Endless forms most beautiful: the evolution of ophidian oral glands, including the venom system, and the use of appropriate terminology for homologous structures

Abstract

The differentiated serous-secreting dental glands of caenophidian snakes are diverse in form despite their developmental homology. This variation makes the elucidation of their evolutionary history a complex task. In addition, some authors identify as many as ten discrete types/subtypes of ophidian oral gland. Over the past decade and a half, molecular systematics and toxinology have deepened our understanding of the evolution of these fascinating and occasionally enigmatic structures. This paper includes a comprehensive examination of ophidian oral gland structure and (where possible) function, as well as new data on rictal glands and their associated anatomy. Following this, appropriate use of terminology, especially that pertaining to homologous structures (including the controversial “venom gland” vs “Duvernoy’s gland” debate), is considered. An interpretation of the evolutionary history of the ophidian venom system, drawing on recent results from molecular systematics, toxinology and palaeontology, concludes the paper.

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References

  1. Alcock A, Rogers L (1902) On the toxic properties of the saliva of certain ‘non poisonous’ colubrines. Proc R Soc of London 70:446–454

    Article  Google Scholar 

  2. Arlinghaus et al (2015) Lectin peptides (TV-lectin). In: Fry BG (ed) Venomous reptiles and their toxins: evolution, pathophysiology and biodiscovery. Oxford University Press, Oxford

    Google Scholar 

  3. Burns B, Pickwell GV (1972) Cephalic glands in sea snakes (Pelamis, Hydrophis and Laticauda). Copeia 3:547–559. doi:10.2307/1442929

    Article  Google Scholar 

  4. Calvete JJ, Ghezellou P, Paiva O, Matainaho T, Ghassempour A, Goudarzi H, Kraus F, Sanz L, Williams DJ (2012) Snake venomics of two poorly known Hydrophiinae: comparative proteomics of the venoms of terrestrial Toxicocalamus longissimus and marine Hydrophis cyanocinctus. J Proteomics 75(13):4091–4101. doi:10.1016/j.jprot.2012.05.026

    CAS  Article  PubMed  Google Scholar 

  5. Cundall D (1995) Feeding behaviour in Cylindrophis and its bearing on the evolution of alethinophidian snakes. J Zool 237(3):353–376. doi:10.1111/j.1469-7998.1995.tb02767.x

    Article  Google Scholar 

  6. Currie AM (2014) Venomous dinosaurs and rear-fanged snakes: homology and homoplasy characterized. Erkenntnis 79(3):701–727. doi:10.1007/s10670-013-9533-5

    Article  Google Scholar 

  7. de Oliveira L, Jared C, da Costa Prudente AL, Zaher H, Antoniazzi MM (2008) Oral glands in dipsadine “goo-eater” snakes: morphology and histochemistry of the infralabial glands in Atractus reticulatus, Dipsas indica, and Sibynomorphus mikanii. Toxicon 51(5):898–913. doi:10.1016/j.toxicon.2007.12.021

    Article  PubMed  Google Scholar 

  8. Dennett DC (1995) Darwin’s dangerous idea: evolution and the meanings of life. Simon & Schuster, New York

    Google Scholar 

  9. Dunson W, Dunson M (1973) Convergent evolution of sublingual salt glands in the marine file snake and the true sea snakes. J Comp Physiol 86(3):193–208. doi:10.1007/BF00696339

    CAS  Article  Google Scholar 

  10. Dunson WA, Dunson MK (1979) A possible new salt gland in a marine homalopsid snake (Cerberus rhynchops). Copeia 4:661–672. doi:10.2307/1443875

    Article  Google Scholar 

  11. Dunson WA, Packer RK, Dunson MK (1971) Sea snakes: an unusual salt gland under the tongue. Science 173(3995):437–441. doi:10.1126/science.173.3995.437

    CAS  Article  PubMed  Google Scholar 

  12. Fry BG, Vidal N, Norman JA, Vonk FJ, Scheib H, Ramjan SFR, Kuruppu S, Fung K, Hedges SB, Richardson MK, Hodgson WC, Ignjatovic V, Summerhayes R, Kochva E (2006) Early evolution of the venom system in lizards and snakes. Nature 439(7076):584–588. doi:10.1038/nature04328

    CAS  Article  PubMed  Google Scholar 

  13. Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SFR, Vidal N, Poelmann RE, Norman JA (2008) Evolution of an arsenal. Mol Cell Proteomics 7(2):215–246. doi:10.1074/mcp.M700094-MCP200

