661
Views
2
CrossRef citations to date
0
Altmetric
Research Article

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

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all

References

  • Arteaga, A., Salazar-Valenzuela, D., Mebert, K., Peñafiel, N., Aguiar, G., Sánchez-Nivicela, J. C., Pyron, R. A., Colston, T. J., Cisneros-Heredia, D. F., Yánez-Muñoz, M. H., Venegas, P. J., Guayasamin, J. M., & Torres-Carvajal, O. (2018). Systematics of South American snail-eating snakes (Serpentes, Dipsadini), with description of five new species from Ecuador and Peru. ZooKeys, 766, 79–147. https://doi.org/10.3897/zookeys.766.24523
  • Avise, J. C. (2000). Phylogeography: The history and formation of species. Harvard University Press.
  • Bancroft, J. D., & Stevens, A. (1996). Theory and practice of histological techniques (4th ed.). Churchill Livingstone.
  • Boulenger, G. A. (1894). Catalogue of the snakes in the British Museum (Natural history). Volume II Containing the conclusion of the Colubridae Aglyphae. Taylor and Francis.
  • Brongersma, L. D. (1958). Some features of the Dipsadinae and Pareinae (Serpentes, Colubridae). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Serie C, 61, 7–12.
  • Cadle, J. E., & Greene, H. W. (1993). Phylogenetic patterns, biogeography, and the ecological structure of Neotropical snake assemblages. In R. E. Ricklefs & D. Schluter (Eds.), Species diversity in ecological communities: Historical and geographical perspective (pp. 281–293). University of Chicago Press.
  • Campbell, J. A., & Smith, E. S. (1998). A new genus and species of colubrid snake from the Sierra de las Minas of Guatemala. Herpetologica, 54, 207–220.
  • Campbell, J. A., Smith, E. S., & Hall, A. S. (2018). Caudals and calyces: The curious case of a consumed Chiapan colubroid. Journal of Herpetology, 52, 458–471. https://doi.org/10.1670/18-042
  • Contrera, M. G. D., Lopes, R. A., Costa, J. R. V., Petenusci, S. O., & Lima-Verde, J. S. (1983). The histology of salivary glands in the colubrid snake Sibynomorphus mikanii (Schlegel, 1837). Canadian Journal of Zoology, 61, 936–941. https://doi.org/10.1139/z83-125
  • Cundall, D., & Greene, H. W. (2000). Feeding in snakes. In K. Schwenk (Ed.). Feeding: Form, function and evolution in tetrapod vertebrates (pp. 293–333). Academic Press.
  • Daza, J. D., Diogo, R., Johnston, P., & Abdala, V. (2011). Jaw muscles across lepidosaurs: A reappraisal. Anatomical Record, 294, 1765–1782. https://doi.org/10.1002/ar.21467
  • Downs, F. L. (1967). Intrageneric relationships among colubrid snakes of the genus Geophis Wagler. Miscellaneous Publications Museum of Zoology, University of Michigan, 131, 1–193. https://hdl.handle.net/2027.42/56375
  • Dunn, E. R. (1935). The snakes of the genus Ninia. Proceedings of the National Academy of Sciences of the United States of America, 21, 9–12. https://doi.org/10.1073/pnas.21.1.9
  • Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution, 63, 1–19. https://doi.org/10.1111/j.1558-5646.2008.00549.x
  • Fernandes, R. (1995). Phylogeny of the dipsadine snakes [Unpublished doctoral dissertation]. The University of Texas at Arlington.
  • Fry, B. G., Casewell, N. R., Wüster, W., Vidal, N., Young, B., & Jackson, T. N. W. (2012). The structural and functional diversification of the Toxicofera reptile venom system. Toxicon, 60, 434–448. https://doi.org/10.1016/j.toxicon.2012.02.013
  • Fry, B. G., Scheib, H., Van Der Weerd, L., Young, B., Mcnaughtan, J., Ramjan, S. F. R., Vidal, N., Poelmann, R. E., & Norman, J. A. (2008). Evolution of an arsenal: Structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular & Cellular Proteomics, 7, 215–246. https://doi.org/10.1074/mcp.M700094-MCP200
  • Gopalakrishnakone, P., & Kochva, E. (1990). Venom glands and some associated muscles in sea snakes. Journal of Morphology, 205, 85–96. https://doi.org/10.1002/jmor.1052050109
  • Grazziotin, F. G., Zaher, H., Murphy, R. W., Scrocchi, G., Benavides, M. A., Zhang, Y., & Bonatto, S. L. (2012). Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): A reappraisal. Cladistics, 28, 437–459. https://doi.org/10.1111/j.1096-0031.2012.00393.x
  • Greene, H. W. (1997). Snakes – The evolution of mystery in nature. University of California Press.
