWilks = 0.220,
P < 0.01). The first three DFs accounted for 92.1% of
the morphological variation of morphotypes and were
correlated with SVL, relative hindleg length, and relative number of lamellae, respectively (Fig. 2). The fourth
function accounted for 4.4% of variation and was correlated with tail length.
Morphotypes differed in SVL (F = 45.35, P < 0.05).
Small-sized anole species belonged to MT1 to 5 and
generally had a mean SVL of < 60 mm. Large-sized anole
species belonged to MT6, 7, and 8, and had a mean
SVL of between 60 and 90 mm. Giant anole species
belonged to MT9 and 10 with a mean SVL of > 90 mm
(Table 1). We found that tail length was also different amongst morphotypes (F = 3.88, P = 0.01). Most
species had tails between 1.5 and two times their SVL.
Short-tailed anoles belonged to MT4 and generally had
a tail less than 1.5 times their SVL. Long-tailed anoles
belonged to MT1, 6, 8, 9, and 10, and exhibited a tail
twice as long as their SVL (Table S1).
Morphotypes also showed differences in their relative foreleg length (F = 10.59 P < 0.01). Most Colombian mainland anoles had forelegs of between 35 and
40% of their SVL in length. Short foreleg anoles belonged to MT4 and generally exhibited forelegs of less
than 35% of their SVL in length. Anoles with long
forelegs belonged to MT2, 3, 5, 6, and 10, and possessed forelimbs of more than 40% of their SVL in
length (Table 1). Relative hindleg length differed amongst
morphotypes (F = 26.39, P < 0.01). Most Colombian mainland anoles had legs between 60 and 80% of their
SVL in length. Short-hindleg anoles belonged to MT4,
and had hindlegs that were less than 50% of their
SVL in length. Long-hindleg anoles belonged to MT2,
5, 6, and 10, and had hindlegs that were more than
80% of their SVL in length (Table S1). Morphotypes
also differed in relative lamellae number (F = 9.37,
P < 0.01). Small species with few lamellae belonged
to MT1, 2, and 5, and possessed fewer than 18 lamellae.
Large or giant anoles with few lamellae (< 22) belonged to MT6, 8, and 9 (Table S1). We did not find
any significant differences amongst morphotypes in
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DIVERSIFICATION OF SOUTH
637
Figure 2. Discriminant functions describing ten anole morphotypes (MTs) based on 59 species of Colombian Anolis. Blue:
MT1, green: MT2; black: MT3, purple: MT4; yellow: MT5; red: MT6; cyan: MT7; grey: MT8, orange: MT9, white: MT10.
Table 1. Comparisons of Anolis beta diversity amongst ecogeographical regions
NBC
MBC
SBC
LCV
MMV
ARF
UMV
CP
LS
WA
CA
EA
MBC
SBC
LCV
MMV
ARF
UMV
CP
LS
WA
CA
EA
SNSM
0.26
0.47
0.25
0.42
0.60
0.76
0.53
0.75
0.83
0.18
0.94
1.00
1.00
0.89
0.88
0.77
0.90
1.00
0.54
0.50
0.85
0.59
0.74
0.83
0.25
0.20
0.88
0.45
0.92
1.00
1.00
0.85
0.83
0.38
0.75
0.82
1.00
0.92
0.92
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
0.50
1.00
1.00
1.00
1.00
1.00
1.00
0.85
1.00
1.00
0.89
0.73
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
Values > 0.6 are in bold.ARF, Cis-Andean tropical rain forests in the Amazonas; CA, central Andes; CP, Caribbean Plains;
EA, eastern Andes; LCV, Lower Cauca River Valley; LS, Cis-Andean savannahs in Los Llanos; MBC, Middle Biogeographical Chocó; MMV, Middle Magdalena River Valley; NBC, Northern Biogeographical Chocó; SBC, Southern Biogeographical Chocó; SNSM, Sierra Nevada de Santa Marta; UMV, Upper Magdalena River Valley; WA, western Andes.
trunk length relative to SVL (F = 1.59, P = 0.143) or
head dimensions relative to SVL (width: F = 0.66,
P = 0.74; height: F = 1.07, P = 0.41; length: F = 0.658,
P = 0.74).
