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Biological Journal of the Linnean Society, 2010, 101, 476–486. With 3 figures
Snake diets and the deep history hypothesis
TIMOTHY J. COLSTON1*, GABRIEL C. COSTA2 and LAURIE J. VITT1
1
Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of
Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA
2
Universidade Federal do Rio Grande do Norte, Centro de Biociências, Departamento de Botânica,
Ecologia e Zoologia. Campus Universitário – Lagoa Nova 59072-970, Natal, RN, Brasil
Received 3 November 2009; accepted for publication 12 May 2010
bij_1502
476..486
The structure of animal communities has long been of interest to ecologists. Two different hypotheses have been
proposed to explain origins of ecological differences among species within present-day communities. The
competition–predation hypothesis states that species interactions drive the evolution of divergence in resource use
and niche characteristics. This hypothesis predicts that ecological traits of coexisting species are independent of
phylogeny and result from relatively recent species interactions. The deep history hypothesis suggests that
divergences deep in the evolutionary history of organisms resulted in niche preferences that are maintained, for
the most part, in species represented in present-day assemblages. Consequently, ecological traits of coexisting
species can be predicted based on phylogeny regardless of the community in which individual species presently
reside. In the present study, we test the deep history hypothesis along one niche axis, diet, using snakes as our
model clade of organisms. Almost 70% of the variation in snake diets is associated with seven major divergences
in snake evolutionary history. We discuss these results in the light of relevant morphological, behavioural, and
ecological correlates of dietary shifts in snakes. We also discuss the implications of our results with respect to
the deep history hypothesis. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society,
2010, 101, 476–486.
ADDITIONAL KEYWORDS: canonical phylogenetic ordination – community ecology – niche theory –
phylogenetic structure – reptile ecology.
INTRODUCTION
The structure of animal communities has been of
interest to ecologists for more than half a century and
is central to understanding why there are so many
species (Andrewartha & Birch, 1954; Hutchinson,
1959). Ongoing species interactions, primarily competition and predation, dominated explanations during
much of the 20th Century (Pianka, 1973; Cody, 1974;
Schoener, 1974; Morin, 1983). The notion that presentday community structure might reflect species’ interactions in the past was introduced by G. E. Hutchinson
(Hutchinson, 1959) but not fully appreciated until
phylogenetics merged with ecology, allowing researchers to identify major shifts in ecological traits of entire
clades (Cadle & Greene, 1993; Losos, 1994; Webb et al.,
2002). Using phylogenies to analyze ecological traits,
*Corresponding author. E-mail: [email protected]
476
researchers have identified ecological shifts within and
among major clades of organisms (Melville, Schulte &
Larson, 2001; Glor et al., 2003; Vitt et al., 2003; Vitt &
Pianka, 2005), demonstrating that some ecological
traits have deep historical origins. We now know that
much of the structure of some present-day communities, with the exception of island communities (Losos
et al., 1998), results from the ability of species with
deep historical roots to coexist (Vitt, Zani & Espósito,
1999; Vitt & Pianka, 2005).
Two very different hypotheses have been proposed
to explain the origins of ecological differences among
species within present-day communities. The first
hypothesis centres on recent effects, as closely-related
taxa diverge to partition available resources in
response to shifts in resource availability, inter-specific
competition or predation (competition–predation
hypothesis). According to the competition–predation
hypothesis, species interactions drive the evolution of
divergence in resource use and niche characteristics
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
SNAKE DIETARY SHIFTS
(food, time, and microhabitat) among species in local
assemblages. This hypothesis predicts that ecological
traits of coexisting species are independent of phylogeny and that major shifts in niche preference result
from interactions among species within present-day
assemblages. This hypothesis has been suggested to
explain local community structure of Amazonian
snakes (Henderson, Dixon & Soini, 1979).
The second hypothesis (deep history hypothesis)
suggests that divergences deep in the evolutionary
history of organisms (rather than recent effects)
resulted in sets of ecological traits (or niche preferences) that are maintained for the most part in
species represented in present-day assemblages (Vitt
& Pianka, 2005). The deep history hypothesis posits
that ecological traits of coexisting species can be predicted based on phylogeny regardless of the community in which individual species presently reside. For
example, just five divergences in the evolutionary
history of lizards (nonsnake squamates) account for
80% of the variation among clades in diets (Vitt &
Pianka, 2005, 2007). Other major ecological traits can
be traced to origins deep in the evolutionary history of
squamates (Vitt et al., 2003).
