Biological Journal of the Linnean Society, 2010, ••, ••–••. With 3 figures Snake diets and the deep history hypothesis TIMOTHY J. COLSTON1*, GABRIEL C. COSTA2 and LAURIE J. VITT1 1Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA 2Universidade 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 2010bij_1502 1..12 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. ADDITIONAL KEYWORDS: canonical phylogenetic ordination – community ecology – niche theory – phylogenetic structure – reptile ecology. INTRODUCTION researchers have identified ecological shifts within and among major clades of organisms (Melville, Schulte & The structure of animal communities has been of Larson, 2001; Glor et al., 2003; Vitt et al., 2003; Vitt & interest to ecologists for more than half a century and Pianka, 2005), demonstrating that some ecological is central to understanding why there are so many traits have deep historical origins. We now know that species (Andrewartha & Birch, 1954; Hutchinson, much of the structure of some present-day communi- 1959). Ongoing species interactions, primarily compe- ties, with the exception of island communities (Losos tition and predation, dominated explanations during et al., 1998), results from the ability of species with much of the 20th Century (Pianka, 1973; Cody, 1974; deep historical roots to coexist (Vitt, Zani & Espósito, Schoener, 1974; Morin, 1983). The notion that present- 1999; Vitt & Pianka, 2005). day community structure might reflect species’ inter- Two very different hypotheses have been proposed actions in the past was introduced by G. E. Hutchinson to explain the origins of ecological differences among (Hutchinson, 1959) but not fully appreciated until species within present-day communities. The first phylogenetics merged with ecology, allowing research- hypothesis centres on recent effects, as closely-related ers to identify major shifts in ecological traits of entire taxa diverge to partition available resources in clades (Cadle & Greene, 1993; Losos, 1994; Webb et al., response to shifts in resource availability, inter-specific 2002). Using phylogenies to analyze ecological traits, competition or predation (competition–predation hypothesis). According to the competition–predation hypothesis, species interactions drive the evolution of *Corresponding author. E-mail: [email protected] divergence in resource use and niche characteristics © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, ••, ••–•• 1 2 T. J. COLSTON ET AL. (food, time, and microhabitat) among species in local S1). Representatives of all major clades and subclades assemblages. This hypothesis predicts that ecological were included. Our approach was to compile dietary traits of coexisting species are independent of phylog- data for snake species representing both ecological and eny and that major shifts in niche preference result phylogenetic diversity. For dietary analyses, we iden- from interactions among species within present-day tified 34 discreet prey categories, varying from fish assemblages. This hypothesis has been suggested to eggs to large vertebrates. These comprised: lizards, explain local community structure of Amazonian mammals, anurans, birds, fish, snakes, amphibian snakes (Henderson, Dixon & Soini, 1979). eggs, reptile eggs, bird eggs, crustaceans, gastropods, The second hypothesis (deep history hypothesis) annelids, caecilians, chilopods, salamanders, amphis- suggests that divergences deep in the evolutionary baenians, carrion, tortoises, crocodilians, fish eggs, history of organisms (rather than recent effects) invertebrate eggs, diplopods, coleopterans, neuropter- resulted in sets of ecological traits (or niche prefer- ans, arachnids, unidentifiable hexapods, isopterans, ences) that are maintained for the most part in dermapterans, lepidopterans, dipterans, hemipterans, species represented in present-day assemblages (Vitt orthopterans, hymenopterans, and other arthropods. & Pianka, 2005). The deep history hypothesis posits Many studies contained quantitative data on prey that ecological traits of coexisting species can be pre- items, often identified to species. However, some dicted based on phylogeny regardless of the commu- studies placed prey into broad categories (e.g. frogs, nity in which individual species presently reside. For lizards, birds, and mammals). Some studies provided example, just five divergences in the evolutionary data on the kinds of prey eaten but with no quantita- history of lizards (nonsnake squamates) account for tive measure of relative proportions of each prey 80% of the variation among clades in diets (Vitt & category. Because of this great variation in quality of Pianka, 2005, 2007). Other major ecological traits can data among published papers, we used the presence or be traced to origins deep in the evolutionary history of absence for the analyses. The advantage is that we can squamates (Vitt et al., 2003). include a large number of snake taxa in our analyses. In the present study, we test the deep history The disadvantage is that we lose some dietary resolu- hypothesis along one niche axis, diet, using snakes as tion and, as a result, our analysis provides a conser- our model clade of organisms. Snakes are gape-limited vative estimate of dietary divergence among snake predators, and are best known because of the diversity clades. of vertebrate prey that they consume (Shine, 1991; Greene, 1997). Many snakes, however, feed on inver- tebrate prey (Webb & Shine, 1993; Webb et al., 2000), PHYLOGENETIC RECONSTRUCTION and a large number of species are dietary specialists. We constructed a phylogenetic hypothesis for the rela- Snakes presumably originated in the Mesozoic (Jiang tionships of the 196 snake species based on several et al., 2007) and occur on all continents except Antarc- recent studies representing a balanced view of snake tica (Greene, 1997). They comprise the largest clade evolutionary history (Heise et al., 1995; Kraus & within squamate reptiles (Serpentes, with over 3100 Brown, 1998; Burbrink, Lawson & Slowinski, 2000; species) and occupy almost every habitat in the world, Vidal et al., 2000, 2007; Wilcox et al., 2002; Lawson including deserts, tropical and temperate forests as et al., 2005; Vidal & Hedges, 2005; Zaher et al., 2009). well as grasslands, freshwater (streams, rivers, lakes), We included studies that used nuclear genes, mito- and the oceans (Shine, 1991; Greene, 1997; Pough, chondrial DNA, and morphological characters to 2001; Vitt & Caldwell, 2008). Historical shifts in snake construct the phylogenetic hypothesis. Parsimony, diets probably resulted in adaptive radiations contrib- maximum likelihood, nonparametric bootstrapping, uting to the diversity of snake species observed in Neighbour-joining, and Bayesian analysis produced present-day snake assemblages. Dietary divergence is highly supported phylogenetic relationships in most often correlated with shifts in morphology (Schluter & instances. Our assumption in the subsequent analy- Grant, 1984), behaviour (Fryer & Iles, 1972), and ses is that this phylogeny accurately represents the ecology (Smith et al., 1978). best available reconstruction of the evolutionary history of snakes. MATERIAL AND METHODS STATISTICAL ANALYSIS SNAKE DIET DATA We used canonical phylogenetic ordination, CPO Dietary data were collected from available literature (Giannini, 2003), a method derived from canonical for 196 species of snakes, including representatives correspondence analysis (Ter Braak, 1986), to test from all ecological biomes and all six continents that the hypothesis that an association exists between contain snakes (see Supporting Information, Appendix snake evolutionary history and snake diets. CPO is a © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, ••, ••–•• SNAKE DIETARY SHIFTS 3 constrained ordination