GEOGRAPHICAL
DISTRIBUTION AND NATURAL HISTORY
OF MORPHOTYPES
We found seven morphotypes shared between the lowlands and Andean regions, two morphotypes (MT2 and
5) that were unique to the lowlands, and one (MT4)
that was exclusive to montane regions (Fig. 1). When
comparing lowland regions, only MT7 was exclusive
to cis-Andean tropical rain forests. MT10 was only observed in trans-Andean rain forests and cloud forests
of WA; the trans-Andean dry forests did not have any
unique morphotypes, whereas MT9 was shared by CP
and Chocó forests. In montane ecogeographical regions,
the Andean and cloud forests of WA, CA, and EA shared
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
four morphotypes; the unique morphotype in the
Paramos was MT4, and LS and SNSM were the regions
with least morphotype diversity (Fig. 1). TransAndean rain forests contained species that represent
90% of morphotypes and the highest species diversity. Cis-Andean rain forest contained only 50% of
morphotypes, represented by nine species (Fig. 1). Dry
regions like CP and LS possessed 60% of morphotypes.
In Andean regions, WA possessed the highest diversity of species whereas EA had the highest morphotype
diversity (70%) (Fig. 1).
Mean beta diversity values amongst ecogeographical
regions was high (0.85), with areas very similar in
species composition (0.18) to fully dissimilar (1.0).
Lowland regions with the lowest values (< 0.4) of beta
diversity were NBC-MBC, MBC-SBC, LCV-CP-MMV,
and LS-ARF. However, amongst those four groups, mean
beta diversity was high (> 0.60). Montane regions were
highly dissimilar, with beta diversity values above 0.70
(Table 1).
Anoles living at the lowest stratum, which use ground
and herbaceous strata mostly in leaf litter and bushes,
belonged to MT2; species of MT5 also used the ground
but reached the upper understorey stratum and used
mostly trunk microhabitats (Table S1). Species of
morphotypes that used mostly understorey stratum were
from MT1, 4, and 6; these preferred bushes, and some
species used grasses or trunks. Species of both MT3
and 8 inhabit strata from the understory to the canopy,
but species of MT3 use trunks whereas anoles of MT8
prefer bushes. Anoles living in the upper levels of the
habitat belong to MT7 and 10, and use trunks to reach
the canopy stratum (Table S1). Anoles of MT9 do not
share strata and microhabitat use between them; for
example, Anolis fraseri and Anoles mirus inhabit bushes
in the understorey, but A. fraseri can reach the canopy
and also uses trunks. By contrast, Anolis onca is more
terrestrial and prefers ground and herbaceous strata;
however, it has been observed on trunks of small trees
and wooden structures of human buildings (M. L.
Calderón-Espinosa, pers. observ.; Table S1).
MORPHOTYPE
EVOLUTION
In the phylogenetic analysis we found that the data
set without partitions (– natural logarithm of Likelihood lnL 21201.6) was preferred over the other data
sets (gen partition –lnL 21207.1 and codon partition
–lnL 21399.4). The Bayes factor of the codon partition vs. no partition data sets was –395.5, and that
for the gen partition vs. no partition data sets was
–11.03, indicating support for the data set without partitions. The inferred topology (Fig. 3) was fully resolved and showed two main clades with high support,
representing the Dactyloa and Norops clades; the main
groups within Dactyloa correspond to the Phenacosaurus,
Western, and latifrons clades sensu Castañeda & de
Queiroz (2011).
Phylogenetic signal was detected for most traits (SVL
K = 1.05 P = 0.001, TLL K = 0.97 P = 0.001, FLL K = 1.13
P = 0.001, HLL K = 1.22 P = 0.001, TRL K = 0.75
P = 0.038, LN K = 1.01 P = 0.001). Only three traits
showed no phylogenetic signal (HW K = 0.72 P = 0.085,
HH K = 0.48 P = 0.780, HL K = 0.43 P = 0.911).