  • Grünwald, C. I., Toribio-Jiménez, S., Montaño-Ruvalcaba, C., Franz-Chávez, H., Peñaloza-Montaño, M. A., Barrera-Nava, E. Y., Jones, J. M., Rodriguez, C. M., Hughes, I. M., Strickland, J. L., & Reyes-Velasco, J. (2021). Two new species of snail-eating snakes of the genus Tropidodipsas (Serpentes, Dipsadidae) from southern Mexico, with notes on related species. Herpetozoa, 34, 233–257. https://doi.org/10.3897/herpetozoa.34.e69176
  • Haas, G. (1931). Die Kiefermuskulatur und die Schädelmechanik der Schlangen in vergleichender Darstellung. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere, 53, 127–198.
  • Harvey, M. B., Fuenmayor, G. R., Portilla, J. R. C., & Rueda-Almonacid, J. V. (2008). Systematics of the enigmatic dipsadine snake Tropidodipsas perijanensis Alemán (Serpentes: Colubridae) and review of morphological characters of Dipsadini. Herpetological Monographs, 22, 106–132. https://doi.org/10.1655/08-025.1
  • Holding, M. L., Trevine, V. C., Zinenko, O., Strickland, J. L., Rautsaw, R. M., Mason, A. J., Hogan, M. P., Parkinson, C. L., Grazziotin, F. G., Santana, S. E., Davis, M. A., Rokyta, D. R. (2022). Evolutionary allometry and ecological correlates of fang length evolution in vipers. Proceedings of the Royal Society B, 289(1982), 20221132. https://doi.org/10.1098/rspb.2022.1132
  • Jackson, K. (2003). The evolution of venom-delivery systems in snakes. Zoological Journal of the Linnean Society, 137, 337–354. https://doi.org/10.1046/j.1096-3642.2003.00052.x
  • Jackson, K. (2007). The evolution of venom-conducting fangs: Insights from developmental biology. Toxicon, 49, 975–981. https://doi.org/10.1016/j.toxicon.2007.01.007
  • Jackson, K., & Fritts, T. H. (1995). Evidence from tooth surface morphology for a posterior maxillary origin of the proteroglyph fang. Amphibia-Reptilia, 16, 273–288. https://doi.org/10.1163/156853895X00073
  • Jackson, T. N. W., Jouanne, H., & Vidal, N. (2019). Snake venom in context: Neglected clades and concepts. Frontiers in Ecology and Evolution, 7, 1–9. https://doi.org/10.3389/fevo.2019.00332
  • Jackson, T. N. W., Young, B., Underwood, G., McCarthy, C. J., Kochva, E., Vidal, N., Weerd, L. V. D., Nabuurs, R., Dobson, J., Whitehead, D., Vonk, F. J., Hendrikx, I., Hay, C., & Fry, B. G. (2017). Endless form most beautiful: The evolution of ophidian oral glands, including the venom system, and the use of appropriate terminology for homologous structures. Zoomorphology, 136, 107–130. https://doi.org/10.1007/s00435-016-0332-9
  • Kardong, K. V. (2002). Colubrid snakes and Duvernoy’s “venom” glands. Journal of Toxicology: Toxin Reviews, 21, 1–19. https://doi.org/10.1081/TXR-120004739
  • Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108
  • Kiernan, J. A. (2015). Histological and histochemical methods – Theory and practice (5th ed.). Scion Publishing Ltd.
  • Kochva, E. (1963). Development of the venom gland and trigeminal muscles in Vipera palaestinae. Cells Tissues Organs, 52, 49–89. https://doi.org/10.1159/000142338
  • Kochva, E. (1978). Oral glands of the reptilia. In C. K. Gans & A. Gans (Eds.), Biology of the Reptilia (Vol. 8, pp. 43–162). Academic Press.
  • Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701. https://doi.org/10.1093/molbev/mss020
  • Laporta-Ferreira, I. L., & Salomão, M. G. (1991). Morphology, physiology and toxicology of the oral glands of a tropical cochleophagous snake, Sibynomorphus neuwiedi (Colubridae – Dipsadinae). Zoologischer Anzeiger, 27, 198–208.
  • Lima, A. C., & Prudente, A. L. C. (2009). Morphological variation and systematics of Dipsas catesbyi (Sentzen, 1796) and Dipsas pavonina Schlegel, 1837 (Serpentes: Dipsadinae). Zootaxa, 2203, 31–48. https://doi.org/10.11646/zootaxa.2203.1.3
  • Maddison, W. P., & Maddison, D. R. (2021). Mesquite. A modular system for evolutionary analysis. Version 3.70 0. http://mesquiteproject.org/mesquite/download/installationWindows.html
  • Mason, A. J., Grazziotin, F. G., Zaher, H., Lemmon, A. R., Moriarty Lemmon, E., & Parkinson, C. L. (2019). Reticulate evolution in nuclear Middle America causes discordance in the phylogeny of palm‐pitvipers (Viperidae: Bothriechis). Journal of Biogeography, 46, 833–844. https://doi.org/10.1111/jbi.13542
  • McCarthy, C. J. (1987). Adaptations of sea snakes that eat fish eggs; with a note on the throat musculature of Aipysurus eydouxi (Gray, 1849). Journal of Natural History, 21, 1119–1128. https://doi.org/10.1080/00222938700770701
  • McCranie, J. R. (2006). A description of the first male of the colubrid snake genus Omoadiphas, with an expanded definition of the genus. Caribbean Journal of Science, 42, 267–269.
  • McDowell, S. B. (1986). The architecture of the corner of the mouth of colubroid snakes. Journal of Herpetology, 20, 353–407. https://doi.org/10.2307/1564502
  • Metscher, B. D. (2009). MicroCT for comparative morphology: Simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BioMedCentral Physiology, 9, 11. https://doi.org/10.1186/1472-6793-9-11
  • Moon, B. R., Penning, D. A., Segall, M., & Herrel, A. (2019). Feeding in snakes: Form, function, and evolution of the feeding system. In V. Bels & I. Whishaw (Eds.), Feeding in vertebrates: Evolution, morphology, behavior, biomechanics (pp. 527–574). Springer Nature.
  • Mulcahy, D. G., Beckstead, T. H., & Sites, J. W. (2011). Molecular systematics of the Leptodeirini (Colubroidea: Dipsadidae) revisited: Species-tree analyses and multi-locus data. Copeia, 2011, 407–417. https://doi.org/10.1643/CH-10-058
  • Oliveira, L., Guerra-Fuentes, R. A., & Zaher, H. (2017). Embryological evidence of a new type of seromucous labial gland in neotropical snail-eating snakes of the genus Sibynomorphus. Zoologischer Anzeiger, 266, 89–94. https://doi.org/10.1016/j.jcz.2016.09.004
  • Oliveira, L., Jared, C., Prudente, A. L. C., Zaher, H., & Antoniazzi, M. M. (2008). Oral glands in dipsadinae “goo-eater” snakes: Morphology and histochemistry of the infralabial glands in Atractus reticulatus, Dipsas indica, and Sibynomorphus mikanii. Toxicon, 51, 898–913. https://doi.org/10.1016/j.toxicon.2007.12.021
  • Oliveira, L., Prudente, A. L. C., & Zaher, H. (2014). Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology, 275, 87–99. https://doi.org/10.1002/jmor.20199
  • Oliveira, L., & Zaher, H. (2022). An overview of the morphology of oral glands in snakes. In D. J. Gower & H. Zaher (Eds.), The origin and early evolutionary origin of snakes (pp. 410–436). Cambridge University Press. https://doi.org/10.1017/9781108938891.024
  • Passos, P., Martins, A., & Pinto-Coelho, D. (2016). Population morphological variation and natural history of Atractus potschi (Serpentes: Dipsadidae) in Northeastern Brazil. South American Journal of Herpetology, 11, 188–211. https://doi.org/10.2994/SAJH-D-16-00034.1
  • Pavón-Vázquez, C. J., Canseco-Márquez, L., & Nieto-Montes de Oca, A. (2013). A new species in the Geophis dubius group (Squamata: Colubridae) from Northern Puebla. México. Herpetologica, 69, 358–370. https://doi.org/10.1655/HERPETOLOGICA-D-12-00095
  • Peters, J. A. (1960). The snakes of the subfamily Dipsadinae. Miscellaneous Publications Museum of Zoology – University of Michigan, 114, 1–224.
