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12 - Origin and Early Diversification of the Enigmatic Squamate Venom Cocktail

from Part III - Genomic Perspectives

Published online by Cambridge University Press:  30 July 2022

By
Vivek Suranse ,
Ashwin Iyer ,
Timothy N. W. Jackson  and
Kartik Sunagar
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
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Summary

Venom, a specialized form of poison, is actively injected by the venomous organism into its target animal to facilitate several quotidian functions. Over a hundred convergent origins of this remarkable functional trait, along with intricate mechanisms of venom delivery, have been documented across animals. Pinpointing the emergence of venom in squamate reptiles has important implications for understanding the evolutionary history of snakes, but it has been challenging. Several competing hypotheses have been put forth to explain the evolutionary origin of squamate venom, including assertions of single, dual and multiple origins. In this chapter, in addition to a summary of this ongoing dialogue, we provide an overview of ecology, composition, delivery mechanisms, and evolutionary models that explain the possible origin and diversification of venom in squamate reptiles.

Keywords

snakeslizardsevolutionvenomicsfangsadaptationvenom glandstranscriptomicsgenomicsToxicofera
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 248 - 268
Publisher: Cambridge University Press
Print publication year: 2022

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References

Schendel, V., Rash, L. D., Jenner, R. A., and Undheim, E. A. B., The diversity of venom: the importance of behavior and venom system morphology in understanding its ecology and evolution. Toxins (Basel), 11 (2019), 666.Google Scholar
Fry, B. G., Roelants, K., Champagne, D. E., et al., The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annual Review of Genomics and Human Genetics, 10 (2009), 483–511.Google Scholar
Fry, B. G., From genome to ‘venome’: molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Research, 15 (2005), 403–420.Google Scholar
Fry, B. G., Scheib, H., van der Weerd, L., et al., Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular and Cellular Proteomics, 7 (2008), 215–46.CrossRefGoogle ScholarPubMed
Fry, B. G., Vidal, N., van der Weerd, L., Kochva, E., and Renjifo, C., Evolution and diversification of the Toxicofera reptile venom system. Journal of Proteomics, 72 (2009), 127–136.Google Scholar
Vidal, N. and Hedges, S. B.. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. Comptes Rendus Biologies, 328 (2005), 1000–1008.CrossRefGoogle ScholarPubMed
Kochva, E., Oral glands of the Reptilia. Biology of the Reptilia. 8 (1978), 43–162.Google Scholar
Pough, F. H., Andrews, R. M., Cadle, J. E., et al., Herpetology 3rd edn. (New Jersey: Prentice Hall, 2004).Google Scholar
Kardong, K. V., Weinstein, S. A., and Smith, T. L., Reptile venom glands: form, function, and future. In Mackessy, S. P., ed., Handbook of Venoms and Toxins of Reptiles (Boca Raton, FL: CRC Press, 2009), pp. 65–91.CrossRefGoogle Scholar
Burbrink, F. T., Grazziotin, F. G., Pyron, R. A., et al. Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology, 69 (2020), 502–520.CrossRefGoogle ScholarPubMed
Daltry, J. C., Wüster, W., and Thorpe, R. S., Diet and snake venom evolution. Nature, 379 (1996), 537–40.Google Scholar
Gibbs, H. L., Sanz, L., Chiucchi, J. E., Farrell, T. M., and Calvete, J. J., Proteomic analysis of ontogenetic and diet-related changes in venom composition of juvenile and adult Dusky Pigmy rattlesnakes (Sistrurus miliarius barbouri). Journal of Proteomics, 74 (2011), 2169–2179.CrossRefGoogle ScholarPubMed
Zancolli, G., Calvete, J. J., Cardwell, M. D., et al., When one phenotype is not enough: divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species. Proceedings of the Royal Society B, 286 (2019), 20182735.Google ScholarPubMed
Casewell, N. R., Jackson, T. N. W., Laustsen, A. H., and Sunagar, K., Causes and Consequences of Snake Venom Variation. Trends in Pharmacological Sciences, 41 (2020), 570–581.Google Scholar
Jackson, T. N. W., Jouanne, H., and Vidal, N., Snake venom in context: Neglected clades and concepts. Frontiers in Ecology and Evolution, 7 (2019), 332.Google Scholar
