Comparative morphology of oral glands in snakes of the family Homalopsidae reveals substantial variation and additional independent origins of salt glands within Serpentes.
diceCT
non-front-fanged snakes
premaxillary glands
salt excretion
sublingual glands
venom glands
Journal
Journal of anatomy
ISSN: 1469-7580
Titre abrégé: J Anat
Pays: England
ID NLM: 0137162
Informations de publication
Date de publication:
18 Jan 2024
18 Jan 2024
Historique:
revised:
24
11
2023
received:
25
08
2023
accepted:
29
12
2023
medline:
18
1
2024
pubmed:
18
1
2024
entrez:
18
1
2024
Statut:
aheadofprint
Résumé
Using diffusible iodine-based contrast-enhanced computed tomography (diceCT), we examined the morphology of the oral glands of 12 species of the family Homalopsidae. Snakes of this family exhibit substantial interspecific morphological variation in their oral glands. Particular variables are the venom glands, ranging from large (e.g., Subsessor bocourti) to small (e.g., Erpeton tentaculatum). The supra- and infralabial glands are more uniform in morphology, being the second most developed in almost all the sampled species. Premaxillary glands distinct from the supralabial glands were observed in five species (Myron richardsonii, Bitia hydroides, Cantoria violacea, Fordonia leucobalia, and Gerarda prevostiana), in addition to Cerberus rynchops, the only species in which this condition was previously documented associated with the excretion of salt. In the three species of the saltwater group of homalopsids (C. violacea, F. leucobalia, and G. prevostiana), the premaxillary glands also extend posteriorly, occupying a large area above the supralabial gland, a condition not observed in any other species of snake studied thus far. Character evolution analyses indicate that premaxillary glands differentiated from the supralabial gland and evolved independently three or four times in the family, always in lineages that invaded marine habitats. Our results suggest that the differentiated premaxillary glands are likely salt glands, as is the case in C. rynchops. If corroborated, this increases to six or seven the number of independent evolutionary origins of salt glands in snakes that have undergone an evolutionary transition to marine life.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : H2020 Marie Sklodowska-Curie Actions
ID : 101024700
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : FAPESP 2017/25089-5
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : FAPESP 2018/09301-7
Informations de copyright
© 2024 Anatomical Society.
Références
Alfaro, M.E., Karns, D.R., Voris, H.K., Brock, C.D. & Stuart, B.L. (2008) Phylogeny, evolutionary history, and biogeography of oriental-Australian rear-fanged water snakes (Colubroidea: Homalopsidae) inferred from mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 46, 576-593. Available from: https://doi.org/10.1016/j.ympev.2007.10.024
Babonis, L.S. & Brischoux, F. (2012) Perspectives on the convergent evolution of tetrapod salt glands. Integrative and Comparative Biology, 52, 245-256. Available from: https://doi.org/10.1093/icb/ics073
Babonis, L.S. & Evans, D.H. (2011) Morphological and biochemical evidence for the evolution of salt glands in snakes. Comparative Biochemistry and Physiology, Part A, 160, 400-411. Available from: https://doi.org/10.1016/j.cbpa.2011.07.008
Babonis, L.S., Hyndman, K.A., Lillywhite, H.B. & Evans, D.H. (2009) Immunolocalization of Na+/K+-ATPase and Na+/K+/2Cl− cotransporter in the tubular epithelia of sea snake salt glands. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 154(4), 535-540. Available from: https://doi.org/10.1016/j.cbpa.2009.08.022
Bernstein, J.M., de Souza, H.F., Murphy, J.C., Voris, H.K., Brown, R.M., Myers, E.A. et al. (2023) Phylogenomics of fresh and formalin specimens resolves the systematics of Old World mud snakes (Serpentes: Homalopsidae) and expands biogeographic inference. Bulletin of the Society of Systematic Biology, 2(1), 1-24. Available from: https://doi.org/10.18061/bssb.v2i1.9393
Bernstein, J.M., Murphy, J.C., Voris, H.K., Brown, R.M. & Ruane, S. (2021) Phylogenetics of mud snakes (Squamata: Serpentes: Homalopsidae): a paradox of both undescribed diversity and taxonomic inflation. Molecular Phylogenetics and Evolution, 160, 107109. Available from: https://doi.org/10.1016/j.ympev.2021.107109
Brischoux, F., Tingley, R., Shine, R. & Lillywhite, H.B. (2012) Salinity influences the distribution of marine snakes: implications for evolutionary transition to marine life. Ecography, 35, 994-1003. Available from: https://doi.org/10.1111/j.1600-0587.2012.07717.x
