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Biological Journal of the Linnean Society, 2012, 107, 210–218. With 2 figures
Colour-polymorphic snake species are older
LIGIA PIZZATTO1 and SYLVAIN DUBEY2*
1
School of Biological Sciences (A08), University of Sydney, Sydney, NSW 2006, Australia
Department of Ecology and Evolution, Biophore Building, University of Lausanne, 1015 Lausanne,
Switzerland
2
Received 3 March 2012; revised 2 April 2012; accepted for publication 2 April 2012
bij_1936
210..218
Many characteristics, for example life-history traits, physiological tolerance to heat and cold, and energy requirements, contribute to a population’s ability to persist in the face of climatic variation. Recent studies have suggested
that the presence of intraspecific colour polymorphism could be another potential contributor to population
resilience (e.g. to climate change) in ectothermic vertebrates such as reptiles. In the present study, we tested for
a relationship between the presence of intraspecific colour polymorphism and the age of snake species. Using
phylogenetic comparative methods, we demonstrate that the presence of intraspecific colour polymorphism is
correlated with the age of a species, with polymorphic snake species being significantly older than monomorphic
species. Understanding how species have dealt with past environmental modifications, such as climate change, can
provide important insights into how they are likely to respond in the future to continuing climate warming.
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218.
ADDITIONAL KEYWORDS: climate change – colour polymorphism – intraspecific diversification –
molecular dating – reptile.
INTRODUCTION
The coloration of an organism affects many facets of
its existence, including fitness-relevant functions
such as behaviour, thermoregulation, and metabolic
physiology, as well as predator–prey interactions
through mimicry, aposematism, and camouflage
(Rosenblum, Hoekstra & Nachman, 2004; Roulin,
2004; Protas & Patel, 2008; McKinnon & Pierotti,
2010; Rosenblum et al., 2010). Consequently, colour
polymorphism within a population and/or a species
(in addition to parameters such as life-history traits,
physiological tolerances, or energy requirements) may
expand the range of environmental conditions under
which at least some individuals are well suited to
meeting local abiotic and biotic challenges (e.g. Theurillat & Guisan, 2001; Dirnböck, Dullinger & Grabherr, 2003; Jiguet et al., 2007; Forcada, Trathan &
Murphy, 2008; Forsman & Aberg, 2008a; Huey &
Tewksbury, 2009; Kearney, Porter & Shine, 2009;
Caesar, Karlsson & Forsman, 2010; Dubey & Shine,
*Corresponding author. E-mail: [email protected]
210
2011a). In addition, intraspecific colour polymorphism
allows individuals to exploit different microhabitat
types (e.g. Shreeve, 1990; Edelaar, Siepielski &
Clobert, 2008), and allows different predator avoidance strategies (e.g. Proehl & Ostrowski, 2011). Thus,
polymorphic populations may be more likely to
successfully face present and future environmental
modifications, such as current global warming, and
modifications in, for example, predator pressure or
food accessibility. Finally, body colour is likely to
be especially significant for ectothermic animals,
because of their reliance upon ambient conditions
for thermoregulation (Clusella-Trullas, van Wyk &
Spotila, 2007). For example, dark ectothermic organisms warm up faster than pale individuals, and are
therefore able to boost their metabolism more rapidly
under low-temperature conditions (Clusella-Trullas
et al., 2007).
Previous studies in owls have suggested that
reddish individuals have a higher survival in warm–
wet years than in cold–dry years. Reddish coloration
(associated with pheomelanic pigments) may be
linked with an ability to deal with warm climatic
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218
COLOUR-POLYMORPHIC SPECIES ARE OLDER
conditions, whereas a non-reddish coloration may be
associated with greater success in colder climates (e.g.
Gehlbach, 1986; Galeotti & Cesaris, 1996; Galeotti
et al., 2003, 2009; Roulin, 2004; Roulin, Burri &
Antoniazza, 2011). Roulin et al. (2011) suggested that
climate change, which is currently more important at
high latitudes, may have dramatic consequences in
non-reddish species located near the poles, and that
colour-polymorphic species (including reddish and
non-reddish individuals) may be at an advantage
because the presence of reddish individuals would
lower the risk of extinction. Consequently, colourpolymorphic populations should be able to exploit
wider niches than monomorphic populations, which
may increase their resilience to extinction (Forsman
et al., 2008; Forsman & Aberg, 2008a; Roulin et al.,
2011).