    CAS  Article  PubMed  Google Scholar 

  14. Fry BG, Roelants K, Norman J, King G, Tyndal J, Lewis R, Norton R, Renjifo C, Rodriguez de la Vega RC (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genom Hum Genet 10:483–511

    CAS  Article  Google Scholar 

  15. Fry BG, Winter K, Norman JA, Roelants K, Nabuurs RJA, van Osch MJP, Teeuwisse WM, van Der Weerd L, McNaughtan JE, Kwok HF, Scheib H, Greisman L, Kochva E, Miller LJ, Gao F, Karas J, Scanlon D, Lin F, Kuruppu S, Shaw C, Wong L, Hodgson WC (2010) Functional and structural diversification of the Anguimorpha lizard venom system. Mol Cell Proteomics 9(11):2369. doi:10.1074/mcp.M110.001370

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Fry BG, Casewell NR, Wuester W, Vidal N, Young B, Jackson TNW (2012) The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 60(4):434–448. doi:10.1016/j.toxicon.2012.02.013

    CAS  Article  PubMed  Google Scholar 

  17. Fry BG, Undheim EAB, Ali SA, Jackson TNW, Debono J, Scheib H, Ruder T, Morgenstern D, Cadwallader L, Whitehead D, Nabuurs R, van der Weerd L, Vidal N, Roelants K, Hendrikx I, Gonzalez SP, Koludarov I, Jones A, King GF, Antunes A, Sunagar K (2013) Squeezers and leaf-cutters: differential diversification and degeneration of the venom system in toxicoferan reptiles. Mol Cell Proteomics 12(7):1881–1899. doi:10.1074/mcp.M112.023143

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Fry BG, Sunagar K, Casewell NR, Kochva E, Roelants K, Scheib H, Wüster W, Vidal N, Young B, Burbrink F, Pyron RA, Vonk FJ, Jackson TNW (2015) The origin and evolution of the Toxicofera reptile venom system. In: Fry BG (ed) Venomous reptiles and their toxins: evolution, pathophysiology and biodiscovery. Oxford University Press, New York, pp 1–31

    Google Scholar 

  19. Gans C (1978) Reptilian venoms: some evolutionary considerations. In: Gans C, Gans, Kyoko A (eds) Biology of the Reptilia. Volume 8. Physiology B. Academic Press, London

    Google Scholar 

  20. Gavrilets S (2008) Evolutionary ecology: fitness landscapes. In: Jorgensen SE, Fath B (eds) Encyclopedia of ecology. Elsevier, Amsterdam

    Google Scholar 

  21. Godfrey-Smith P (1994) A modern history theory of functions. Noûs 28(3):344–362

    Article  Google Scholar 

  22. Gopalakrishnakone P, Kochva E (1990a) Unusual aspects of the venom apparatus of the blue coral snake, Maticora bivirgata. Arch Histol Cytol 53(2):199

    CAS  Article  PubMed  Google Scholar 

  23. Gopalakrishnakone P, Kochva E (1990b) Venom glands and some associated muscles in sea-snakes. J Morphol 205(1):85–96. doi:10.1002/jmor.1052050109

    Article  Google Scholar 

  24. Gould SJ, Vrba ES (1982) Exaptation; a missing term in the science of form. Paleobiology 8(1):4–15

    Article  Google Scholar 

  25. Haas G (1964) Anatomical observations on the head of Liotyphlops albirostris (Typhlopidae, Ophidia). Acta Zool 45(1–2):1–62. doi:10.1111/j.1463-6395.1964.tb00709.x

    Article  Google Scholar 

  26. Haas G (1968) Anatomical observations on the head of Anomalepis aspinosus (Typhlopidae, Ophidia). Acta Zool 49(1–2):63–139. doi:10.1111/j.1463-6395.1968.tb00147.x

    Article  Google Scholar 

  27. Hifumi T, Sakai A, Yamamoto A, Murakawa M, Ato M, Shibayama K, Ginnaga A, Kato H, Koido Y, Inoue J, Abe Y, Kawakita K, Hagiike M, Kuroda Y (2014) Clinical characteristics of yamakagashi (Rhabdophis tigrinus) bites: a national survey in Japan, 2000–2013. J Intensive Care 2(1):19. doi:10.1186/2052-0492-2-19

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hsiang AY, Field DJ, Webster TH, Behlke ADB, Davis MB, Racicot RA, Gauthier JA (2015) The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evol Biol 15:87