In the present study, we test the deep history
hypothesis along one niche axis, diet, using snakes as
our model clade of organisms. Snakes are gape-limited
predators, and are best known because of the diversity
of vertebrate prey that they consume (Shine, 1991;
Greene, 1997). Many snakes, however, feed on invertebrate prey (Webb & Shine, 1993; Webb et al., 2000),
and a large number of species are dietary specialists.
Snakes presumably originated in the Mesozoic (Jiang
et al., 2007) and occur on all continents except Antarctica (Greene, 1997). They comprise the largest clade
within squamate reptiles (Serpentes, with over 3100
species) and occupy almost every habitat in the world,
including deserts, tropical and temperate forests as
well as grasslands, freshwater (streams, rivers, lakes),
and the oceans (Shine, 1991; Greene, 1997; Pough,
2001; Vitt & Caldwell, 2008). Historical shifts in snake
diets probably resulted in adaptive radiations contributing to the diversity of snake species observed in
present-day snake assemblages. Dietary divergence is
often correlated with shifts in morphology (Schluter &
Grant, 1984), behaviour (Fryer & Iles, 1972), and
ecology (Smith et al., 1978).
MATERIAL AND METHODS
SNAKE DIET DATA
Dietary data were collected from available literature
for 196 species of snakes, including representatives
from all ecological biomes and all six continents that
contain snakes (see Supporting Information, Appendix
477
S1). Representatives of all major clades and subclades
were included. Our approach was to compile dietary
data for snake species representing both ecological and
phylogenetic diversity. For dietary analyses, we identified 34 discreet prey categories, varying from fish
eggs to large vertebrates. These comprised: lizards,
mammals, anurans, birds, fish, snakes, amphibian
eggs, reptile eggs, bird eggs, crustaceans, gastropods,
annelids, caecilians, chilopods, salamanders, amphisbaenians, carrion, tortoises, crocodilians, fish eggs,
invertebrate eggs, diplopods, coleopterans, neuropterans, arachnids, unidentifiable hexapods, isopterans,
dermapterans, lepidopterans, dipterans, hemipterans,
orthopterans, hymenopterans, and other arthropods.
Many studies contained quantitative data on prey
items, often identified to species. However, some
studies placed prey into broad categories (e.g. frogs,
lizards, birds, and mammals). Some studies provided
data on the kinds of prey eaten but with no quantitative measure of relative proportions of each prey
category. Because of this great variation in quality of
data among published papers, we used the presence or
absence for the analyses. The advantage is that we can
include a large number of snake taxa in our analyses.
The disadvantage is that we lose some dietary resolution and, as a result, our analysis provides a conservative estimate of dietary divergence among snake
clades.
PHYLOGENETIC
RECONSTRUCTION
We constructed a phylogenetic hypothesis for the relationships of the 196 snake species based on several
recent studies representing a balanced view of snake
evolutionary history (Heise et al., 1995; Kraus &
Brown, 1998; Burbrink, Lawson & Slowinski, 2000;
Vidal et al., 2000, 2007; Wilcox et al., 2002; Lawson
et al., 2005; Vidal & Hedges, 2005; Zaher et al., 2009).
We included studies that used nuclear genes, mitochondrial DNA, and morphological characters to
construct the phylogenetic hypothesis. Parsimony,
maximum likelihood, nonparametric bootstrapping,
Neighbour-joining, and Bayesian analysis produced
highly supported phylogenetic relationships in most
instances. Our assumption in the subsequent analyses is that this phylogeny accurately represents the
best available reconstruction of the evolutionary
history of snakes.
STATISTICAL
ANALYSIS
We used canonical phylogenetic ordination, CPO
(Giannini, 2003), a method derived from canonical
correspondence analysis (Ter Braak, 1986), to test
the hypothesis that an association exists between
snake evolutionary history and snake diets. CPO is a
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
478
T. J. COLSTON ET AL.
constrained ordination method that associates a
dependent matrix (diet in this case) with an independent matrix (phylogeny) maximizing the correlation between the two datasets. The significance of
the association is then determined by comparisons
with null models generated by Monte Carlo simulations. The goal of the analysis is similar to a Mantel
test, in the sense that a relationship between two
matrices is established. However, CPO detects variation overlooked by Mantel test and assigns significance to shifts in dependent variables associated
with each divergence point in the phylogeny, rather
than producing a significance value across the entire
tree (Giannini, 2003). For detailed information on
the method and some applications please refer to
(Giannini, 2003; Vitt & Pianka, 2005; Werneck, Colli
& Vitt, 2009).