Burns, B. & Pickwell, G.V. (1972) Cephalic glands in sea snakes (Pelamis, Hydrophis and, cephalic glands in sea snakes (pelamis, Hydrophis and Laticauda) Laticauda). Copeia, 1972, 547, 559. Available from: https://doi.org/10.2307/1442929
Callahan, S., Crowe-Riddell, J.M., Nagesan, R.S., Gray, J.A. & Rabosky, A.R.D. (2021) A guide for optimal iodine staining and high throughput diceCT scanning in snakes. Ecology and Evolution, 22, 11587-11603. Available from: https://doi.org/10.1002/ece3.7467
Deepak, V., Cooper, N., Poyarkov, N.A., Kraus, F., Burin, G., Das, A. et al. (2022) Multilocus phylogeny, natural-history traits, and classification of natricine (Serpentes: Natricinae) snakes. Zoological Journal of the Linnean Society, 195, 279-298. Available from: https://doi.org/10.1093/zoolinnean/zlab099
Dunson, W.A. & Dunson, M.K. (1973) Convergent evolution of sublingual salt glands in the marine file snake and true sea snakes. Journal of Comparative Physiology, 86, 193-208. Available from: https://doi.org/10.1007/BF00696339
Dunson, W.A. & Dunson, M.K. (1979) Possible new salt gland in a marine Homalopsid snake (Cerberus rynchops). Copeia, 1979, 661-672. Available from: https://doi.org/10.2307/1443875
Dunson, W.A. & Mazzotti, F.J. (1989) Salinity as a limiting factor in the distribution of reptiles in Florida Bay: a theory for the estuarine origin of marine snakes and turtles. Bulletin of Marine Science, 44, 229-244.
Dunson, W.A., Packer, R.K. & Dunson, M.K. (1971) Sea snakes: an unusual salt gland under the tongue. Science, 173, 437-441. Available from: https://doi.org/10.1126/science.173.3995.437
Edwards, S.L. & Marshall, W.S. (2012) Principles and patterns of osmoregulation and euryhalinity in fishes. Fish Physiology, 32, 1-44. Academic Press. Available from: https://doi.org/10.1016/B978-0-12-396951-4.00001-3
Fabre, A.C., Bickford, D., Segall, M. & Herrel, A. (2016) The impact of diet, habitat use, and behaviour on head shape evolution in homalopsid snakes. Biological Journal of the Linnean Society, 118, 634-647. Available from: https://doi.org/10.1111/bij.12753
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. Available from: 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. et al. (2008) Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular & Cellular Proteomics, 7(2), 215-246. Available from: https://doi.org/10.1074/mcp.M700094-MCP200
Gabe, M. & Saint-Girons, H. (1969) Données histologiques sur les glandes salivaires des lépidosauriens. Memoires du Museum National d'Histoire Naturelle, 58, 3-116.
Gignac, P.M., Kley, N.J., Clarke, J.A., Colbert, M.W., Morhardt, A.C., Cerio, D. et al. (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy, 228, 889-909. Available from: https://doi.org/10.1111/joa.12449
Gripshover, N.D. & Jayne, B.C. (2023) Using natricine snakes to test how prey type and size affect predatory behaviors and performance. Frontiers in Behavioral Neuroscience, 17, 1134131. Available from: https://doi.org/10.3389/fnbeh.2023.1134131
Jackson, T.N.W., Jouanne, H. & Vidal, N. (2019) Snake venom in context: neglected clades and concepts. Frontiers in Ecology and Evolution, 332, 1-9. Available from: https://doi.org/10.3389/fevo.2019.00332
Jackson, T.N.W., Young, B., Underwood, G., McCarthy, C.J., Kochva, E., Vidal, N. et al. (2017) Endless forms 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. Available from: https://doi.org/10.1007/s00435-016-0332-9
Jayne, B.C., Voris, H.K. & Heang, K.B. (1988) Diet, feeding behavior, growth, and numbers of a population of Cerberus rynchops (Serpentes: Homalopsinae) in Malaysia. Fieldiana Zoology, 50, 1-15. Available from: https://doi.org/10.5962/bhl.title.2872
Jayne, B.C., Voris, H.K. & Ng, P.K.L. (2002) Snake circumvents constraints, Snake circumvents constraints on prey size on prey size. Nature, 418(6894), 143. Available from: https://doi.org/10.1038/418143a
Jayne, B.C., Voris, H.K. & Ng, P.K.L. (2018) How big is too big? Using crustacean-eating snakes (Homalopsidae) to test how anatomy and behavior affect prey size and feeding performance. Biological Journal of the Linnean Society, 123, 636-650. Available from: https://doi.org/10.1093/biolinnean/bly007
Kardong, K.V. (2002) Colubrid snakes and Duvernoy's ‘venom’ glands. Journal of Toxicology - Toxin Reviews, 21, 1-19. Available from: https://doi.org/10.1081/TXR-120004739
Kochva, E. (1978) Oral glands of the Reptilia. In: Gans, C.K. & Gans, A. (Eds.) Biology of the Reptilia, Vol. 8. London, New York: Academic Press, pp. 43-162.
