Phyllomedusa 9(2):121-131, 2010 © 2010 Departamento de Ciências Biológicas - ESALQ - USP ISSN 1519-1397 Ecological and phylogenetic influences on maxillary dentition in snakes Andrew Knox and Kate Jackson Department of Biology, Whitman College, Walla Walla, Washington 99362, USA. E‑mail: [email protected]. Abstract Ecological and phylogenetic influences on maxillary dentition in snakes. The maxillary dentition of snakes was used as a system with which to investigate the relative importance of the interacting forces of ecological selective pressures and phylogenetic constraints in determining morphology. The maxillary morphology of three groups of snakes having different diets, with each group comprising two distinct lineages—boids and colubroids— was examined. Our results suggest that dietary selective pressures may be more significant than phylogenetic history in shaping maxillary morphology. Keywords: Serpentes, dentition, diet, ecology, evolution, morphology. Resumo Influências ecológicas e filogenéticas sobre a dentição maxilar das serpentes. Usamos a dentição maxilar das serpentes como um sistema para investigar a importância relativa das pressões seletivas ecológicas e das restrições filogenéticas na determinação da morfologia. Examinamos a morfologia maxilar de três grupos de serpentes com diferentes dietas, com cada grupo compreendendo duas linhagens distintas—Boidae e Colubroidea. Nossos resultados sugerem que as pressões seletivas relacionadas à dieta podem ser mais significativas que a história filogenética na conformação da morfologia maxilar. Keywords: Serpentes, dentição, dieta, ecologia, evolução, morfologia. Introduction and that dentitional morphology would be correlated with the type of prey favored by Morphology is controlled by the interaction different species. Phylogeny constrains the of phylogeny and selective pressure (Losos and “starting point” from which the morphology of a Miles 1994). We hypothesized that in the case of structure deviates in response to various selective snake maxillary dentition, form follows function, pressures (i.e., natural selection). Therefore, we reasoned that the relative strength of selective pressures could be tested by examining the extent to which maxillary dentition in a species deviated Received 14 September 2010. Accepted 20 November 2010. from the plesiomorphic condition of the lineage. Distributed December 2010. Our goal was to test the impact of selective Phyllomedusa - 9(2), December 2010 121 Knox and Jackson pressures attributable to different types of prey have few, small teeth thought to facilitate by observing the variation in the maxillary regurgitation of the egg shell after its contents dentition in snakes. have been consumed (Savitzky 1983). In contrast, Alethinophidian snakes have teeth on four or snakes that prey on soft‑shelled eggs have broad, five bones—the palatine, pterygoid, dentary, bladelike teeth to slice open the eggs for digestion maxilla, and sometimes, a premaxilla. However, (Broadley 1979). Based on these studies many snakes have evolved specific dentitional documenting dentitional specializations in patterns that affect their function. Because snakes, a comprehensive study can be undertaken maxillary morphology is highly variable, it is an to describe taxonomic and ecological patterns. important taxonomic character; the dentition has Comparison of the morphological variation been used as a character trait for describing and of ophidian maxillae with the dietary habits of identifying snake taxa for more than a century snakes may lead to a better understanding of the (e.g., Boulenger 1896) and is still used today selective pressures acting on the morphology of (e.g., Chippaux 2006). Because ophidian maxillary the maxilla. An ecomorphological perspective morphology varies interspecifically, it is useful allows us to explore whether diverse prey for identifying and describing snakes, along with availability might have driven rapid evolution other features, such as scales, hemipenal from a generalized plesiomorphic condition in morphology, and mo lecular characters. We used the colubroid ancestor. If so, then we should a collection of snake maxillae originally assembled observe a strong correlation between different for taxonomic studies to investigate the rela‑ types of maxillary dentition in snakes and their tionship between dentitional morphology and preferred type of prey. diet in a diversity of snakes. To test the role of phylogenetic constraints in Several studies have demonstrated apparent shaping morphology, we examined representatives correlations between specific types of prey and of two lineages of snakes—the boids and the the maxillary morphology of species of snakes colubroids (excluding taxa with highly specialized (e.g., Savitzky 1981, Vaeth et al. 1985, Jackson maxillary dentition for the injection of venom). et al. 1999, Jackson and Fritts 2004). For example, We recognize that this combination is far from Savitzky (1981) addressed dentitional specializa‑ ideal because Boidae comprises about 43 species, tion for a specific prey type; he hypothesized whereas Colubroidea contains some 2300 species that the occurrence of hinged teeth in some snake (Jackson 2007). The colubroids in our study are genera is associated with durophagy, and is an a diverse assemblage belonging to the para‑ adaptation that prevents the teeth from breaking phyletic group traditionally referred to as when it comes in contact with hard‑bodied prey. “Colubridae.” However, the two lineages are Other studies (Savitzky 1983, Cundall and Irish reciprocally monophyletic and distantly related; 1989, Greene 1989, Jackson and Fritts 2004) nonetheless, many taxa from each lineage fill elaborated this hypothesis to include other similar ecological niches. Potentially, analysis of morphological modifications, such as the the differences between boids and colubrids that presence of a large diastema in the maxillary share the same niche may provide insight into dentition and an arched maxillary bone for the the operative selective pressures and the ways in purpose of encircling the hard‑bodied prey as the which these pressures interact with phylogenetic snake bites it. Substantially lengthened teeth constraints. It is important to note fundamental were reported in predators that prey on soft items differences in the dentitional patterns of colubrids such as slugs (Zweifel 1954), and piscivorous and boids—colubrids have a posterior fang, snakes typically have numerous, sharp, sometimes enlarged and/or grooved, which often posteriorly curved teeth (Savitzky 1983). Snakes conducts venom, whereas boids lack a posterior that are specialized for calcareous egg‑eating fang but usually have enlarged anterior teeth. Phyllomedusa - 9(2), December 2010 122 Ecological and phylogenetic influences on maxillary dentition in snakes These are phylogenetically determined morpho‑ thon), Pituophis catenifer deserticola (Bull logies that may be modified by selective Snake), Lamprophis lineatus (Striped House pressures. Thus, we are interested in determining Snake), Psammophylax rhombeatus (Rhombic whether the maxillae of boids more strongly Skaapsteker), and Calabaria reinhardtii (African resemble those of other boids or is their maxillary Burrowing Python). Systematic and ecological morphology more similar to that of colubroids information appears in Table 1 and maxillae are that fill similar dietary niches. illustrated in Figure 1. Despite the fact that these species eat mammals, Materials and Methods their respective ranges of prey are at times diverse and may include other types of prey or have We compiled dietary information from the “generalist” qualities. Python sebae preys on literature for 45 species of snakes. We chose antelope and other large mammals. Lamprophis snakes that specialized on particular prey to lineatus is a generalist that feeds primarily on investigate explicit selective pressure. A total of rodents. Liasis mackloti is a semi‑aquatic generalist 45 colubroid and boid snake maxillae was pho‑ that consumes small mammals and some reptiles. tographed; snakes from Africa and South America Calabaria reinhardtii is fossorial and feeds on were most numerous. Species were grouped rodents by suffocating them. Pituophis catenifer according to their dietary preferences before eats small mammals and bird eggs, and their maxillae were examined. We focused on Psammophylax rhombeatus consumes mostly three dietary groupings—viz., species pre ferring mammals, in addition to lizards and amphibians. (1) mammalian, (2) aquatic, or (3) arboreal prey. Only one of these taxa has enlarged posterior Maxillae were stored in a 75% ethanol dentition—Psammophylax rhombeatus, which solution. All African specimens had been has grooved posterior fangs. None of the maxillae sputter‑coated with a gold/palladium mixture for is curved or contains diastemata. Python sebae, scanning electron microscopy as part of another Pituophis. catenifer, Lamprophis lineatus, and study. Maxillae were secured to a contrasting Liasis mackloti share many dentitional color of construction paper with double‑sided characteristics, including moderate intertooth tape to photograph them. The camera was mounted spacing, the absence of striations, and anterior to a photocopy stand and the photographed with and posterior teeth that are angled posteriorly at an Olympus Evolt E‑510 Digital SLR camera approximately 45˚, owing to moderate curvature with accessory components (Zuiko 50‑mm of the teeth. Lamprophis lineatus, P.