We used presence–absence data in our diet matrix,
where ‘1’ indicated the presence and ‘0’ indicated the
absence of the prey item in the diet. Because snake
body size can affect size (and presumably type) of prey
ingested (Shine & Thomas, 2005), we used maximum
snout–vent length for each snake species as a covariate in our analysis to minimize the effect of body
size. The analysis was performed using CANOCO,
version 4.53 (Ter Braak & Smilauer, 2002). Monte
Carlo permutation tests were performed in stepwise
analysis on each clade using 9999 permutations. Symmetric scaling and unimodal methods were used, and
rare prey categories were downweighted. Each clade
was tested one at a time manually to obtain F- and
P-values. After each clade was tested, significant
clades were included in the model and the subsequent
clade that most reduced the variance was tested and
included if statistically significant (P < 0.05).
RESULTS
Snakes used in our analysis ate a wide diversity of
prey that varied in size from small social insects (e.g.
termites and ants) to large mammals and reptiles.
More than 20% of the 181 species of alethinophidian
snakes (referred to as advanced, nonblind snakes) ate
lizards, mammals, frogs, birds, fish, and snakes, with
more than half eating lizards (Table 1). Almost 70% of
the variation in diets among snake clades is associated with seven major divergences in snake evolutionary history (Fig. 1, Table 2). No scolecophidians
(blind snakes) ate vertebrates. All ate insects and
their eggs, with some eating spiders, centipedes, and
millipedes.
The most ancient divergence in snake evolutionary
history, the blind snake/advanced snake divergence,
accounted for almost 25% of the dietary divergence.
Although blind snakes and advanced snakes typically
separate in spatial niche space (all blind snakes are
fossorial whereas most modern snakes are terrestrial
or arboreal), they are often found in the same geographic regions (Martins & Oliveira, 1998; França &
Araújo, 2007; França et al., 2008). The next six clades
contributing to significant dietary divergences are, in
rank order, Leptotyphlopidae, Homalopsinae, Natricinae, Aparallactinae, Tachymenini, and Pareatinae
(Table 2). Five other clades, Viperidae, Colubrinae,
Dipsadinae, Boidae, and Elapinae, are significant contributors to dietary variation but each explains less
than 3% of the total dietary divergence. Advanced
snakes as a group are distributed directly opposite to
blind snakes across a gradient of prey types varying
from vertebrates to arthropods (Fig. 2). It is also
shown that natricines and homalopsines are strongly
tied to the frog-salamander-fish end of a vertebrate
prey gradient that extends from terrestrial vertebrates to aquatic vertebrates and gastropods. Tachymenini and pareatine snakes are weakly associated
with the aquatic end of the vertebrate prey gradient,
whereas aparallactine snakes are weakly associated
with the terrestrial vertebrate portion of the vertebrate prey gradient.
A plot of snake species scores on the two canonical
axes describing dietary variation reveals just how
extreme blind snakes are compared to advanced
snakes (Fig. 3). Most species of blind snakes feed
primarily on larvae and pupae of termites and ants,
with species of leptotyphlopids feeding on some other
arthropods as well. Relatively few advanced snakes
have exploited the high prey diversity and abundance
of arthropods. Within advanced snakes, natricines and
homalopsines have independently converged to feed on
aquatic vertebrate prey, including frogs, salamanders,
and fishes, whereas most remaining advanced snakes
feed primarily on terrestrial vertebrates, including
birds, mammals, reptiles, and some amphibians. A few
have specialized on gastropods (Fig. 3).
DISCUSSION
Although the origin of snakes within squamate reptiles remains uncertain, Serpentes is clearly a monophyletic clade that arose in the Mesozoic Era,
diverging into the two major clades, Scolecophidia
(blind snakes) and Alethinophidia (advanced snakes),
probably during the Hauterivian of the early Cretaceous, approximately 133 Mya (Caldwell & Lee, 1997;
Caprette et al., 2004; Burbrink & Pyron, 2008). More
than 500 species of blind snakes are known, comprising three ecologically similar families (Greene, 1997).