Kochva, E. (1987) The origin of snakes and evolution of the venom apparatus. Toxicon, 25, 65-106. Available from: https://doi.org/10.1016/0041-0101(87)90150-4
Kochva, E. & Gans, C. (1970) Salivary glands of snakes. Clinical Toxicology, 3, 363-387. Available from: https://doi.org/10.3109/15563657008990115
Kopstein, F. (1931) Herpetologische Notizen IV von Dr. Felix Kopstein Fordonia leucobalia Schegel und Cerberus rhynchops Schneider. Treubia, 13(1), 1-14.
Kumar, B., Sanders, K.L., George, S. & Murphy, J. (2012) The status of Eurostus dussumierii and Hypsirhina chinensis (Reptilia, Squamata, Serpentes): with comments on the origin of salt tolerance in homalopsid snakes. Systematics and Biodiversity, 10(4), 479-489. Available from: https://doi.org/10.1080/14772000.2012.751940
Mackessy, S.P. (2022) Venom production and secretion in reptiles. Journal of Experimental Biology, 225, jeb227348. Available from: https://doi.org/10.1242/jeb.227348
Maddison, W.P. & Maddison, D.R. (2021) Mesquite. A modular system for evolutionary analysis. Version 3.70. https://www.mesquiteproject.org/Installation.html
McNamara, J.C. & Freire, C.A. (2022) Strategies of invertebrate osmoregulation: an evolutionary blueprint for transmuting into fresh water from the sea. Integrative and Comparative Biology, 62, 376-387. Available from: https://doi.org/10.1093/icb/icac081
Metscher, B.D. (2009) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse nonmineralized animal tissues. BMC Physiology, 9(1), 1-14. Available from: https://doi.org/10.1186/1472-6793-9-11
Mori, A. (1998) Prey-handling behavior of three species of homalopsine snakes: features associated with piscivory and Duvernoy's gland. Journal of Herpetology, 32, 40-50. Available from: https://doi.org/10.2307/1565477
Murphy, J.C. (2007) Homalopsid snakes: evolution in the mud. Malabar, Florida: Krieger Publishing Company.
Murphy, J.C. & Voris, H.K. (2014) A checklist and key to the homalopsid snakes (Reptilia, Squamata, Serpentes), with the description of New Genera. Fieldiana Life and Earth Sciences, 8, 1-43. Available from: https://doi.org/10.3158/2158-5520-14.8.1
Oliveira, L., Grazziotin, F.G., Sánchez-Martínez, P.M., Sasa, M., Flores-Villela, O., Prudente, A.L.C. et al. (2023) Phylogenetic and morphological evidence reveals the association between diet and the evolution of the venom delivery system in neotropical goo-eating snakes. Systematics and Biodiversity, 21(1), 2153944. Available from: https://doi.org/10.1080/14772000.2022.2153944
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. Available from: https://doi.org/10.1002/jmor.20199
Oliveira, L. & Zaher, H. (2022) An overview of the morphology of oral glands in snakes. In: Gower, D.J. & Zaher, H. (Eds.) The origin and early evolutionary origin of snakes. Cambridge: Cambridge University Press, pp. 410-436. Available from: https://doi.org/10.1017/9781108938891.024
Palci, A., Seymour, R.S., Nguyen, C.N., Hutchinson, M.N., Lee, M.S.Y. & Sanders, K.L. (2019) Novel vascular plexus in the head of a sea snake (Elapidae, Hydrophiinae) revealed by high-resolution computed tomography and histology. Royal Society Open Science, 6, 191099. Available from: https://doi.org/10.1098/rsos.191099
Rasmussen, A.R., Murphy, J.C., Ompi, M., Gibbons, J.W. & Uetz, P. (2011) Marine reptiles. PLoS One, 6(11), e27373. Available from: https://doi.org/10.1371/journal.pone.0027373
Rossman, D.A. (1963) Relationships and taxonomic status of the north American, relationships and taxonomic status of the north American Natricine Snake genera Liodytes, Regina, and Clonophis natricine snake genera Liodytes, Regina, and Clonophis. Occasional Papers of the Museum of Natural Science, Louisiana State University, 29, 1-29. Available from: https://doi.org/10.31390/opmns.029
Saint-Girons, H. (1989) Les glandes céphaliques exocrines des Reptiles. II. - Considérations fonctionnelles et évolutives. Annales Des Sciences Naturelles, Zoologie, 10, 1-17.