Similarly, the evolution of intraspecific colour polymorphism may have allowed ectothermic species to
withstand past modifications of their environment,
such as Pleistocene glaciations (1.8–0.012 Ma), more
successfully than did otherwise similar monomorphic
taxa. Polymorphic species may thus be expected to be
older than monomorphic species because of the lower
probability of historic extinctions (Forsman et al.,
2008).
In the present study, we tested this hypothesis by
investigating the relationship between colour polymorphism (considering species with true withinpopulation polymorphism and species with variable
colour patterns) and the age of snake species (the age
of the oldest intraspecific diversification event, which
is the minimum length of time since existing populations within a species last shared a common ancestor), by assembling data from published molecular
phylogenies.
MATERIAL AND METHODS
AGE
OF SPECIES AND COLOUR POLYMORPHISM
We estimated the age of a species, as described in
Dubey & Shine (2011b, 2012) and Weir & Schluter
(2007), i.e. by using the oldest intraspecific diversification event (based on molecular dating) within each
species (see Table 1). This measure estimates the
minimum length of time since existing populations
within a species last shared a common ancestor. We
reviewed papers on phylogeny, polymorphism, and
geographic distribution of 72 species of snakes around
the world to test for a relationship between colour
polymorphism and the age of taxa. We excluded data
on known non-monophyletic taxa and, in order to
avoid inaccurate species age estimations, only data
from comprehensive phylogeographic and phylogenetic studies were included in the analyses.
211
Species were classified as being polymorphic (i.e.
exhibiting at least two different colour morphs) or
monomorphic based on field guides and previously
published studies (Forsman & Åberg, 2008b; see
Table 1). Sexually colour dimorphic species were considered as polymorphic only if polymorphism is
present within at least one sex, otherwise they were
considered as non-polymorphic, as in Forsman &
Aberg (2008a, b). In addition, there is no reason to
expect colour polymorphism to persist over evolutionary time, given that it is not always stable and hence
may be transient through time (Gray & McKinnon,
2007; Cameron & Pokryszko, 2008; Forsman & Aberg,
2008a, b; Lepetz et al., 2009). Consequently, a polymorphic population could become monomorphic
through the elimination of a morph, or it could
develop into geographic variations (Hedrick, 2006;
Forsman & Aberg, 2008a, b). Thus, no distinction was
made between species considered as exhibiting geographic variation in coloration or within-population
polymorphism (as in Forsman & Aberg, 2008a, b), and
both types were classified as variable colorations.
Similarly, morphs could have been extinct in past
events, rendering a species monomorphic in our classification. However, we are unable to recognize such
situations.
ANALYSES
From the initial 72 taxa, we had a complete data set
for 67 species. Thus, we reconstructed a phylogenetic
hypothesis for 67 snake species, from seven families
(22 Viperidae, 22 Colubridae, ten Elapidae, nine
Leptyphlopidae, one Typhlopidae, two Boidae, and
one Homalopsidae), using cytochrome b sequences
downloaded from GenBank and aligned by eye. For
maximum likelihood (ML), models of DNA substitution were selected using the Bayesian Information
Criterion (BIC; Schwarz, 1978) implemented in
JMODELTEST 0.1.1 (Guindon & Gascuel, 2003;
Posada, 2008). The model best fitting our data was
the GTR + I + G. We performed ML heuristic searches
using PHYML (Guindon & Gascuel, 2003). Sequences
of Varanus komodoensis and Lacerta viridis were
used to root the tree. Because no cytochrome b
sequences of Typhlops vermicularis were available in
GenBank, and as it was the only member of the
family included in our data set, and we wished to
retain it, we used the cytochrome b sequence of
another species (Typhlops platycephalus) to perform
the analyses.