By contrast, advanced snakes have diversified into
more than 2300 species (approximately 80% of all
extant snakes) in thirteen or more families, with
species occupying almost all imaginable microhabitats in temperate and tropical regions of the world
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
SNAKE DIETARY SHIFTS
479
Table 1. Frequency of snake species within each major clade feeding on prey types used in this analysis
Lizards
Mammals
Anurans
Birds
Fish
Snakes
Other Arthropods
Amph. eggs
Reptile eggs
Bird eggs
Crustaceans
Gastropods
Annelids
Caecilians
Chilopods
Salamanders
Amphisbaenians
Carrion
Tortoises
Crocodilians
Fish eggs
Invert. eggs
Diplopods
Coleopterans
Neuropterans
Arachnids
Unidentifiable Hexapods
Isopterans
Dermapterans
Lepidopterans
Dipterans
Hemipterans
Orthopterans
Hymenopterans
Alethinophidians (N = 181)
Scolecophidians (N = 14)
Number
of species
Percent
of clade
Number
of species
Percent
of clade
100
83
72
48
46
37
27
14
12
12
9
8
8
6
6
4
4
3
2
2
2
2
1
1
1
0
0
0
0
0
0
0
0
0
55.25
45.86
39.78
26.52
25.41
20.44
14.92
7.74
6.63
6.63
4.97
4.42
4.42
3.32
3.32
2.22
2.21
1.66
1.11
1.10
1.11
1.11
0.55
0.55
0.55
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0
0
0
0
0
0
14
0
0
0
0
0
0
0
2
0
0
0
0
0
0
13
2
1
2
4
12
8
2
2
2
2
2
14
0
0
0
0
0
0
100
0
0
0
0
0
0
0
14.29
0
0
0
0
0
0
92.86
14.29
7.14
14.29
28.57
85.71
57.14
14.29
14.29
14.29
14.29
14.29
100
Percent of species is the percent with respect to the total number of species in each clade. The number of snake species
represented in each clade is indicated in parentheses. Prey types are ranked by their frequency of use in alethinophidians.
(Shine, 1991; Greene, 1997). We first discuss dietary
divergences detected in our analysis. We then discuss
the relevant morphological, behavioural, and ecological correlates of dietary shifts in snakes. Finally,
we discuss our results in light of the deep history
hypothesis.
DIETARY
DIVERGENCES
Our analysis of snake diets indicates that significant
dietary shifts occurred deep within snake evolutionary history, a pattern similar to that described for
squamate reptiles typically referred to as ‘lizards’
(Vitt et al., 2003). Blind snakes eat small invertebrates, most of which are social insects and their