    Article  PubMed  PubMed Central  Google Scholar 

  29. Jackson K (2003) The evolution of venom-delivery systems in snakes. Zool J Linn Soc 137(3):337–354. doi:10.1046/j.1096-3642.2003.00052.x

    Article  Google Scholar 

  30. Jackson TN, Fry BG (2016) A tricky trait: applying the fruits of the “function debate” in the philosophy of biology to the “venom debate” in the science of toxinology. Toxins 8:263

    Article  PubMed Central  Google Scholar 

  31. Jackson TNW, Casewell NR, Fry BG (2013a) Response to “Replies to Fry et al. (Toxicon 2012, 60/4, 434–448). Part A. Analyses of squamate reptile oral glands and their products: a call for caution in formal assignment of terminology designating biological function. Toxicon 64:106–112. doi:10.1016/j.toxicon.2012.11.006

    CAS  Article  PubMed  Google Scholar 

  32. Jackson TNW, Casewell NR, Fry BG (2013b) Response to “Replies to Fry et al. (Toxicon 2012, 60/4, 434-448). Part B. Analyses of squamate reptile oral glands and their products: a call for caution in formal assignment of terminology designating biological function”. Toxicon 64:113–115. doi:10.1016/j.toxicon.2012.12.023

    CAS  Article  PubMed  Google Scholar 

  33. Kardong KV (2012) Replies to Fry et al. (Toxicon 2012, 60/4, 434-448). Part B. Properties and biological roles of squamate oral products: the “venomous lifestyle” and preadaptation. Toxicon 60(5):964. doi:10.1016/j.toxicon.2012.06.001

    CAS  Article  PubMed  Google Scholar 

  34. Kelly CMR, Barker NP, Villet MH, Broadley DG (2009) Phylogeny, biogeography and classification of the snake superfamily Elapoidea: a rapid radiation in the late Eocene. Cladistics 25(1):38–63. doi:10.1111/j.1096-0031.2008.00237.x

    Article  Google Scholar 

  35. Kelly CMR, Branch WR, Broadley DG, Barker NP, Villet MH (2011) Molecular systematics of the African snake family Lamprophiidae Fitzinger, 1843 (Serpentes: Elapoidea), with particular focus on the genera Lamprophis Fitzinger 1843 and Mehelya Csiki 1903. Mol Phylogenet Evol 58(3):415–426. doi:10.1016/j.ympev.2010.11.010

    CAS  Article  PubMed  Google Scholar 

  36. Kiernan JA (1999) Histological and histochemical methods: theory and practice, 3rd edn. Butterworth Heinemann, Oxford

    Google Scholar 

  37. Kochva ET (1958) The head muscles of Vipera palaestinae and their relation to the venom gland. J Morphol 102(1):23–53. doi:10.1002/jmor.1051020103

    Article  Google Scholar 

  38. Kochva E (1962) On the lateral jaw musculature of the solenoglypha with remarks on some other snakes. J Morphol 110(2):227–284. doi:10.1002/jmor.1051100209

    Article  Google Scholar 

  39. Kochva E (1965) The development of the venom gland in the opisthoglyph snake, Telescopus fallax, with remarks on Thamnophis sirtalis (Colubridae, Reptilia). Copeia 1965:147–154

    Article  Google Scholar 

  40. Kochva E (1978) Oral glands of the reptilia. In: Gans C, Gans, Kyoko A (eds) Biology of the Reptilia. Volume 8. Physiology B. Academic Press, London

    Google Scholar 

  41. Kochva E (1987) The origin of snakes and evolution of the venom apparatus. Toxicon 25(1):65–106. doi:10.1016/0041-0101(87)90150-4

    CAS  Article  PubMed  Google Scholar 

  42. Kochva E, Gans C (1965) The venom gland of Vipera palestinae with comments on the glands of some other viperines. Cells Tissues Organs 62(3):365–401

    Article  Google Scholar 

  43. Kochva E, Gans C (1970) Salivary glands of snakes. Clin Toxicol 3(3):363–387. doi:10.3109/15563657008990115

    CAS  Article  PubMed  Google Scholar 

  44. Kochva E, Shayer-Wollberg M, Sobol R (1967) The special pattern of the venom gland in Atractaspis and its bearing on the taxonomic status of the genus. Copeia 4:763–772. doi:10.2307/1441887