Modica, M. V., Sunagar, K., Holford, M., and Dutertre, S.,. Diversity and evolution of animal venoms: Neglected targets, ecological iInteractions, future perspectives. Frontiers in Ecology and Evolution, 8 (2020), 65.CrossRefGoogle Scholar
Cardoso, F. C., Ferraz, C. R., Arrahman, A., et al., Multifunctional toxins in snake venoms and therapeutic implications: from pain to hemorrhage and necrosis. Frontiers in Ecology and Evolution, 7 (2019), 218.Google Scholar
Casewell, N. R., Harrison, R. A., Wüster, W., and Wagstaff, S. C., Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics, 10 (2009), 564.Google Scholar
Currier, R. B., Harrison, R. A., Rowley, P. D., Laing, G. D., and Wagstaff, S. C., Intra-specific variation in venom of the African Puff Adder (Bitis arietans): Differential expression and activity of snake venom metalloproteinases (SVMPs). Toxicon, 55 (2010), 864–873.Google Scholar
Senji Laxme, R. R., Khochare, S., de Souza, H. F., et al., Beyond the ‘big four’: Venom profiling of the medically important yet neglected Indian snakes reveals disturbing antivenom deficiencies. PLoS Neglected Tropical Diseases, 13 (2019), e0007899.Google Scholar
Sunagar, K., Undheim, E. A., Scheib, H., et al., Intraspecific venom variation in the medically significant Southern Pacific Rattlesnake (Crotalus oreganus helleri): biodiscovery, clinical and evolutionary implications. Journal of Proteomics, 99 (2014), 68–83.Google Scholar
Jackson, T. N., Koludarov, I., Ali, S. A., et al., Rapid radiations and the race to redundancy: An investigation of the evolution of Australian elapid snake venoms. Toxins (Basel), 8 (2016), 309.Google Scholar
Mackessy, S. P., Williams, K., and Ashton, K. G., Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: a case of venom paedomorphosis? Copeia, 2003 (2003), 769–782.CrossRefGoogle Scholar
Rokyta, D. R., Margres, M. J., Ward, M. J., and Sanchez, E. E., The genetics of venom ontogeny in the eastern diamondback rattlesnake (Crotalus adamanteus). PeerJ, 5 (2017), e3249.Google Scholar
Sanz, L., Gibbs, H. L., Mackessy, S. P., and Calvete, J. J., Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. Journal of Proteome Research. 5 (2006), 2098–2112.Google Scholar
Barlow, A., Pook, C. E., Harrison, R. A., and Wüster, W., Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proceedings of the Royal Society B, 276 (2009), 2443–2449.Google Scholar
Mackessy, S. P., Sixberry, N. M., Heyborne, W. H., and Fritts, T., Venom of the Brown Treesnake, Boiga irregularis: ontogenetic shifts and taxa-specific toxicity. Toxicon, 47 (2006), 537–548.Google Scholar
Li, M., Fry, B. G., and Kini, R. M., Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). Journal of Molecular Evolution, 60 (2005), 81–89.Google Scholar
Durban, J., Perez, A., Sanz, L., et al., Integrated ‘omics’ profiling indicates that miRNAs are modulators of the ontogenetic venom composition shift in the Central American rattlesnake, Crotalus simus simus. BMC Genomics, 14 (2013), 234.Google Scholar
Ujvari, B., Casewell, N. R., Sunagar, K., et al., Widespread convergence in toxin resistance by predictable molecular evolution. Proceedings of the National Academy of Sciences of the USA, 112 (2015), 11911–11916.Google Scholar
Rowe, A. H., Xiao, Y., Rowe, M. P., Cummins, T. R., and Zakon, H. H., Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin. Science, 342 (2013), 441–446.Google Scholar
Holding, M. L., Drabeck, D. H., Jansa, S. A., and Gibbs, H. L., Venom resistance as a model for understanding the molecular basis of complex coevolutionary adaptations. Integrative and Comparative Biology, 56 (2016), 1032–1043.Google Scholar
Biardi, J. E., Chien, D. C., and Coss, R. G.. California ground squirrel (Spermophilus beecheyi) defenses against rattlesnake venom digestive and hemostatic toxins. Journal of Chemical Ecology, 32 (2006), 137–154.Google Scholar
Jansa, S. A. and Voss, R. S., Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS One, 6 (2011), e20997.Google Scholar
Holding, M. L., Biardi, J. E., and Gibbs, H. L., Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey. Proceedings of the Royal Society B, 283 (2016), 20152841.Google Scholar
Barchan, D., Kachalsky, S., Neumann, D., et al., How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proceedings of the National Academy of Sciences of the USA, 89 (1992), 7717–7721.Google Scholar