larvae (Webb & Shine, 1993; Webb et al., 2000). These
snakes inhabit nests of social insects, usually but
not always underground, and occasionally eat other
arthropods, probably within social insect nests. They
do not eat a variety of other invertebrates that are
common underground but usually not associated with
social insect nests (e.g. earthworms, cicada larvae,
and scarabeid beetle larvae). By contrast, advanced
snakes eat a wider range of prey types varying from
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
480
T. J. COLSTON ET AL.
Uromacer frenatus
Antillophis parvifrons
Erythrolamprus aesculapii
Liophis breviceps
Xenodon rhabdocephalus
Xenodopholis scalaris
Xenoxybelis argenteus
Hydrodynastes gigas
Helicops angulatus
Helicops hagmanni
Helicops leopardinus
Philodryas olfersii
Philodryas patagoniensis
Phylodryas viridissimus
Clelia clelia
Drepanoides anomalus
Pseudoboa coronata
Taeniophallus brevirostris
Taeniophallus nicagus
Oxyrhopus formosus
Tripanurgos compressus
Tomodon dorsatus
Imantodes cenchoa
Dipsas indica
Atractus alphonsehogei
Atractus latifrons
Thamnophis couchii
Thamnophis elegans
Thamnophis marcianus
Thanmophis melanogaster
Thamnophis sirtalis
Storeria occipitomaculata
Storeria dekayi
Regina grahamii
Nerodia clarkii
Nerodia cyclopion
Nerodia erythrogaster
Nerodia fasciata
Nerodia harteri
Nerodia rhombifer
Nerodia sipedon
Natrix natrix
Natrix maura
Natrix tesselata
Afronatrix anoscopus
Phyllorhynchus decurtatus
Phyllorhynchus browni
Spilotes pullatus
Tantilla gracilis
Tantilla melanocephala
Oxybelis aeneus
Oxybelis fulgidus
Oligodon formosanus
Chironius fuscus
Chironius multiventris
Pseustes poecilonotus
Leptophis ahaetulla
Boiga irregularis
Boiga blandingi
Dasypeltis scabra
Lycodon aulicus
Symphimus mayae
Dendrophidion dendrophis
Mastigodryas boddaerti
Drymoluber dichrous
Gyalopion quadrangulare
Rhinobothryum lentiginosum
Arizona elegans
Rhinocheilus lecontei
Pantherophis obsoleta
Pituouphis catenifer
Coronella austriaca
Zamenis lineatus
Elaphe quatorlineata
Coluber hippocrepis
Grayia smythii
Tropidechis carinatus
Notechis scutatus
Hoplocephalus bungaroides
Aipysurus eydouxii
Emydocephalus annulatus
Lapemis curtis
Oxyuranus microlepidotus
Oxyuranus scutellatus
Vermicella annulata
Unechis dwyeri
Unechis spectbilis
Unechis nigrostriatus
Unechis nigriceps
Unechis monachus
Unechis gouldii
Unechis flagellum
Unechis carpentariae
Suta suta
Laticauda crockeri
Laticauda colubrina
Micrurus averyi
Micrurus surinamensis
Micrurus spixii
Micrurus lemniscatus
Micrurus hemprichii
Naja nigrircollis
Naja nigricincta
Naja mossambica
Naja anchietae
Naja annulifera
Naja nivea
Naja melanoleuca
Dendroaspis jamesoni
Hemachatus haemachatus
Aspidelaps lubricus
Psammophis phillipsi
Psammophis trinasalis
Psammophis mossambicus
Psammophis notostictus
Psammophis namibensis
Psammophis jallae
Psammophis breviostris
Mehelya capensis
Atractaspis aterrima
Polemon acanthias
Tachymenini
6
3
Natricinae
Aparallactinae
5
Enhydris bocourti
Enhydris sieboldii
Enhydris innominata
Enhydris polylepis
Enhydris plumbea
Enhydris enhydris
Enhydris doriae
Enhydris chinensis
Myron richardsonii
Gerarda prevostiana
Fordonia leucobalia
Cerberus rynchops
Cantoria violacea
Bitia hydroides
Homalopsis buccata
Crotalus horridus
Crotalus lepidus
Crotalus o. concolor
Sistrurus catenatus
Agkistrodon piscivorus
Lachesis muta
Bothrops moojeni
Bothrops atrox
Gloydius shedaoensis
Calloselasma rhodostoma
Atheris squamiger
Echis coloratus
Bitis nasicornis
Bitis gabonica
Vipera ammodytes
Vipera ursinii
Pareas carinatus
Homalopsinae
4
Pareatinae
7
Acrochordus granulatus
Eryx colubrinus
Eryx tataricus
Eryx johnii
Eryx jayakari
Eryx jaculus
Eryx elegans
Eryx conicus
Eryx miliaris
Charina bottae
Charina trivirgata
Candoia aspera
Candoia carinata
Candoia bibroni
Corallus enydris
Corallus hortulanus
Corallus caninus
Epicates cenchria
Eunectes murinus
Boa constrictor
Calabaria reinhardti
Python sebae
Python regius
Morelia spilota
Loocemus bicolor
Xenopeltis unicolor
Cylindrophis rufus
1
Alethinophidia
Leptotyphlopidae
Scolecophidia
2
Anilius scytale
Tropidophis melanurus
Ramphotyphlops australis
Ramphotyphlops pinguis
Ramphotyphlops nigrescens
Ramphotyphlops bituberculatus
Rhinotyphlops lalandei
Rhinotyphlops s. petersii
Rhinotyphlops mucruso
Typhlops bibronii
Typhlops fornasinii
Typhlophis squamosus
Leptotyphlops humilis
Leptotyphlops dulcis
Leptotyphlops scutifrons
Figure 1. Phylogenetic hypothesis for 196 snake species used in the present study. Numbers indicate the seven clades
that explain most of the variance in the diet matrix (Table 2).