    Article  Google Scholar 

  45. Laporta-Ferreira LI, Salomão DGM (1991) Morphology, physiology and toxicology of the oral glands of a tropical cochleophagous snake, Sibynomorphus neuwiedi (Colubridae-Dipsadinae), 227(3–4). Fischer, Jena, ALLEMAGNE

  46. Lee MSY, Hugall AF, Lawson R, Scanlon JD (2007) Phylogeny of snakes (Serpentes): combining morphological and molecular data in likelihood, Bayesian and parsimony analyses. Syst Biodivers 5(4):371–389. doi:10.1017/S1477200007002290

    Article  Google Scholar 

  47. Lillywhite HB (1996) Husbandry of the little file snake, Acrochordus granulatus. Zoo Biol 15(3):315–327

    Article  Google Scholar 

  48. Luna LG (1968) Manual of histological staining methods of the armed forces institute of pathology, 3rd edn. McGraw-Hill Book Company, New York

    Google Scholar 

  49. Mackessy SP (1991) Morphology and ultrastructure of the venom glands of the northern pacific rattlesnake Crotalus viridis oreganus. J Morphol 208(1):109–128. doi:10.1002/jmor.1052080106

    Article  Google Scholar 

  50. Mackessy SP, Baxter LM (2006) Bioweapons synthesis and storage: the venom gland of front-fanged snakes. Zoologischer Anzeiger A J Comp Zool 245(3–4):147–159. doi:10.1016/j.jcz.2006.01.003

    Article  Google Scholar 

  51. Marques V Oa, Sazima Ivan (2008) Winding to and fro: constriction in the snake Anilius scytale, vol 103. British Herpetological Society, London

    Google Scholar 

  52. McDowell SB (1968) Affinities of the snakes usually called Elaps lacteus and E. dorsalis. J Linn Soc Lond Zool 47(313):561–578. doi:10.1111/j.1096-3642.1968.tb00550h.x

    Article  Google Scholar 

  53. McDowell SB (1969) Toxicocalamus, a New Guinea genus of snakes of the family Elapidae. J Zool 159(4):443–511. doi:10.1111/j.1469-7998.1969.tb03900.x

    Article  Google Scholar 

  54. McDowell SB (1986) The Architecture of the Corner of the Mouth of Colubroid Snakes. Journal of Herpetology 20(3):353–407

    Article  Google Scholar 

  55. Mebs D (1978) Pharmacology of reptilian venoms. In: Gans C, Gans, Kyoko A (eds) Biology of the Reptilia. Volume 8. Physiology B. Academic Press, London

    Google Scholar 

  56. Millikan RG (1989) In defense of proper functions. Philos Sci 56(2):288–302. doi:10.1086/289488

    Article  Google Scholar 

  57. O’Shea M, Parker F, Kaiser H (2015) A new species of New Guinea worm-eating snake, genus Toxicocalamus (Serpentes: Elapidae), from the Star Mountains of Western Province, Papua New Guinea, with a revised dichotomous key to the genus. Bull Mus Comp Zool 161(6):241–264. doi:10.3099/0027-4100-161.6.241

    Article  Google Scholar 

  58. Phisalix M (1922) Animaux Venimeux et VENINS, vol II. Masson, Paris

    Google Scholar 

  59. Phisalix M, Caius R (1918) L’extension de la fonction venimeuse dans l’ordre entiè re des ophidiens et son existence chez des familles ou elle n’avait pas été soupçonnée jusqu’içi. Journal de Physiologie et de Pathologie Générale 17:923–964

    Google Scholar 

  60. Pyron RA, Burbrink FT, Colli GR, de Oca ANM, Vitt LJ, Kuczynski CA, Wiens JJ (2011) The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58(2):329–342. doi:10.1016/j.ympev.2010.11.006

    Article  PubMed  Google Scholar 

  61. Sakai F, Carneiro SM, Yamanouye N (2012) Morphological study of accessory gland of Bothrops jararaca and its secretory cycle. Toxicon 59(3):393–401. doi:10.1016/j.toxicon.2011.12.012

    CAS  Article  PubMed  Google Scholar 

  62. Salomão M, Laporta-Ferreira IL (1994) The role of secretions from the supralabial, infralabial, and duvernoy's glands of the slug-eating snake Sibynomorphus mikani (Colubridae: Dipsadinae) in the immobilization of molluscan prey. J Herpetol 28(3):369–371. doi:10.2307/1564537

    Article  Google Scholar 

  63. Shine R, Schwaner T (1985) Prey constriction by venomous snakes: a review, and new data on Australian species. Copeia 4:1067–1071. doi:10.2307/1445266