Evolution of morphological diversity in mainland
anoles seems to have followed four convergent regimes
across ten shifts, as suggested by the most strongly
supported model MORPHbwd. Two of the four regimes
matched with MT4 and 8 and remain regimes are associated with the main clades Norops and Dactyloa
(Fig. 4). The other multipeak scenarios (SURF and
MORPHfwd) had no support (Fig. 4). Other scenarios
also had no support and did not describe the morphological diversification of Anolis of northwestern South
America: OU (lnL = 1139, Δ AICc = 94.2), BM (lnL = 1132,
Δ AICc = 62.4), and EB (lnL = 1111.4, Δ AICc = 125).
COMPARISON
BETWEEN MAINLAND MORPHOTYPES AND
CARIBBEAN
ECOMORPHS
Four first DFs based on data without phylogenetic correction accounted for 96% of the morphological variation (DF1: ΛWilks = 0.002 P < 0.01; DF2: ΛWilks = 0.02
P < 0.01; DF3: ΛWilks = 0.1 P < 0.01; DF4:
ΛWilks = 0.220 P < 0.01). The first and second DFs correlated with SVL and relative hindleg length, respectively (Fig. 5). The grass-bush species were classified
into MT1 and 5. The trunk-crown species were classified into MT7 and 3. The trunk-ground species classified into MT5 and 3. Trunk anole species classified
into MT3. The twig anole and crown-giant anole species
were classified into MT4 and 10, respectively. Analysis of data with surface identified six regimes, collapsing MT10 with crown-giant, twig species with MT4,
trunk-ground with MT5, trunk-crown species with MT7,
and MT8 species in MT6. In addition, MT1, 2, 3, grassbush, and trunk species were combined into a single
regime (Fig. 5).
DISCUSSION
Mainland anoles represent almost 60% of Anolis species
(Losos, 2009) and our evaluated species represent nearly
30% of the mainland radiation. Nonetheless, our results
essentially represent the full range of phenotypic diversity across the main geographical regions of northwestern South America. The main morphological
patterns of anoles identified here are not expected to
change, although those species for which little data
are available might be classified into other morphotypes
when more data are acquired. In general, the morphological diversity of Colombian mainland anoles can
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DIVERSIFICATION OF SOUTH
639
Figure 3. Consensus Bayesian tree for 28 species of mainland Colombian Anolis, their main clades, and their geographical distribution. Values at nodes indicate posterior probability (PP); black circles at nodes indicate PP = 1.0. Coloured
ovals at tips identify morphotypes (MTs) as follows: blue: MT1, green: MT2; black: MT3, purple: MT4; yellow: MT5; red:
MT6; cyan: MT7; grey: MT8, orange: MT9, white: MT10. Filled bars indicate geographical distribution: montane (white),
cis-Andean (grey), trans-Andean (black), and wide distribution (red).
be summarized into ten morphotypes defined mainly
by their body size and secondarily by their body shape,
defined here as proportions of limbs, tail, and lamellae
number (as a proxy of the toe length) to SVL.
The pattern of morphological variation found here
resembles the Anolis assemblage from the Middle Biogeographical Chocó (Velasco & Herrel, 2007) and the
West Indies anoles (Losos, 1992), where morphological variation is explained primarily by body size and
secondarily by body shape. This finding is not surprising given that these traits are important for struc-
turing anole communities (Schoener, 1968; Williams,
1972; Roughgarden, 1974).
Differences in body size and shape promote coexistence because morphology determines greatly the manner
in which species use the resources within a habitat
(Garland & Losos, 1994). In this way, body size relates
to food type and perch height whereas limb proportion relates to perch type and foraging behaviour (Losos,
1990b, c, 1992). In addition, all of these traits together not only restrict the performance of species to the
use of specific structural habitats, but also restrict
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
Figure 4. Morphotype Regime (MORPHfwd), Morphoype Regime Collapsed (MORPHbwd) and Surface Regime (SURF)
hypothesis performance of morphological regime shifts for 28 species of Anolis of northwestern South America. Colours
indicate morphotypes (MTs) as follows: blue: MT1, green: MT2; black: MT3, purple: MT4; yellow: MT5; red: MT6; cyan:
MT7; grey: MT8, orange: MT9, light grey: MT10.
interspecific relationships with other anole species. Our
results reinforce the idea that morphological variation is a relevant factor in structuring anole communities in northwestern South America.
