Phylogenetic and morphological evidence reveals the association between diet and the evolution of the venom delivery system in Neotropical goo-eating snakes

Abstract

Advanced endoglyptodont snakes share a complex but homologous venom delivery system associated with the upper jaw and its dentition. Recently, a remarkable novel lower jaw venom delivery system was described for the Neotropical dipsadine radiation of goo-eating snakes. While most dipsadines are opistoglyphous and exhibit large, mainly serous venom glands associated with the upper jaw and supralabial glands, goo-eating dipsadine snakes are aglyphous and lack serous upper labial venom glands. Here, we provide new morphological and histological information on the oral glands and maxillary dentition of representatives of the major lineages of dipsadines that help trace the evolutionary steps that shaped the venom delivery system of dipsadines. We performed a maximum likelihood analysis on a molecular dataset that includes 443 terminals and seven loci. Our results show that goo-eating dipsadines form a monophyletic assemblage that includes the genus Adelphicos for the first time, along with Geophis, Atractus, Ninia, Chersodromus, Tropidodipsas, Sibon, and Dipsas. We also provide the first evidence of a complete shift from an upper jaw to a lower jaw venom delivery system associated with their specialized feeding behaviour. Unlike other dipsadines who exhibit typical endoglyptodont anteroposteriorly ridged posterior maxillary teeth, goo-eating dipsadines have uniform lateromedially ridged teeth throughout their maxilla. Our results indicate that the loss of the endoglyptodont venom delivery system occurred in the most recent common ancestor of goo-eating dipsadines, probably resulting from the loss of the embryonic posterior maxillary lamina responsible for the development of the venom delivery system.

Key words:

• Dipsadidae
• Duvernoy’s glands
• goo-eaters
• maxillary teeth
• non-front-fanged snakes
• venom glands

Acknowledgements

The authors are deeply indebted to Francisco L. Franco (Instituto Butantan), William Duellman, Linda Trueb (Museum of Natural History, University of Kansas), W. Ronald Heyer, Jorge Zug, Roy McDiarmid, Kevin de Queiroz (National Museum of Natural History), Jim McGuire and Carol Spencer (Museum of Vertebrate Zoology, University of California, Berkeley) for providing important specimens for dissection. We are grateful to Alberto B. Carvalho and Vanessa Yamamoto for scanning the specimens and editing the images at the Laboratório de Microtomografia Computadorizada do Museu de Zoologia, and to Marta M. Antoniazzi and Carlos Jared for providing support and allowing the use of their histological facilities at the Laboratório de Biologia Celular do Instituto Butantan. We also thank Valdir J. Germano and Aline Benetti for their help with specimens from the Herpetological Collections of the Instituto Butantan (Coleção Alfonse Richard Hoge) and Museu de Zoologia, respectively. This research was carried out in strict accordance with Brazilian federal laws, all sequenced tissues and histologically processed specimens were obtained exclusively from scientific collections.

Author contributions

LO, FG, and HZ conceived the work and wrote the manuscript. LO and FG performed the morphological experiments, conducted the phylogenetic analyses, edited the figures, and contributed equally for this study. LO, AP, and HZ dissected the specimens and conducted the gross anatomical studies. All authors contributed to data collection and to the construction of the dataset. All authors read, critically edited, and approved the final manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental material

Supplemental material for this article can be accessed here: https://doi.org/10.1080/14772000.2022.2153944.

Associate Editor: Dr Susan Tsang

Additional information

Funding

L.O. and F.G. were supported by scholarships from Fundação de Amparo à Pesquisa do Estado de São Paulo [FAPESP grant numbers 2014/14364-7, 2018/09301-7, 2012/08661-3, 2016/13469-5]. This work was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo [FAPESP grant numbers 2011/50206-9, 2016/50127-5], Conselho Nacional de Desenvolvimento Científico e Tecnológico [CNPq grant number 30.2611/2018-5], Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [CAPES grant numbers PROTAX 562171/2010–0, 44.0413/2015-0], and National Science Foundation (NSF grant number DEB-0613802].