    Article  Google Scholar 

  64. Shine R, Keogh JS (1996) Food habits and reproductive biology of the endemic melanesian elapids: are tropical snakes really different? J Herpetol 30(2):238–247. doi:10.2307/1565515

    Article  Google Scholar 

  65. Shivik JA (2006) Are vultures birds, and do snakes have venom, because of macro- and microscavenger conflict? Bioscience 56(10):819–823. doi:10.1641/0006-3568(2006)56[819:AVBADS]2.0.CO;2

    Article  Google Scholar 

  66. Simões BF, Sampaio FL, Jared C, Antoniazzi MM, Loew ER, Bowmaker JK, Rodriguez A, Hart NS, Hunt DM, Partridge JC, Gower DJ (2015) Visual system evolution and the nature of the ancestral snake. J Evol Biol 28(7):1309–1320

    Article  PubMed  Google Scholar 

  67. Slowinski JB, Boundy J, Lawson R (2001) The phylogenetic relationships of Asian coral snakes (Elapidae: Calliophis and Maticora) based on morphological and molecular characters. Herpetologica 57(2):233–245

    Google Scholar 

  68. Smeets RE, Melman PG, Hoffmann JJ, Mulder AW (1991) Severe coagulopathy after a bite from a ‘harmless’ snake (Rhabdophis subminiatus). J Intern Med 230(4):351

    CAS  Article  PubMed  Google Scholar 

  69. Streicher JW, Wiens JJ (2016) Phylogenomic analyses reveal novel relationships among snake families. Mol Phylogenet Evol 100:160–169

    Article  PubMed  Google Scholar 

  70. Stuebing RB, Inger RF (1993) Field guide to the snakes of Borneo. Natural History Publications (Borneo), Malaysia

    Google Scholar 

  71. Taub AM (1966) Ophidian cephalic glands. J Morphol 118(4):529–541. doi:10.1002/jmor.1051180406

    CAS  Article  PubMed  Google Scholar 

  72. Taub AM (1967) Comparative histological studies on Duvernoy’s gland of colubrid snakes. Bulletin of the AMNH; v. 138, article 1. American Museum of Natural History, New York

  73. Teynie A, David P, Lottier A, Le MD, Vidal N, Nguyen TQ (2015) A new genus and species of xenodermatid snake (Squamata: Caenophidia: Xenodermatidae) from northern Lao People’s Democratic Republic. Zootaxa 3926(1):523–540. doi:10.11646/zootaxa.3926.4.4

    Article  PubMed  Google Scholar 

  74. Underwood G (1997) An overview of venomous snake evolution. In: Thorpe RS, Wüster W, Malhotra A (eds) Venomous snakes: ecology, evolution and snakebite, Symposia of the Zoological Society of London, No 70. Clarendon Press, Oxford, pp 1–13

  75. Underwood G (2002) On the rictal structures of some snakes. Herpetologica 58(1):1–17. doi:10.1655/0018-0831(2002)058[0001:OTRSOS]2.0.CO;2

    Article  Google Scholar 

  76. Underwood G, Kochva E (1993) On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae). Zool J Linn Soc 107(1):3–64. doi:10.1006/zjls.1993.1002

    Article  Google Scholar 

  77. Vidal N (2002) Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. J Toxicol Toxin Rev 21(1–2):21–41. doi:10.1081/TXR-120004740

    Article  Google Scholar 

  78. Vidal N, David P (2004) New insights into the early history of snakes inferred from two nuclear genes. Mol Phylogenet Evol 31(2):783–787. doi:10.1016/j.ympev.2004.01.001

    CAS  Article  PubMed  Google Scholar 

  79. Vidal N, Hedges SB (2005) The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. CR Biol 328:1000–1008

    CAS  Article  Google Scholar 

  80. Vidal N, Delmas AS, David P, Cruaud C, Couloux A, Hedges SB (2007a) The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. CR Biol 330:182–187

    CAS  Article  Google Scholar 

  81. Vidal N, Delmas AS, Hedges SB (2007b) The higher-level relationships of alethinophidian snakes inferred from seven nuclear and mitochondrial genes. In: Henderson RW, Powell R (eds) Biology of the boas and pythons, vol 1. Eagle Mountain Publ, Eagle Montain, pp 27–33