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
481
SNAKE DIETARY SHIFTS
Table 2. Results of a phylogenetic ordination analysis based on a canonical correspondence analysis for diets of 196 snake
species representing all major clades in all major biomes of the world
Clade
Variation
Variation%
F
P
Scolecophiida/Alethinophidia
Leptotyphlopidae
Homalopsinae
Natricinae
Aparallactinae
Tachymenini
Pareatinae
Aniliidae
Atractaspididae
Viperidae
Pythoninae
Colubrinae
Dipsadinae
Boidae
Boodontinae
Elapinae
Elapidae
Colubridae
Psammophiinae
Cylindrophiidae
Laticaudaudinae
Anomalepididae
Crotalinae
Caenophidia
Henophidia
Boinae
Xenopeltidae
Xenodontinae
0.74
0.32
0.29
0.29
0.16
0.13
0.12
0.09
0.08
0.07
0.07
0.07
0.07
0.06
0.05
0.05
0.04
0.04
0.04
0.04
0.04
0.03
0.03
0.03
0.02
0.02
0.01
0.01
24.75
10.73
9.73
9.73
5.43
4.16
4.13
2.86
2.73
2.40
2.30
2.20
2.20
1.97
1.80
1.60
1.33
1.33
1.27
1.23
1.20
1.07
1.00
0.87
0.73
0.53
0.33
0.23
21.26
9.61
9.52
9.10
5.44
4.30
4.20
2.99
2.90
2.54
2.47
2.39
2.39
2.16
1.99
1.78
1.50
1.50
1.40
1.37
1.34
1.18
1.11
0.96
0.82
0.58
0.37
0.27
< 0.01
< 0.01
< 0.01
< 0.01
0.02
0.03
0.04
0.08
0.10
0.01
0.06
< 0.01
0.03
0.01
0.09
0.04
0.10
0.16
0.17
0.16
0.23
0.19
0.31
0.40
0.30
0.84
0.77
0.80
Clades are ranked by the amount of variation explained at each node. Although significance drops off after the seventh
clade, a few clades lower in the ranking attain significance. However, the portion of total variance explained by each of
these is minimal (less than 2.5% for each one).
invertebrates to large vertebrates. None specialize on
adults, larvae or pupae of social insects. Advanced
snakes that do specialize on invertebrates (small prey
relative to head size), such as the Aparallactinae,
tend to specialize on invertebrates such as centipedes,
although some species also eat amphisbaenians and
earthworms (Gower & Rasmussen, 2004). The Aparallactinae is located closest to the origin in Figure 2,
suggesting that its dietary preference is not strongly
associated with a particular group of prey.
MORPHOLOGICAL
CORRELATES OF
DIETARY DIVERGENCE
The present study shows that dietary divergence
within a clade may be an evolutionary first response
to morphological adaptations. The transition from
small (relative to body size) invertebrate prey types
(blind snakes) to large prey types (advanced snakes)
is associated with a wide range of changes in morphology. Blind snakes have relatively rigid nonkinetic skulls, whereas advanced snakes have toothed
palatopterygoid jaw arches and a highly kinetic lower
jaw (Kley, 2006; Vincent et al., 2006). Rigid nonkinetic
skulls of blind snakes limit the size of prey that can
be consumed. The highly kinetic skull of advanced
snakes, along with independence of lower jaws resulting from a lack of an anterior symphysis, allows them
to feed on much larger prey (relative to head size)
using a ratcheting motion of the lower jaws, effectively pulling the prey down the snake’s throat. Alternatively, recent studies have suggested that the
morphology of blind snakes might comprise a highly
derived specialization for fossoriality and/or a diet
based on ants and termites (Kley, 2006; Rieppel, Kley
& Maisano, 2009).
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
T. J. COLSTON ET AL.
Gastropods
Annelids
Crustaceans
4.0
2.5
482
Prey category
Clades
Amph. Eggs
Homalopsinae
Natricinae
Scolecophidia
Fish
Alethinophidia
Aquatic Prey
Hymenopterans
Homalopsinae
Isopterans
Hexapods
Trachymeninae
Pareatinae
Anurans
Alethinophidia
Arthropods (unid)
Inverts (unid)
Scolecophidia
Crocodilians
Aparallactinae
-1.5
Tortoises
Caecilians
-1.0
Coleopterans
Chilopods Leptotyphlopidae
Aves
Neuropterans
Snakes
Diplopods
Lizards
Mammals
Bird Eggs
Carrion
Amphisbaenians
Fish Eggs
Reptiles (misc.)