The morphological diversity of Anolis from mainland Colombia seems to be higher than in the West
Indies anoles when only the six typical ecomorphs described for the islands are considered. However, many
other species considered as unique ecomorphs, such as
false chameleons, terrestrial, semiaquatic, rock-wall
dwelling and cave ecomorphs, occur throughout the West
Indies (Losos, 2009). Recently, Mahler et al. (2013) found
15 adaptive peaks (morphotypes) occurring in the West
Indies, including unique ecomorphs. Direct comparison between our findings and Mahler et al.’s (2013) study
is not possible owing to differences in the morphological and phylogenetic data. Our findings are based on
28–54 species and four to nine traits, whereas Mahler
et al. (2013) used a phylogeny of 100 species and 11
traits; however, then we identified higher morphological diversity with less morphological and phylogenetic
data.
It is possible that we are underestimating the real
morphological variation of the anole mainland radiation, to include only 59 species. However if we combine
our data (small phylogeny with nine traits and large
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 632–647
Figure 5. Morphological comparison between species of northwestern South America and the Caribbean. In the DFA, the triangles are Caribbean ecomorphs.
Colours indicate morphotypes (MTs) as follows: blue: MT1, green: MT2; black: MT3, purple: MT4; yellow: MT5; red: MT6; cyan: MT7; grey: MT8, orange: MT9,
light grey: MT10. Ecomorphs are labelled as CG, crown-giant; GB, grass-bush; TC, trunk-crown; TG, trunk-ground; TR, trunk-ground; and TW, twig Caribbean
ecomorphs. Blue colour (A) in backward chronograph includes MT1, MT2, MT3, GB, and TR.
DIVERSIFICATION OF SOUTH
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 632–647
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
phylogeny with five traits) some interesting issues
emerge: first, we identified a multipeak adaptive model
as the most probable scenario to explain the morphological variation in mainland Anolis; second, our analyses supported the convergent nature of the morphological
diversity of Anolis of northwestern South America; and
third, some morphotypes match the Caribbean
ecomorphs and there are at least two morphological
regimes unique to the mainland.
MORPHOLOGICAL
ANOLIS
SOUTH AMERICA
COMPOSITION OF
ASSEMBLAGES OF NORTHWESTERN
The morphological composition of the Anolis mainland assemblages showed an interesting pattern of
shared morphotypes amongst sites with similar vegetation types and altitudes despite the sites having different species compositions, as reflected in the high
beta diversity values. Morphological Anolis assemblages can be grouped according to elevation and vegetation as follows: anoles of lowland forest, montane
forest, grassland and savannah, and Paramos. Lowland
forests include dry forests with under 1800 mm of precipitation and deciduous vegetation in the dry season,
and rain forests with precipitation above 1800 mm and
evergreen vegetation. Despite climatic differences
between these lowland forests, both types offer multiple vegetation strata that are favourable to Anolis, such
as canopy, understorey, herbaceous layer, and leaf litter.
As anoles are mostly arboreal lizards and given what
we know about their adaptive evolution, we expect these
environments to support high species and morphotype
diversity, but not all do so. For example, Anolis assemblages from the dry forests of the upper Magdalena
River show low species diversity. Despite differences
in species diversity amongst localities, each anole assemblage of lowland trans- or cis-Andean forests was
composed of a minimum of four morphotypes: MT1,
2, 3, and 5, each one associated with one of the main
forest strata.
Some peculiarities in morphotype composition of forest
lowland assemblages emerge. In localities from SBC
forest inhabits Anolis fasciatus, a species of MT6 that
is mostly montane. The occurrence of montane
morphotypes in lowland forests, especially in the Chocó
forest, could be explained by the lower limit of montane
forests on the western slope of the Andes than on the
central and eastern slopes. Alternatively, Amazonian
assemblages also include a unique morphotype (MT7)
composed of species of the Dactyloa Eastern Clade with
cis-Andean distributions, whose origin is probably Amazonian (Castañeda & de Queiroz, 2011).
