What makes a fang? Phylogenetic and ecological controls on tooth evolution in rear-fanged snakes

• Main Authors: Erin P. Westeen, Andrew M. Durso, Michael C. Grundler, Daniel L. Rabosky, Alison R. Davis Rabosky
• Format: Article
• Language: English
• Published: BMC 2020-07-01
• Series: BMC Evolutionary Biology
• Subjects: Macroevolution; Morphology; Computed tomography; Evolutionary ecology; Dietary ecology; Dentition
• Online Access: http://link.springer.com/article/10.1186/s12862-020-01645-0

Abstract Background Fangs are a putative key innovation that revolutionized prey capture and feeding in snakes, and – along with their associated venom phenotypes – have made snakes perhaps the most medically-significant vertebrate animals. Three snake clades are known for their forward-positioned fangs, and these clades (Elapidae, Viperidae, and Atractaspidinae) contain the majority of snakes that are traditionally considered venomous. However, many other snakes are “rear-fanged”: they possess potentially venom-delivering teeth situated at the rear end of the upper jaw. Quantification of fang phenotypes – and especially those of rear-fanged species – has proved challenging or impossible owing to the small size and relative rarity of many such snakes. Consequently, it has been difficult to understand the evolutionary history of both venom and prey-capture strategies across extant snakes. We quantified variation in the dentition of 145 colubriform (“advanced”) snake species using microCT scanning and compared dental characters with ecological data on species’ diet and prey capture method(s) to understand broader patterns in snake fang evolution. Results Dental traits such as maxilla length, tooth number, and fang size show strong phylogenetic signal across Colubriformes. We find extreme heterogeneity and evolutionary lability in the rear-fanged phenotype in colubrid (colubrine, dipsadine, and natricine lineages) and lamprophiid snakes, in contrast to relative uniformity in the front fanged phenotypes of other groups (vipers and, to a lesser extent, elapids). Fang size and position are correlated with venom-use in vipers, elapids, and colubrid snakes, with the latter group shifting fangs anteriorly by shortening the entire maxillary bone. We find that maxilla length and tooth number may also be correlated with the evolution of dietary specialization. Finally, an ancestral state reconstruction suggests that fang loss is a recurring phenomenon in colubrid snakes, likely accompanied by shifts in diet and prey capture mode. Conclusions Our study provides a framework for quantifying the complex morphologies associated with venom use in snakes. Our results suggest that fang phenotypes, and particularly the rear-fanged phenotype, in snakes are both diverse and labile, facilitating a wide range of ecological strategies and contributing to spectacular radiations of these organisms in tropical and subtropical biomes worldwide.