Sakar, S.C. (1922) A comparative study of the buccal glands and teeth of the opisthoglypha, and a discussion on the evolution of the order from aglypha. Proceedings of the Zoological Society of London, 93, 295-322. Available from: https://doi.org/10.1111/j.1096-3642.1923.tb02188.x
Savitzky, A.H. (1983) Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist, 23(2), 397-409. Available from: https://doi.org/10.1093/icb/23.2.397
Shock, B.C., Foran, C.M. & Stueckle, T.A. (2009) Effects of salinity stress on survival, metabolism, limb regeneration, and ecdysis in Uca pugnax. Journal of Crustacean Biology, 29, 293-301. Available from: https://doi.org/10.1651/08-2990.1
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. Zoological Journal of the Linnean Society, 41, 351-368. Available from: https://doi.org/10.1111/j.1096-3642.1940.tb02079.x
Taub, A.M. (1966) Ophidian cephalic glands. Journal of Morphology, 118, 529-542. Available from: 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.
Tucker, A.S. & Miletich, I. (2010) Salivary glands: developed, adaptation and disease. Basel: Karger, p. 150.
Tumlison, R. & Roberts, K.G. (2018) Prey-handling behavior in the Gulf crayfish snake. Herpetological Conservation and Biology, 13(3), 617-621.
Uetz, P., Freed, P., Aguilar, R. & Hošek, J. (2023) The Reptile Database. http://www.reptile-database.org
Underwood, G. (1997) An overview of venomous snake evolution. In: Thorpe, R.S., Wüster, W. & Malhotra, A. (Eds.) Venomous snakes. Ecology, evolution and snakebite, n. 70. Oxford: Clarendon Press, pp. 1-13.
Underwood, G. (2002) On the rictal structures of some snakes. Herpetologica, 58(1), 1-17. Available from: https://doi.org/10.1655/0018-0831(2002)058[0001:OTRSOS]2.0.CO;2
Vidal, N. (2002) Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. Journal of Toxinology: Toxin Review, 21, 21-41. Available from: https://doi.org/10.1081/TXR-120004740
Voris, H.K. & Murphy, J.C. (2002) The prey and predators of Homalopsine snakes. Journal of Natural History, 36, 1621-1632. Available from: https://doi.org/10.1080/00222930110062642
Waters, R.M. (2000) Feeding behavior of crayfish snakes (Regina): allometry, ontogeny and adaptations to an extremely specialized diet. Ph.D. Dissertation, University of Tennessee, Knoxville, Tennessee, USA. 165 p.
Weinstein, S.A., Warrell, D.A., White, J. & Keyler, D.E. (2011) ‘Venomous’ bites from non-venomous snakes: a critical analysis of risk and management of ‘colubrid’ snake bites. Waltham, MA: Elsevier.
Weinstein, S.A., Smith, T.L. & Kardong, K. (2010) Reptile venom glands: form, function, and future. In: Mackessy, S.P. (Ed.) CRC handbook of reptile venoms and toxins. Boca Raton: Taylor Francis, pp. 65-91.
Zaher, H., Murphy, R.W., Arredondo, J.C., Graboski, R., Machado-Filho, P.R., Mahlow, K. et al. (2019) Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS One, 15, 1-82. Available from: https://doi.org/10.1371/journal.pone.0216148
Zaher, H., Oliveira, L., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, M.M. et al. (2014) Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BioMed Central Evolutionary Biology, 14, 58. Available from: https://doi.org/10.1186/1471-2148-14-58