The next group with high morphological diversity
corresponds to montane forest assemblages and some
studies of Colombian montane anoles indicate that at
least three species are observed per locality
(Hernández-Ruz et al., 2001; Caicedo et al., 2006;
Molina-Zuluaga & Gutiérrez-Cárdenas, 2007;
Moreno-Arias et al., 2009). Cloud and Andean forests
offer the same vegetal strata as lowland forests; species
in these environments correspond to arboreal anoles
and include morphotypes of canopy (MT4 and 10), understory anoles (MT3 and 6), and understorey and herbaceous anoles (MT1). However, unlike lowland forests,
species of morphotypes that use leaf litter are not found
in cloud and Andean forests.
Paramos only occur above 3200 m a.s.l. and these
are environments dominated by tall grasses in the herbaceous stratum and by Espeletia spp. and Ericaceae
in the shrub stratum. Only anole species of MT4 are
found in these mountain-top environments.
Savannah environments are grasslands with scarce
forest vegetation, which includes only riparian forest,
palm forests, and matas de monte (isolated arboreal
formations inside savannahs). Despite the sparse vegetation, this environment also includes all strata mentioned previously, yet only understorey species like MT1
and leaf-litter species of MT5 are observed in these
environments. Savannah is probably the extreme
lowland environment for anoles because precipitation is very high in the rainy season and very low in
the dry season, thus maintaining hydric stress throughout the year. In addition, forest vegetation is a limiting resource that is only available in narrow riparian
forest and small and isolated matas de monte.
In the highlands, Paramos are extreme environments, not only because of the altitude, which is a constraint for reptiles, but also because of the extreme
temperature change across the day, and because
Paramos also suffer hydric stress, especially during the
dry season. Drastic reductions in numbers of Anolis
species and morphological diversity are associated with
increases in elevation.
Recent evidence has shown that environmental filters,
such as elevation and climate, are strong determinants of the structure of local Anolis ecomorph communities because they affect environmental niches that
functionally restrict some ecomorphs, and hence produce
a patchy distribution of sets of coexisting ecomorphs
(Wollenberg, Veith & Lötters, 2014). In general terms,
this pattern can be used to describe differences in the
lowland and highland anole morphotype compositions across northwestern South America. An idea to
be tested is whether or not species of MT2 and 5 exhibit
low thermoregulation performance in highlands compared with lowlands. This could explain the absence
of forest terrestrial anoles in montane forests given
that the lowest strata in montane forests are less warm
owing to the altitude and the constant presence of
clouds.
As we mentioned above, because highland environments are climatically extreme, we would expect that
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DIVERSIFICATION OF SOUTH
species display adaptations to these challenging conditions; indeed, some highland species have larger body
scales and perform better under hydric stress than
lowland anoles. In addition, differences in the vegetation structure in highlands compared with lowlands
may relate to the absence of canopy anoles. However,
it is interesting that it is highland-specific anoles (MT4)
that exhibit the most extreme morphology, shortest
arms and legs, of all the anole morphotypes. They
preferentially use twigs and very narrow surfaces
and exhibit very slow movements (owing to their very
shorts limbs). Therefore, environmental filters could
be explain these features, and we hypothesize that
predator interactions (biotic filters) could play a more
relevant role, and that very slow movements are probably the best strategy to avoid predators that respond
to fast movements, such as birds. These ideas are
reinforced when taking into account that virtually all
highland diurnal predators are birds, and that arboreal diurnal snakes (other typical predators of anoles
in lowlands) are only represented by Chironius
monticola.
ECOLOGY
OF
ANOLIS ASSEMBLAGES OF
SOUTH AMERICA
NORTHWESTERN
Several studies have revealed relationships amongst
morphology, ecology, and behaviour (Miles & Ricklefs,
1984; Pianka, 1986). In Anolis, some morphological attributes translate into performance capability, and these
capabilities constrain the ecology of anoles (Losos,
1990a). Anole lizards are an example of ecomorphological
relationships. Williams (1972) coined ecomorph as a
term to define groups of anole species with similar morphology and habitat use but without close phylogenetic
relationships. Later, Losos (1990a, c) demonstrated quantitatively the links amongst morphological, ecological, and behavioural traits in Greater Antilles anoles.