All statistical tests were run using various R
routines (R Development Core Team, 2008). First,
we tested for phylogenetic signal in the age (logtransformed) of species using the Blomberg’s K statistic (Blomberg, Garland & Ives, 2003), calculated
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218
212
L. PIZZATTO and S. DUBEY
Table 1. Raw data on the age of species (log-transformed), based on oldest intraspecific diversification events, as revealed
by molecular phylogenies (with corresponding references), presence of colour polymorphism, and reproductive mode
(viviparous or not) of the species used in the present study
Species
Age
Polymorphism
Viviparity
References
Agkistrodon bilineatus
Agkistrodon contortrix
Agkistrodon piscivorus
Atropoides mexicanus
Atropoides nummifer
Atropoides olmec
Bitis arietans
Cerrophidion godmani
Charina bottae
Coluber constrictor
Contia tenuis
Coronella austriaca
Crotalus aquilus
Crotalus atrox
Crotalus cerastes
Crotalus lepidus
Crotalus mitchellii
Crotalus pusillus
Crotalus ruber
Crotalus tigris
Diadophis punctatus
Drysdalia coronoides
Drysdalia mastersii
Enhydris subtaeniata
Gloydius brevicaudus
Guinea bicolor
Hoplocephalus bungaroides
Hoplocephalus stephensii
Lampropeltis getula
Lampropeltis pyromelana
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Leptodeira nigrofasciata
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Naja pallida
Namibiana occidentalis
Natrix maura
Natrix natrix
Natrix tesselata
Nerodia erythrogaster
Nerodia fasciata
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Nerodia sipedon
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Pseudechis australis
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Thamnophis validus
Tricheilostoma macrolepis
Trimorphodon biscutatus
Typhlops vermicularis
Vipera ammodytes
Vipera aspis
Vipera berus
-0.2924
0.1399
0.3979
0.0309
0.3320
0.1490
0.6021
0.7562
0.9217
0.7782
0.7505
0.7033
0.2765
0.1335
0.1847
0.3927
0.5682
-0.0223
-0.6778
-0.7212
0.8382
0.0969
-0.1549
0.1461
0.3284
0.0580
-0.0706
-0.0706
0.6911
0.7482
0.5263
0.8129
0.3590
1.1492
0.5699
1.3636
1.2430
0.8692
0.6767
0.9877
0.2430
-0.2676
0.3365
0.0374
0.4502
0.8129
0.7243
0.7782
0.8261
-0.0506
0.2330
0.2695
0.4329
-0.1675
0.5911
0.6628
0.7959
0.6522
0.1399
-0.5452
0.5423
0.9823
0.7924
0.6128
0.5623
0.1461
Yes
Yes
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Yes
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Yes
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© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218
COLOUR-POLYMORPHIC SPECIES ARE OLDER
and analysed in the package ‘PICANTE’ (Kembel
et al., 2010). As this analysis presented a highly significant phylogenetic signal (k = 0.098, PIC variance
Z = -2.54, P = 0.001), we continued our analyses using
phylogenetic comparative methods. We explored the
relationships between presence/absence of colour
polymorphism and the age of the species [log(oldest
intraspecific diversification in millions of years)]
using a phylogenetic generalized least squares model,
which incorporates information about relatedness,
provided as a phylogenetic tree, into the error term of
a generalized least squares model (GLM), assuming a
particular model of trait evolution (see Martins &
Hansen, 1997). In our analyses, we assumed a Brownian model of evolution and the phylogenetic information was incorporated into the GLM (package ‘nmle’;
Pinheiro et al., 2009), using the package ‘APE’
(Paradis, Claude & Strimmer, 2004).
Because the age of a species can also be related to
its geographic distribution (Weir & Schluter, 2007;
Dubey & Shine, 2011b, 2012), we included the mean
latitude and range covered (difference in latitude
between the northern- and the southernmost known
population) of the species as covariates in the analyses. Similarly, the reproductive mode (egg laying
versus live bearing) and the mean snout–vent length
(SVL) of the adults were also considered as covariates, as variations are present in our data set and
could potentially have an impact on the ages of
species. Non-significant variables were removed one
by one from the models, and we selected the model
with the lowest AIC as the model with the best fit
(Crawley, 2007). The normality of the observed versus
fitted residuals, and homogeneity of the variances,
were examined through the visual inspection of plots
and the fitted correlation line.