  • Phisalix, M. (1922). Animaux venimeux et venins (Vol. 2). Masson & Cie.
  • Pyron, R. A., Arteaga, A., Echevarria, L. Y., & Torres-Carvajal, O. (2016). A revision and key for the tribe Diaphorolepidini (Serpentes: Dipsadidae) and checklist for the genus Synophis. Zootaxa, 4171, 293–320. https://doi.org/10.11646/zootaxa.4171.2.4
  • Pyron, R. A., Burbrink, F. T., Colli, G. R., de Oca, A. N. M., Vitt, L. J., Kuczynski, C. A., & Wiens, J. J. (2011). The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Molecular Phylogenetics and Evolution, 58, 329–342. https://doi.org/10.1016/j.ympev.2010.11.006
  • Pyron, R. A., Guayasamin, J. M., Peñafiel, N., Bustamante, L., & Arteaga, A. (2015). Systematics of Nothopsini (Serpentes, Dipsadidae), with a new species of Synophis from the Pacific Andean slopes of southwestern Ecuador. ZooKeys, 541, 109–147. https://doi.org/10.3897/zookeys.541.6058
  • Rhoda, D., Polly, P. D., Raxworthy, C., & Segall, M. (2021). Morphological integration and modularity in the hyperkinetic feeding system of aquatic-foraging snakes. Evolution, 75, 56–72. https://doi.org/10.1111/evo.14130
  • Salomão, M. G., & Laporta-Ferreira, I. L. (1994). The role of secretions from the supralabial, infralabial, and Duvernoy’s glands of the slug-eating snake Sibynomorphus mikanii (Colubridae: Dipsadinae) in the immobilization of molluscan prey. Journal of Herpetology, 28, 369–371. https://doi.org/10.2307/1564537
  • Savitzky, A. H. (1974). The relationships of the Xenodontinae colubrid snakes related to Ninia [Unpublished master’s thesis]. Lawrence.
  • Savitzky, A. H. (1983). Coadapted character complexes among snakes: Fossoriality, piscivory, and durophagy. American Zoologist, 23, 397–409. https://doi.org/10.1093/icb/23.2.397
  • Shayer-Wollberg, M., & Kochva, E. (1967). Embryonic development of the venom apparatus in Causus rhombeatus (Viperidae, Ophidia). Herpetologica, 23, 249–259. https://www.jstor.org/stable/3890795
  • Sheehy, C. (2012). Phylogenetic relationships and feeding behavior of Neotropical snail-eating snakes (Dipsadinae, Dipsadini) [Doctoral dissertation, UT Arlington]. Repository Name. http://hdl.handle.net/10106/11501
  • Smith, M., & Bellairs, A. A. (1947). The head glands of snakes, with remarks on the evolution of the parotid gland and teeth of the opisthoglypha. Journal of the Linnean Society of London, Zoology, 41, 351–368. https://doi.org/10.1111/j.1096-3642.1940.tb02079.x
  • Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England), 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  • Taub, A. M. (1966). Ophidian cephalic glands. Journal of Morphology, 118, 529–542. https://doi.org/10.1002/jmor.1051180406
  • Taub, A. M. (1967). Comparative studies on Duvernoy’s gland of colubrid snakes. Bulletin of the American Museum of Natural History, 138, 1–50.
  • Underwood, G. (1997). An overview of venomous snake evolution. Symposium of the Zoological Society of London. In R. S. Thorpe, W. Wüster & A. Malhotra (Eds.) Venomous snake. Ecology, evolution and snakebite (pp. 1–13). Clarendon Press.