Owing to the evolution of subdigital lamellae, anoles
are mostly arboreal but several species also show diverse
microhabitat uses, and are semiarboreal, terrestrial,
or semiaquatic (Losos, 2009). Colombian anoles are not
an exception and also use a wide variety of
microhabitats; six morphotypes are arboreal, and the
remaining four are semi-arboreal. Semiaquatic species
also occur but they cannot be classified into a particular morphotype.
Although the ecology of many mainland anole species
is unknown, the matches between morphotypes and
ecomorphs found here permit us to infer some associations between our morphological groups and their
predominant habitat use.
Giant species of MT10 and some of MT7 use mostly
tree trunks in the upper strata and canopy. Anolis
frenatus and Anolis punctatus seem ecologically similar
to the crown-giant ecomorph from the Greater Antil-
643
les (Irschick et al., 1997), but A. punctatus is not enough
large to be a giant anole and it also matches with the
trunk-crown ecomorph. The absence of MT10 in
Amazonas can be explained because giant anole evolution was constrained by the presence of larger canopy
lizards, such as Plica plica and Uracentron flaviceps,
which are large lizards that use trunks of large trees
(Vitt, Zani & Avila-Pires, 1997; R. A. Moreno-Arias pers.
observ. 2014). These lizards may have restricted the
evolution of anoles towards giant forms owing to niche
incumbency or a priority effect.
In addition, several species of MT8 use shrubs or
tree trunks and branches in the canopy and understorey
strata, but species of MT6 are more common in the
understorey to herbaceous strata. These two
morphotypes apparently do not have a Caribbean
ecomorph counterpart, although Anolis biporcatus and
Anolis chocorum are recognized as crown-giants
(Castro-Herrera, 1988; Losos, 2009).
Small anoles of MT3 live in the lowlands, and use
mostly tree trunks from the understorey to the canopy
(Table S1). Whereas Anolis anchicayae, Anolis chloris,
Anolis ortonii and Anolis peraccae resemble the trunkcrown ecomorph, Anolis pentaprion was previously recognized as twig anole (Irschick et al., 1997; Losos, 2009).
For the latter two species, recent ecological data (R.
A. Moreno-Arias, unpubl. data) plus their lichenose
colour pattern indicate that these species resemble the
Caribbean trunk ecomorph more than the trunkcrown ecomorph.
Small and tiny anoles of MT4 are found from midmountain to Paramos regions, and use branches and
twigs from the understorey to the canopy (Table S1).
This group shows a greater similarity to a Caribbean
ecomorph than does any other group. In the same vein
as other studies (Schaad & Poe, 2010), our results also
identified MT4 species as twig anoles.
Species of MT1 use mostly trunks and branches of
small trees, shrubs, and herbs of the understorey or
herbaceous strata, but rarely use the ground (Table S1).
Only two species (Anolis auratus and Anolis
fuscoauratus) have been recognized by other authors
as grass-bush anoles (Irschick et al., 1997; Schaad &
Poe, 2010).
Species of MT2 inhabit the ground, leaf litter, and
log falls, and sometimes use shrubs and herbs (Table S1).
Schaad & Poe (2010) identified Anolis granuliceps as
a member of the grass-bush ecomorph despite it was
the species morphologically furthest from members of
the grass-bush group. Irschick et al. (1997) showed that
Anolis trachyderma is the morphological centroid of
the trunk-ground morphotype, but its nearest neighbour was a grass-bush species. Matching a Caribbean ecomorph for the MT2 species is complicated, and
requires more quantitative data of their ecology;
however, we suggest that species of MT2 correspond
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R. A. MORENO-ARIAS AND M. L. CALDERÓN-ESPINOSA
to a unique mainland ecomorph owing to their greater
preference for the ground compared with the other
morphotypes.
MT5 anoles use tree trunks, shrubs, and ground
in nearly the same proportions (Table S1). Anolis
scypheus grouped within the trunk-ground ecomorph
(Irschick et al., 1997), and the ecology of the remaining species suggests that they are also trunk-ground
anoles.
Large anoles of MT9, despite their shared morphological attributes, show disparate microhabitat uses.