RESULTS
The phylogeny of the snake species used to perform
the phylogenetic comparative analyses is shown in
Figure 1. The best-fit model contained only reproductive mode and presence/absence of polymorphism
(Akaike’s information criterion, AIC = 88.90, logLik = -40.45). None of the other variables had significant effects on the age of the species (all P > 0.13), and
generated models with AIC ranging from 98.4 to
120.1. The age of a species was marginally correlated
with reproductive mode (t = -1.87, P = 0.067, coefficient = -0.39) and was positively correlated with the
presence of polymorphism (t = 3.13, P = 0.0026, coefficient = 0.30): older species tended to be oviparous
(Fig. 2A), and were in general polymorphic (Fig. 2B).
Several young species, such as Thamnophis validus,
Nerodia taxispilota, Nerodia rhombifer, Crotalus
cerastes, Crotalus tigris, Crotalus ruber, Crotalus
213
atrox, Guinea bicolor, Leptotyphlops kafubi, and most
Naja species, are also monomorphic. However, other
young species (e.g. Nerodia fasciata, Hoplocephalus
stephensii, Drysdalia coronoides, Drysdalia mastersii,
and Naja hage) are polymorphic, and the oldest
species Leptotyphlops nigricans, Leptotyphlops scutifrons, and Leptotyphlops sylvicolus are monomophic
(Table 1).
DISCUSSION
Our study reveals that the presence of intraspecific
colour polymorphism is strongly correlated with the
age of a species (i.e. the oldest intraspecific diversification event): polymorphic snake species are significantly older than monomorphic species. This result
can be explained by the important ecological roles
that colour variation plays in ectothermic species
(e.g. thermoregulation, behaviour, and prey–predator
interactions; e.g. Rosenblum et al., 2004, 2010;
Clusella-Trullas, 2006; Clusella-Trullas et al., 2007).
Moreover, it is likely that intraspecific colour polymorphism may promote the ecological success of taxa
(Forsman & Aberg, 2008a; Roulin et al., 2011), and
that polymorphic taxa may be able to exploit a larger
diversity of habitat types. In addition, theory predicts
that variable coloration enhances the rate of geographic range expansion (Forsman et al., 2008), and
thus the capacity of species to colonize new habitats.
Hence, polymorphism may allow species to successfully face novel environmental challenges, such as
Pleistocene climate fluctuations (leading to the contraction and subsequent expansion of species; e.g.
Dubey et al., 2006) or current global warming (e.g.
Roulin et al., 2011).
In Europe, adders (Vipera berus) and asp vipers
(Vipera aspis) exhibit extensive intraspecific colour
variation, including melanistic forms, probably as an
adaptation to enhance rates of heat transfer while
basking in cold areas (Monney, Luiselli & Capula,
1996). Genetic data suggest that these snakes persisted in European refugia more successfully than did
most other taxa of reptiles and amphibians (i.e. not
only in southern European refugia, but also in central
Europe; Ursenbacher et al., 2006a, b; Joger et al.,
2007). Consistent with this finding, Forsman & Aberg
(2008a) showed that Australian reptile species exhibiting colour polymorphism have broader distributions
and exploit a higher number of habitat types.
In addition, fewer polymorphic than monomorphic
reptile species are represented among species currently listed as threatened in Australia (Forsman &
Aberg, 2008a), and the same trend is true for Australian frogs (Forsman & Hagman, 2009). Similarly, in
North American Squamates, polymorphic species tend
to have more northerly geographic distributions, and
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218
214
L. PIZZATTO and S. DUBEY
Diadophis punctatus
Contia tenuis
Thamnophis validus
Nerodia taxispilota
Nerodia rhombifer
Nerodia fasciata
Nerodia sipedon
Nerodia erythrogaster
Natrix tesselata
Natrix natrix
Natrix maura
Trimorphodon biscutatus
Masticophis flagellum
Coluber constrictor
Coronella austriaca
Lampropeltis pyromelana
Lampropeltis zonata
Lampropeltis getula
Pituophis deppei
Pituophis catenifer
Leptodeira nigrofasciata
Malpolon monspessulanus
Enhydris subtaeniata
Pseudechis australis
Hoplocephalus bungaroides
Hoplocephalus stephensii
Drysdalia mastersii
Drysdalia coronoides
Naja haje
Naja nubiae
Naja pallida
Naja katiensis
Naja mossambica
Cerrophidion godmani
Atropoides lmec
Atropoides mexicanus
Atropoides nummifer
Agkistrodon contortrix
Agkistrodon bilineatus
Agkistrodon piscivorus
Gloydius brevicaudus
Sistrurus miliarius
Sistrurus catenatus
Crotalus mitchelli
Crotalus tigris
Crotalus ruber
Crotalus atrox
Crotalus lepidus
Crotalus aquilus
Crotalus pusillus
Crotalus cerastes
Bitis arietans
Vipera berus
Vipera ammodytes
Vipera aspis
Charina bottae
Lichanura trivirgata
Typhlops platycephalus
Guinea bicolor
Tricheilostoma macrolepis
Namibia occidentalis
Leptotyphlops kafubi
Leptotyphlops nigroterminus
Leptotyphlops scutifrons
Leptotyphlops sylvicolis
Leptotyphlops nigricans
Varanus komodoensis
Lacerta viridis
0.5
Figure 1. Phylogeny of the 1113-bp cytochrome b gene in snake species, used in the phylogenetic comparative analyses
with a maximum likelihood (ML) procedure and the GTR + I + G model of substitution.