    Google Scholar 

  82. Vidal N, Branch WR, Pauwels OSG, Hedges SB, Broadley DG, Wink M, Cruaud C, Joger U, Nagy ZT (2008) Dissecting the major African snake radiation: a molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia). Zootaxa 1945:51–66

    Google Scholar 

  83. Vidal N, Rage J-C, Couloux A, Hedges SB (2009) Snakes (Serpentes). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 390–397

    Google Scholar 

  84. Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MAG, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, Mirtschin PJ, Kochva E, Witte F, Fry BG, Woods AE, Richardson MK (2008) Evolutionary origin and development of snake fangs. Nature 454(7204):630–633

    CAS  Article  PubMed  Google Scholar 

  85. Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ, McCleary RJR, Kerkkamp HME, Vos RA, Guerreiro I, Calvete JJ, Wüster W, Woods AE, Logan JM, Harrison RA, Castoe TA, de Koning APJ, Pollock DD, Yandell M, Calderon D, Renjifo C, Currier RB, Salgado D, Pla D, Sanz L, Hyder AS, Ribeiro JMC, Arntzen JW, van den Thillart GEEJM, Boetzer M, Pirovano W, Dirks RP, Spaink HP, Duboule D, McGlinn E, Kini M, Richardson MK (2013) The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci USA 110(51):20651–20656. doi:10.1073/pnas.1314702110

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. Wang G, He S, Huang S, He M, Zhao E (2009) The complete mitochondrial DNA sequence and the phylogenetic position of Achalinus meiguensis (Reptilia: Squamata). Chin Sci Bull 54(10):1713–1724. doi:10.1007/s11434-009-0160-0

    CAS  Google Scholar 

  87. Webb JK, Shine R (1993) Dietary habits of Australian Blindsnakes (Typhlopidae). Copeia 3:762–770

    Article  Google Scholar 

  88. Weinstein SA (2011) “Venomous” bites from non-venomous snakes: a critical analysis of risk and management of “colubrid” snake bites. Elsevier, Waltham

    Google Scholar 

  89. Weinstein SA (2015) Snake venoms: A brief treatise on etymology, origins of terminology, and definitions. Toxicon 103:188–195. doi:10.1016/j.toxicon.2015.07.005

    CAS  Article  PubMed  Google Scholar 

  90. Weinstein SA, Keyler DE, White J (2012) Replies to Fry et al. (Toxicon 2012, 60/4, 434-448). Part A. Analyses of squamate reptile oral glands and their products: a call for caution in formal assignment of terminology designating biological function. Toxicon 60(5):954. doi:10.1016/j.toxicon.2012.05.006

    CAS  Article  PubMed  Google Scholar 

  91. Wollberg M, Kochva E, Underwood G (1998) On the rictal glands of some atractaspid snakes. Herpetol J 8:137–143

    Google Scholar 

  92. Yang DC, Deuis JR, Dashevsky D, Dobson J, Jackson TNW, Brust A, Xie B, Koludarov I, Debono J, Hendrikx I, Hodgson WC, Josh P, Nouwens A, Baillie GJ, Bruxner TJC, Alewood PF, Peng KLK, Frank N, Vetter I, Fry BG (2016) The snake with the scorpion’s sting: novel three-finger toxin sodium channel agonists from the venom of the long-glanded blue coral snake. Toxins 8(10):303. doi:10.3390/toxins8100303

    Article  PubMed Central  Google Scholar 

  93. Zaher H, de Oliveira L, Grazziotin F, Campagner M, Jared C, Antoniazzi M, Prudente A (2014) Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evol Biol 14:58. doi:10.1186/1471-2148-14-58

    Article  PubMed  PubMed Central  Google Scholar 

  94. Zheng Y, Wiens JJ (2016) Combining phylogenomics and supermatrix approaches, and a time-calibrated phylogeny for squamates reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol 94:537–557

    Article  PubMed  Google Scholar 

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Acknowledgements

This paper is dedicated to the memory of Garth Underwood. TNJ was funded by a UQ PhD Scholarship and BGF was funded by the Australian Research Council. We thank Thomas Oerther and Dieter Gross for their MRI help.

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Correspondence to Bryan G. Fry.

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This paper complied with the relevant legislation surrounding animal use, and all work was done on previously collected, preserved specimens in collections, and thus, animal ethics approval was not needed.

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Jackson, T.N.W., Young, B., Underwood, G. et al. 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 (2017). https://doi.org/10.1007/s00435-016-0332-9

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Keywords

  • Snake
  • Venom
  • Evolution
  • Anatomy
  • Terminology
  • Function