Anolis fraseri uses tree trunks in the canopy like species
of MT10; A. mirus is similar to species of MT6 that
also use branches in the understorey, whereas A. onca
is a typical anole of xerophytic vegetation near beaches
that uses bushes, shrubs, and the ground, similar to
species of MT1. It is interesting that MT5 anoles possess
the most robust bodies and some authors have observed very aggressive behaviour in A. fraseri and
A. mirus (F. Castro-Herrera & S. Ayala, unpubl. data),
which leaves the relationship between body robustness and aggressive behaviour occurring in this clade
as an open hypothesis to test.
Semiaquatic anoles do not constitute a morphologically distinctive group on the basis of the characters
used here. Instead, three species (Anolis lynchi, Anolis
poecilopus, and Anolis rivalis) were assigned to MT5
and the other two species (Anolis macrolepis and Anolis
maculigula) to MT1 and MT8, respectively. All
semiaquatic species use vegetation of herbaceous and
understorey strata surrounding streams and pools, but
also use other microhabitats. Anolis macrolepis is also
found on the ground, whereas A. maculigula,
A. poecilopus, and A. rivalis use rocks and boulders in
streams and pools (Williams, 1984; Miyata, 1985; F.
Castro-Herrera & S. Ayala, unpubl. data).
Therefore, semiaquatic anoles support the idea that
the semiaquatic habit can be acquired through a variety
of body plans. Another possibility is that other traits
not evaluated here, such as tail shape (related to swimming performance), could be a link amongst species
exhibiting a semiaquatic ecology, as suggested by Leal,
Knox & Losos (2002). Studies on performance and morphology will give some clues to defining semiaquatic
anoles as an ecomorph type.
EVOLUTION
OF
ANOLIS
MORPHOLOGICAL DIVERSITY
OF NORTHWESTERN
SOUTH AMERICA
A phylogenetic signal was present in the data analysed here for six traits (SVL, TLL, FLL, HLL, TRL
and LN). Most morphological traits followed a
trajectory influenced by the phylogenetic history of
species. Nevertheless, Revell et al. (2008) showed that,
in addition to genetic drift, high values of phylogenetic
signal occur when evolution is not entirely neutral,
such as in stabilizing selection at a constantly weak
strength, highly fluctuating natural selection, or when
the evolutionary rate or changes in adaptive shifts
decrease through time. Evolution of morphological traits
in anoles shows different intensities of phylogenetic
signal; variables representing limbs and size features can have low or high Blomberg et al. K values,
but always with significant values for phylogenetic
signal (Pinto et al., 2008; Hertz et al., 2013). In addition, convergent and deterministic evolution of morphology and ecology, bounded by ecological limits, is
recognized as the main pattern of evolution of anole
Caribbean radiation (Losos et al., 1998; Mahler et al.,
2010, 2013).
This pattern was the most frequently observed in
our data, as most traits exhibited high phylogenetic
signal without fitting neutral models, suggesting a deterministic morphological pattern of evolution for mainland anoles in northwestern South America.
Other traits, like head dimensions, which showed
low Blomberg et al. K values, exhibited phylogenetic
correlation. Low values for HW could be a result of
punctuated divergent selection. Low values for HH
and HL could be explained by a strong stabilizing
selection or bounded phenotypic evolution under high
mutation rates, as some theoretical models suggest
for evolutionary processes that show low phylogenetic
signal (Revell et al., 2008). In relation to the tempo
of evolution of morphological traits, the neutral model
BM had high support compared with the variable rate
of evolution model EB, suggesting that phylogeny
best predicts the patterns and rates of evolution for
these particular traits; this supports the stabilizing
selection scenarios, which were more supported
than the BM or EB, for explaining morphological
evolution.
Although we cannot infer the magnitude of the fluctuation of selection across the phylogeny to make inferences of where the main changes occur, the links
between (1) constant rates of evolution based on very
poor support of EB (AICc = 57.6) compared with BM,
(2) strength of selection towards a particular phenotypic peak, and (3) high values of phylogenetic signal
in most traits, suggest that the main morphological
shifts are concentrated near the root of the tree. It is
likely that major morphological shifts in northwestern South America mainland anoles occurred early in
their history. Therefore, the species to fill the same
morphological peak increased their morphological covariance, with respect to species of other morphological peaks, more than expected by neutral evolution,
which explains the high values of phylogenetic signal
observed in most traits. Thus, the observed pattern
of morphological evolution of mainland anoles
from northwestern South America is similar to
the niche occupancy (Revell et al., 2008) and niche
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DIVERSIFICATION OF SOUTH
differentiation (Price, 1997) models, which describe evolution following an adaptive radiation (Schluter, 2000).