CCA Axis 1
Arachnids (unid)
Lepidopterans
Hemipterans
Dermapterans
Orthopterans
Dipterans
Arthropodprey
(excluding aquatics)
3.0
Figure 2. Biplot from a phylogenetic ordination based on
canonical correspondence analysis (CCA) relating snake
phylogeny (arrows) to snake diets (triangles). Canonical
axes represent linear combinations of diet to snake phylogeny. Arrows represent correlations of phylogeny with
axes and arrow length represents the strength of the
relationship. Snake diet items are weighted averages of
each species scores. The first canonical axis accounts for
32.5% and the second canonical axis accounts for 31.3% of
total variation. Diet items (triangles) close to the graph
centre (0, 0) indicate either low association with any snake
clade (arrows) or a positive association with a specific
combination of all snake clades. Diet items displayed in
the periphery of the graph indicate either high association
with a specific snake clade or an occasional association, particularly for those clades with low occurrence
(Ter Braak & Smilauer, 2002).
BEHAVIOURAL
CCA Asix 2
Natricinae
CORRELATES OF DIETARY DIVERGENCE
An obvious behavioural consequence of dietary divergence comes from the fact that, within advanced
snakes, several different modes of prey detection and
capture have evolved, including possibly multiple
origins of venom delivery systems (Fry et al., 2008).
Chemosensory systems have been shown to evolve to
detect specific prey types and are most effective at
detecting current prey (Cooper, 2008). Even though
all snake species utilize chemosensory systems to
find prey (Halpern, 1992), the diversity of prey eaten
by advanced snakes suggests that chemosensory
systems have likely diverged in response to historical
dietary shifts. Some advanced snakes, such as pitvipers (e.g. Crotalus, Bothrops, and Trimeresurus),
which employ a sit-and-wait foraging mode, use
chemosensory cues to detect ambush sites and then
use infra-red sensory systems to detect passing prey
Vertebrate Prey
-2.0
CCA Axis 2
Salamanders
-1.5
CCA Axis 1
2.5
Figure 3. Bipolot showing blind snakes (red circles) and
advanced snakes (all other symbols) in the first two
canonical correspondence axes of dietary niche space with
advanced snakes broken down to show that all natricines
and homalopsines (two clades of advanced snakes) have
taken advantage of aquatic prey with all other advanced
snakes restricted primarily to other vertebrate prey types.
CCA, canonical correspondence analysis.
(Clark, 2002, 2004). Other advanced snakes such
as racers (e.g. Coluber, Masticophis, and Chironius),
which employ an active foraging mode, use vision to
locate prey and chemical cues to discriminate prey
(Greene, 1997; Mullin & Cooper, 1998). Blind snakes
have reduced eyes without the ability to simply locate
prey visually (Greene, 1997) and lack infra-red
sensory systems (Greene, 1997).
ECOLOGICAL
CORRELATES OF DIETARY DIVERGENCE
The most obvious ecological correlate of the dietary
shift from subterranean insects to largely terrestrial
and aquatic vertebrates is the shift from a fossorial
lifestyle in blind snakes compared to the much more
diverse range of lifestyles found within advanced
snakes. Blind snakes occupy a relatively narrow niche
globally, with all species living within subterranean
(and occasionally, arboreal) social insect nests. The
results obtained in the present study clearly reveal
that snakes in the Scolecophidia almost exclusively
exploit a resource not used by advanced snakes
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
SNAKE DIETARY SHIFTS
(Fig. 3). Most snakes in the Alethinophidia are terrestrial, arboreal, aquatic or marine, although some
have independently evolved subterranean lifestyles.
Among the latter, some species live in sand (e.g.
Chionactis and Chilomeniscus) or under leaf litter
and within humus (e.g. Atractus) but none live within
social insect nests. As a consequence of this diverse
use of microhabitats, diets of advanced snakes are not
only diverse (Fig. 3) but have diverged repeatedly
during the evolutionary history of snakes. Another
evident ecological correlate of diet occurs in aquatic
lineages, especially Natricinae and Homalopsinae,
both of which feed mainly on aquatic vertebrates
(frogs, salamanders, and fishes). These lineages have
independently specialized on aquatic prey: the
Natricinae primarily in freshwater habitats in the
New World, and the Homalopsinae primarily in freshwater habitats the Old World, including Australia.