Drabeck, D. H., Dean, A. M., and Jansa, S. A.. Why the honey badger don’t care: Convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites. Toxicon, 99 (2015), 68–72.Google Scholar
Sunagar, K., Casewell, N., Varma, S., et al., Deadly innovations: unraveling the molecular evolution of animal venoms. In Gopalakrishnakone, P. and Calvete, J. J., eds., Venom Genomics and Proteomics (Dordrecht: Springer, 2014), pp. 1–23.Google Scholar
Sunagar, K. and Moran, Y.. The rise and fall of an evolutionary innovation: Contrasting strategies of venom evolution in ancient and young animals. PLoS Genetics, 11 (2015), e1005596.Google Scholar
Girish, K. S., Jagadeesha, D. K., Rajeev, K. B., and Kemparaju, K.. Snake venom hyaluronidase: an evidence for isoforms and extracellular matrix degradation. Molecular and Cellular Biochemistry, 240 (2002), 105–110.Google Scholar
Tu, A. T. and Hendon, R. R., Characterization of lizard venom hyaluronidase and evidence for its action as a spreading factor. Comparative Biochemistry and Physiology B, 76 (1983), 377–383.Google Scholar
Katkar, G. D., Sundaram, M. S., NaveenKumar, S. K., et al., NETosis and lack of DNase activity are key factors in Echis carinatus venom-induced tissue destruction. Nature Communications, 7 (2016), 11361.Google Scholar
Lu, Q., Clemetson, J. M., and Clemetson, K. J.. Snake venoms and hemostasis. Journal of Thrombosis and Haemostasis, 3 (2005), 1791–1799.Google Scholar
Xiong, S. and Huang, C.. Synergistic strategies of predominant toxins in snake venoms. Toxicology Letters, 287 (2018), 142–154.Google Scholar
Modahl, C. M. and Mackessy, S. P., Venoms of rear-fanged snakes: New proteins and novel activities. Frontiers in Ecology and Evolution, 7 (2019), 279.Google Scholar
Tasoulis, T. and Isbister, G. K., A review and database of snake venom proteomes. Toxins (Basel), 9 (2017), 9.CrossRefGoogle ScholarPubMed
Fry, B. G., Undheim, E. A., Ali, S. A, et al., Squeezers and leaf-cutters: differential diversification and degeneration of the venom system in toxicoferan reptiles. Molecular and Cellular Proteomics, 12 (2013), 1881–1899.Google Scholar
Sunagar, K., Jackson, T. N., Undheim, E. A., et al., Three-fingered RAVERs: Rapid Accumulation of Variations in Exposed Residues of snake venom toxins. Toxins (Basel), 5 (2013), 2172–2208.CrossRefGoogle ScholarPubMed
Jackson, T. N., 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 (2017), 107–130.Google Scholar
Sanggaard, K. W., Dyrlund, T. F., Thomsen, L. R., et al., Characterization of the gila monster (Heloderma suspectum suspectum) venom proteome. Journal of Proteomics, 117 (2015), 1–11.CrossRefGoogle ScholarPubMed
Yap, M. K. K. and Misuan, N., Exendin-4 from Heloderma suspectum venom: From discovery to its latest application as type II diabetes combatant. Basic & Clinical Pharmacology & Toxicology, 124 (2019), 513–527.Google Scholar
Kochva, E.. The origin of snakes and evolution of the venom apparatus. Toxicon, 25 (1987), 65–106.Google Scholar
Auffenberg, W.. The Behavioral Ecology of the Komodo Monitor (Gainsville, FL: University Presses of Florida, 1981).Google Scholar
Fry, B. G., Wroe, S., Teeuwisse, W., et al., A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus . Proceedings of the National Academy of Sciences of the USA, 106 (2009), 8969–8974.Google Scholar
Koludarov, I., Jackson, T. N., op den Brouw, B., et al., Enter the dragon: The dynamic and multifunctional evolution of Anguimorpha lizard venoms. Toxins (Basel), 9 (2017), 242.Google Scholar
Fry, B. G., Vidal, N., Norman, J. A., et al., Early evolution of the venom system in lizards and snakes. Nature, 439 (2006), 584–588.Google Scholar
Nei, M., Gu, X., and Sitnikova, T., Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Sciences of the USA, 94 (1997), 7799–7806.Google Scholar
Fry, B. G., Wüster, W., Kini, R. M., et al., Molecular evolution and phylogeny of elapid snake venom three-finger toxins. Journal of Molecular Evolution, 57 (2003), 110–129.Google Scholar
Casewell, N. R., Wagstaff, S. C., Harrison, R. A., Renjifo, C., and Wüster, W., Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin genes. Molecular Biology and Evolution, 28 (2011), 2637–2649.CrossRefGoogle ScholarPubMed
Suryamohan, K., Krishnankutty, S. P., Guillory, J., et al., The Indian cobra reference genome and transcriptome enables comprehensive identification of venom toxins. Nature Genetics, 52 (2020), 106–117.Google Scholar