  • Underwood, G. (2002). On the rictal structures of some snakes. Herpetologica, 58, 1–17. https://doi.org/10.1655/0018-0831(2002)058[0001:OTRSOS]2.0.CO;2
  • Underwood, G., & Kochva, E. (1993). On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae). Zoological Journal of the Linnean Society, 107, 3–64. https://doi.org/10.1111/j.1096-3642.1993.tb01252.x
  • Vaeth, R. H., Rossman, D. A., & Shoop, W. (1985). Observations of tooth surface morphology in snakes. Journal of Herpetology, 19, 20–26. https://doi.org/10.2307/1564416
  • Vidal, N. (2002). Colubroid systematics: Evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. Journal of Toxicology: Toxin Reviews, 21, 21–41. https://doi.org/10.1081/TXR-120004740
  • Villatoro-Castañeda, M., & Ariano-Sánchez, D. (2017). Rediscovery of the Guatemalan Yellow-lipped snake, Chapinophis xanthocheilus (Serpentes: Dipsadidae), with comments on its distribution and ecology. Herpetological Review, 48, 25–28.
  • Vonk, F. J., Admiraal, J. R., Jackson, K., Reshef, R., De Bakker, M. A. G., Vanderschoot, K., Berge, I. V. D., Atten, M. V., Burgerhout, E., Beck, A., Mirtschin, P. J., Kochva, E., Witte, F., Fry, B. G., Woods, A. E., & Richardson, M. K. (2008). Evolutionary origin and development of snake fangs. Nature, 454, 630–633. https://doi.org/10.1038/nature07178
  • Weinstein, S. A., Smith, T. L., & Kardong, K. (2010). Reptile venom glands form, function, and future. In S. P. Mackessy (Ed.), Handbook of venoms and toxin of reptiles (pp. 65–91). CRC Taylor & Francis.
  • Wilson, L. D., & Townsend, J. H. (2007). A checklist and key to the snakes of the genus Geophis (Squamata: Colubridae: Dipsadinae), with commentary on distribution and conservation. Zootaxa, 1395, 1–31. https://doi.org/10.11646/zootaxa.1395.1.1
  • Zaher, H. (1994). Comments on the evolution of the jaw adductor musculature of snakes. Zoological Journal of the Linnean Society, 111, 339–384. https://doi.org/10.1111/j.1096-3642.1994.tb01488.x
  • Zaher, H., Grazziotin, F. G., Cadle, J. E., Murphy, R. W., Moura-Leite, J. C., & Bonatto, S. L. (2009). Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American xenodontines: A revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, 49, 1–153. https://doi.org/10.1590/S0031-10492009001100001
  • Zaher, H., Mohabey, D. M., Grazziotin, F. G., Jeffrey, A., & Mantilla, W. (in press). The skull of Sanajeh indicus, a Cretaceous snake with an upper temporal bar, and the origin of ophidian wide-gaped feeding. Zoological Journal of the Linnean Society, zlac001. https://doi.org/10.1093/zoolinnean/zlac001
  • Zaher, H., Murphy, R. W., Arredondo, J. C., Graboski, R., Machado-Filho, P. R., Mahlow, K., Montingelli, G. G., Quadros, A. B., Orlov, N. L., Wilkinson, M., Zhang, Y. P., & Grazziotin, F. G. (2019). Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). Public Library of Science One, 14, e0216148. https://doi.org/10.1371/journal.pone.0216148
  • Zaher, H., Oliveira, L., Grazziotin, F. G., Campagner, M., Jared, C., Antoniazzi, M. M., & Prudente, A. L. (2014). Consuming viscous prey: A novel protein-secreting delivery system in Neotropical snail-eating snakes. BioMedCentral Evolutionary Biology, 14, 58. https://doi.org/10.1186/1471-2148-14-58
  • Zaher, H., Yánez-Muñoz, M. H., Rodrigues, M. T., Graboski, R., Machado, F. A., Altamirano-Benavides, M., Bonatto, S. L., & Grazziotin, F. G. (2018). Origin and hidden diversity within the poorly known Galapagos snake radiation (Serpentes: Dipsadidae). Systematics and Biodiversity, 16, 614–642. https://doi.org/10.1080/14772000.2018.1478910

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.