LOCAL
COMMUNITY STRUCTURE AND THE
DEEP HISTORY HYPOTHESIS
The results of the present study demonstrate that
major dietary shifts occurred early in snake evolutionary history, therefore supporting the deep history
hypothesis. However, these results do not rule out the
potential role of competition and predation in the
structure of local communities. Examination of local
communities alone has little exploratory power in
ecology and evolutionary biology (Ricklefs, 2008). The
field of phylogenetic community ecology provides a
framework to study the relative contribution of competition and habitat filtering in community structure
(Webb et al., 2002; Chazdon et al., 2003; Anderson,
Lachance & Starmer, 2004). A necessary first step is
to examine the distribution of ecological characters
among species on an independently derived phylogeny. Three possible scenarios exist: (1) ecological characters evolved randomly in the group (i.e Brownian
motion), in this case sister species will tend to share
some degree of ecological similarity (phylogenetic
inertia); (2) ecological characters will tend to be more
similar than expected under a random walk model
(niche conservatism), in this case sister species are
very similar to each other ecologically; and (3) ecological characters are more different than expected by
a random walk model, in this case sister species will
have very different ecological strategies (niche evolution). With this information in hand, it is possible to
explore how the local community composition reflects
the regional species pool (Webb et al., 2002). Again,
Three possibilities exist: (1) the local community is a
random subset of the regional species pool; (2) the
local community is a subset of closely related species
(phylogenetic clustering); and (3) the local community
is a subset of distant related species (phylogenetic
483
overdispersion). The interplay of these two factors
will determine the relative contribution of the two
processes on shaping community structure (Webb
et al., 2002; Cooper, Rodriguez & Purvis, 2008). For
example, in groups that show niche conservatism if
the local community is assembled as a subset of
closely-related species (phylogenetic clustering), this
would be evidence for habitat filtering playing a role
in structuring the local assemblage, whereas, if the
local community is assembled by a subset of distant
related species, this would be evidence that competition played a role in structuring the local assemblage
(Webb et al., 2002).
A recent study showed that phylogenetic overdispersion is a common tendency for mammalian communities (Cooper et al., 2008). However, that same
study did not assess whether any ecological trait of
coexisting species was related to the phylogeny (e.g.
phylogenetic overdispersion would not be an evidence
of competition if a given niche characteristic were not
related to phylogeny). Overall, phylogenetic structure
and ecological interactions may both act to determine
community structure (Kraft, Valencia & Ackerly,
2008; Werneck et al., 2009). The challenge remains in
identifying the relative contribution of these two
major forces in different organisms, regions, and specific traits (Kembel, 2009). Our analysis reveals that
snake diets are associated with ancient events in the
evolutionary history of the group. Future studies
should focus on whether or not local snake communities around the world are composed of random
subsets (i.e. not clustered or overdispersed) of the
regional species pool.
CAVEAT
Similar to recent studies on nonsnake squamates
(lizards), the present analysis shows that a major
ecological trait of snakes, the food they eat, has shifted
during the evolutionary history of the clade, and that
many present-day species simply eat what their ancestors ate, regardless of where they now live. Unlike
studies on lizards, in which quantitative and comparable data were available on relative proportions of
prey categories in the diets of many species (Vitt &
Pianka, 2005, 2007), the present study was constrained to presence–absence data in constructing our
prey matrix for analyses. Effectively, this renders a
specialist that might occasionally eat something different as a generalist, relatively speaking. As a consequence, our analysis misses many potential dietary
shifts that would be detected with quantitative data
and is thus conservative. In addition, reconstruction of
the evolutionary relationships of squamates, including
snakes, is in a state of flux, as new techniques,
additional genes, better analyses, and better taxon
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486
484
T. J. COLSTON ET AL.
sampling are applied. The phylogeny used in the
present study was based on current available published analyses and is likely to change as more data
and better analyses are used. Nevertheless, we are
confident that the major dietary shifts identified in the
present study will hold.
ACKNOWLEDGEMENTS
We thank the University of Oklahoma Zoology
Department and the Sam Noble Oklahoma Museum
of Natural History for financial support. We graciously thank the many snake natural historians who
collected diet data used in our analyses. G.C.C. was
supported by a Fulbright/CAPES PhD fellowship
(#15053155-2018/04-7).
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Appendix S1. References used for diet data.
Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials
supplied by the authors. Any queries (other than missing material) should be directed to the corresponding
author for the article.
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 476–486