Brown, D. D., Wensink, P. C., and Jordan, E., A comparison of the ribosomal DNA’s of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. Journal of Molecular Biology, 63 (1972), 57–73.Google Scholar
Moran, Y., Weinberger, H., Sullivan, J. C., et al., Concerted evolution of sea anemone neurotoxin genes is revealed through analysis of the Nematostella vectensis genome. Molecular Biology and Evolution, 25 (2008), 737–747.Google Scholar
Brust, A., Sunagar, K., Undheim, E. A. B., et al., Differential evolution and neofunctionalization of snake venom metalloprotease domains. Molecular and Cellular Proteomics, 12 (2013), 651–663.Google Scholar
Kordis, D. and Gubensek, F., Adaptive evolution of animal toxin multigene families. Gene, 261 (2000), 43–52.Google Scholar
Casewell, N. R., Wüster, W., Vonk, F. J., Harrison, R. A., and Fry, B. G.. Complex cocktails: the evolutionary novelty of venoms. Trends in Ecology and Evolution, 28 (2013), 219–229.Google Scholar
Hargreaves, A. D., Swain, M. T., Hegarty, M. J., Logan, D. W., and Mulley, J. F., Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biology and Evolution, 6 (2014), 2088–2095.Google Scholar
Reyes-Velasco, J., Card, D. C., Andrew, A. L., et al., Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Molecular Biology and Evolution, 32 (2015), 173–183.Google Scholar
Lei, Q., Li, C., Zuo, Z., et al., Evolutionary Insights into RNA trans-Splicing in Vertebrates. Genome Biology and Evolution, 8 (2016), 562–577.CrossRefGoogle ScholarPubMed
Ogawa, T., Oda-Ueda, N., Hisata, K., et al., Alternative mRNA splicing in three venom families underlying a possible production of divergent venom proteins of the Habu Snake, Protobothrops flavoviridis. Toxins (Basel), 11 (2019), 581.Google Scholar
Cousin, X., Bon, S., Massoulie, J., and Bon, C., Identification of a novel type of alternatively spliced exon from the acetylcholinesterase gene of Bungarus fasciatus. Molecular forms of acetylcholinesterase in the snake liver and muscle. Journal of Biological Chemistry, 273 (1998), 9812–9820.CrossRefGoogle ScholarPubMed
Fry, B. G., Winter, K., Norman, J. A., et al., Functional and structural diversification of the Anguimorpha lizard venom system. Molecular and Cellular Proteomics, 9 (2010), 2369–2390.CrossRefGoogle ScholarPubMed
Lynch, V. J., Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evolutionary Biology, 7 (2007), 2.Google Scholar
Sunagar, K., Johnson, W. E., O’Brien, S. J., Vasconcelos, V., and Antunes, A., Evolution of CRISPs associated with toxicoferan-reptilian venom and mammalian reproduction. Molecular Biology and Evolution, 29 (2012), 1807–1822.Google Scholar
Jackson, K., The evolution of venom-delivery systems in snakes. Zoological Journal of the Linnean Society, 137 (2003), 337–354.Google Scholar
Koludarov, I., Jackson, T. N., Pozzi, A., and Mikheyev, A. S., Family saga: reconstructing the evolutionary history of a functionally diverse gene family reveals complexity at the genetic origins of novelty. bioRxiv, (2019), 583344.Google Scholar
Taub, A. M.. Ophidian cephalic glands. Journal of Morphology, 118 (1966), 529–542.CrossRefGoogle ScholarPubMed
Vonk, F. J., Admiraal, J. F., Jackson, K., et al., Evolutionary origin and development of snake fangs. Nature, 454 (2008), 630–633.Google Scholar
Phisalix, M. and Caius, R.. L’extension de la fonction venimeuse dans l’ordre entière 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 (1918), 923–964.Google Scholar
Fry, B. G., Casewell, N. R., Wüster, W., et al., The structural and functional diversification of the Toxicofera reptile venom system. Toxicon, 60 (2012), 434–448.Google Scholar
Jackson, T. N. and Fry, B. G., 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 (2016), 263.Google Scholar
Hargreaves, A. D., Swain, M. T., Logan, D. W., and Mulley, J. F., Testing the Toxicofera: comparative transcriptomics casts doubt on the single, early evolution of the reptile venom system. Toxicon, 92 (2014), 140–156.CrossRefGoogle ScholarPubMed
Townsend, T., Larson, A., Louis, E., and Macey, J. R.. Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Systematic Biology 53 (2004), 735–757.Google Scholar
Conesa, A., Madrigal, P., Tarazona, S., et al., A survey of best practices for RNA-seq data analysis. Genome Biology, 17 (2016), 13.Google Scholar

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