have more extensive geographic ranges (Forsman &
Åberg, 2008b), suggesting that they are able to tolerate a broader range of environmental conditions and
colder climates.
What could explain the presence/maintenance of
monomorphic species, given the advantage provided
by colour polymorphism? Because colour polymorphism can lead to speciation events through, for
example, reproductive isolation through sexual selection (see review of Gray & McKinnon, 2007), monomorphic species could be the result of relatively
recent speciation events. In addition, we can expect
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 210–218
COLOUR-POLYMORPHIC SPECIES ARE OLDER
215
tropics (Weir & Schluter, 2007). Our results demonstrate that the age of a species is not only determined
by external factors such as climatic variations, but
also by the morphological characteristics of species,
and how such characteristics allow species to deal
with temporal or geographic variations in their
environment.
Finally, our results also suggest that there is a
trend for egg-laying species to be slightly older that
live-bearing species, a pattern that could be explained
by an ancestral state of oviparity in Squamates
(lizards and snakes). Indeed, (ovo-)viviparity evolved
multiple times from oviparity as a result of abiotic
and biotic selections in Squamates (e.g. Shine & Bull,
1979; Shine, 1983).
In conclusion, understanding how species have
dealt with climate change in the past can provide
important insights into how they are likely to respond
to climate change in the future. Based on our results,
monomorphic species are likely to suffer more from
future climate variations than are polymorphic taxa.
ACKNOWLEDGEMENTS
Figure 2. Differences in the ages of snake species
[log(oldest intraspecific diversification in a million years)]
according to their reproductive mode (A), and presence or
absence of polymorphism (B). Circles represent averages
and bars represent the standard errors of the raw values
(i.e. not corrected for effects of phylogeny and covariates).
that heterogeneous habitats favour colour polymorphism, through the optimization of crypsis through
different processes for example (Gehlbach, 1988),
whereas homogeneous habitats may prevent the evolution of colour polymorphism. Consequently, species
living in such habitats are more likely to be monomorphic. Finally, species living in restricted areas
may be less prone to exhibit colour polymorphism
compared with widespread species (which occupy
various habitat types; Forsman & Aberg, 2008a).
Besides colour polymorphism, the age of a species is
also correlated with differences in past climatic conditions. For example, Dubey & Shine (2011b, 2012)
found that Northern Hemisphere amphibian and
reptile taxa from temperate areas are younger than
Southern Hemisphere taxa. This pattern probably
results from the occurrence of more extreme Pleistocene glacial events in the Northern than in the
Southern Hemisphere, potentially eliminating much
of the then-existing biodiversity (e.g. Hewitt, 2000,
2003). Similarly, in birds and mammals, the age of
species was younger at high latitudes than in the
We thank W. Wüster, A. Forsman, D. G. Broadley,
R. R. Pinto, and P. Passor for providing information
about the presence of colour polymorphism in particular species, S. Keogh for providing DNA sequences of
Hoplocephalus species, S. Blomberg for helpful tips
on using R, A. Roulin, R. Tingley, and anonymous
reviewers for providing helpful comments, and the
Swiss National Science Foundation and the Australian Research Council for funding.
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