Both MORPHbwd and the comparison between the
mainland and Caribbean anole species supported convergent evolution of morphology in at least six
morphotypes. This finding is similar to the known convergence pattern of Caribbean anole radiation (Losos
et al., 1998; Mahler et al., 2010), which supports the
theory that mainland radiation probably followed a
similar pathway to the Caribbean radiation. Convergence between mainland and Caribbean anoles may
have been rejected previously because different studies
used different morphological variables (Velasco & Herrel,
2007; Pinto et al., 2008; Schaad & Poe, 2010) to those
used originally to define the ecomorphs, or because of
the absence of a phylogenetic framework (Irschick et al.,
1997). Unlike these previous studies, we performed a
comparison with the original variables used to define
the ecomorphs under a phylogenetic framework to demonstrate that convergence between the radiations occurs
in at least six of the 15 possible ecomorphs defined
by island communities (Mahler et al., 2013).
CONCLUSION
In summary, the morphological diversity of northwestern South America mainland Anolis can be grouped
into ten morphotypes defined by similar ecologically
relevant traits as found in the Caribbean radiation (size,
limb proportions, and subdigital lamellae). The distribution of these morphotypes reveals patterns of convergence in lowland and mid-mountain forests, with
a unique morphotype occurring in high-mountain forests
(MT4), suggesting that similar selective factors leaded
morphological diversification in lowland and midmountain forests while unique factors constrained morphological diversity in high mountains. Morphotypes
defined with similar traits as those that define Caribbean ecomorphs reflect some aspects of their natural
history, indicating a possible convergence in ecology
with Caribbean species; however, this hypothesis
remains to be tested as quantitative data on the habitat
use of mainland species are lacking. Our results add
information that tries to explain the ecomorphological
diversification of mainland anoles, but a true understanding requires the following questions to be answered: are the processes underlying morphological
evolution in Caribbean and mainland anoles the same?;
are the species with disparate ecology within MT9 linked
by similar behaviours?; do Anolis assemblages in tropical rainforests converge in ecology?; and what are the
most relevant ecological filters assembling morphotype
communities? The evidence presented here suggests
that the pattern of morphological evolution for traits
that are ecologically relevant in mainland anoles from
northwestern South America followed a deterministic
645
route across an adaptive landscape, with some adaptive peaks being convergent – a situation already demonstrated in their Caribbean counterparts. Therefore,
we hypothesize that the processes driving the adaptive radiations of mainland and Caribbean anoles have
been similar.
ACKNOWLEDGEMENTS
We thank our anonymous reviewers for their invaluable suggestions for the analyses of the data. We thank
Luke Mahler for resolving some questions about the
SURFACE package. We thank Kriistina Hurme for
the English editing. This project was developed under
the scholarship ‘Generación del Bicentenario 2010’
of the Departamento Administrativo de Ciencia,
Tecnología e Innovación of Colombia (COLCIENCIAS).
This paper represents part of the formal requirements for R. A. Moreno-Arias to obtain his PhD degree.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Table S1. Number of species and individuals, means of morphological trait values, microhabitat and vegetation stratum for ten morphotypes of Colombian mainland Anolis. Morphological trait abbreviations: SVL, snout–
vent length; TLL, tail length; FLL, foreleg length; HLL, hindleg length; LTR, trunk length; HW, head width;
HH, head height; HL, head length; LN, subdigital lamellae under third and fourth phalanges of fourth toe.
Microhabitat abbreviations: B, bushes; G, grass; Gr, ground; LL, leaf litter; T, trunk; S, semiaquatic. Stratum
abbreviations: G, ground; H, herbaceous; U, understory; C, canopy. SD in parentheses.
Table S2. GenBank accession numbers of sequences used to build the phylogeny of northwestern South American Anolis.
© 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 632–647