Early evolution of the venom system in lizards and snakes (original) (raw)

References

  1. Kochva, E. in Biology of the Reptilia Vol 8 (eds Gans, S. K. & Gans, C.) 43–162 (Academic, London, 1978)
    Google Scholar
  2. Vidal, N. Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. J. Toxicol. Toxin Rev. 21, 21–41 (2002)
    Article Google Scholar
  3. Vidal, N. & Hedges, S. B. Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. C. R. Biol. 325, 987–995 (2002)
    Article CAS Google Scholar
  4. Fry, B. G. et al. Isolation of a neurotoxin (alpha-colubritoxin) from a ‘non-venomous’ colubrid: evidence for early origin of venom in snakes. J. Mol. Evol. 57, 446–452 (2003)
    Article ADS CAS Google Scholar
  5. Fry, B. G. et al. LC/MS (liquid chromatography, mass spectrometry) analysis of Colubroidea snake venoms: evolutionary and toxinological implications. Rapid Commun. Mass Spectrom. 17, 2047–2062 (2003)
    Article ADS CAS Google Scholar
  6. Kochva, E. Development of the venom gland and trigeminal muscles in Vipera palaestinae. Acta Anat. 52, 49–89 (1963)
    Article Google Scholar
  7. Kochva, E. The development of the venom gland in the opisthoglyph snake Telescopus fallax with remarks on Thamnophis sirtalis (Colubridae, Reptilia). Copeia 2, 147–154 (1965)
    Article Google Scholar
  8. Kochva, E. The origin of snakes and evolution of the venom apparatus. Toxicon 25, 65–106 (1987)
    Article CAS Google Scholar
  9. Kochva, E. Atractaspis (Serpentes, Atractaspididae) the Burrowing Asp; a multidisciplinary minireview. Bull. Nat. Hist. Mus. Lond. Zool. 68, 91–99 (2002)
    Google Scholar
  10. Underwood, G. & Kochva, E. On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae). Zool. J. Linn. Soc. 107, 3–64 (1993)
    Article Google Scholar
  11. Underwood, G. in Venomous Snakes: Ecology, Evolution and Snakebite (eds Thorpe, R. S., Wüster, W. & Malhotra, A.) 1–13 (Symp. Zool. Soc. Lond. no. 70, Clarendon, Oxford, 1997)
    Google Scholar
  12. Jackson, K. The evolution of venom-delivery systems in snakes. Zool. J. Linn. Soc. 137, 337–354 (2003)
    Article Google Scholar
  13. Fry, B. G. & Wüster, W. Assembling an arsenal: Origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences. Mol. Biol. Evol. 21, 870–883 (2004)
    Article CAS Google Scholar
  14. Vidal, N. & Hedges, S. B. Molecular evidence for a terrestrial origin of snakes. Proc. R. Soc. Lond. B Suppl. 271, S226–S229 (2004)
    Article CAS Google Scholar
  15. Townsend, T. M., Larson, A., Louis, E. & Macey, J. R. Molecular phylogenetics of Squamata: The position of snakes, Amphisbaenians, and Dibamids, and the root of the squamate tree. Syst. Biol. 53, 735–757 (2004)
    Article Google Scholar
  16. Gabe, M. & Saint Girons, H. Données histologiques sur les glandes salivaires des lépidosauriens. Mém. Mus. Natl Hist. Nat. Paris 58, 1–118 (1969)
    Google Scholar
  17. Gabe, M. & Saint Girons, H. in Toxins of Animal and Plant Origin (eds de Vries, A. & Kochva, E.) 65–68 (Gordon & Breach, London, 1971)
    Google Scholar
  18. Gygax, P. Entwicklung, Bau und Funktion der Giftdruse (Duvernoy's gland) von Natrix tessellata. Acta Trop. Zool. 28, 225–274 (1971)
    Google Scholar
  19. 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 Res. 15, 403–420 (2005)
    Article CAS Google Scholar
  20. Fry, B. G. et al. Molecular evolution of elapid snake venom three finger toxins. J. Mol. Evol. 57, 110–129 (2003)
    Article ADS CAS Google Scholar
  21. Huang, T. F. & Chiang, H. S. Effect on human platelet aggregation of phospholipase A2 purified from Heloderma horridum (beaded lizard) venom. Biochim. Biophys. Acta 1211, 61–68 (1994)
    Article CAS Google Scholar
  22. Fry, B. G. et al. Electrospray liquid chromatography/mass spectrometry fingerprinting of Acanthophis (death adder) venoms: taxonomic and toxinological implications. Rapid Commun. Mass Spectrom. 16, 600–608 (2002)
    Article ADS CAS Google Scholar
  23. Fry, B. G. et al. Novel natriuretic peptides from the venom of the inland taipan (Oxyuranus microlepidotus): Isolation, chemical and biological characterization. Biochem. Biophys. Res. Commun. 327, 1011–1015 (2005)
    Article CAS Google Scholar
  24. Sopiev, O., Makeev, B. M., Kudryavtsev, S. B. & Makarov, A. N. A case of intoxication by a bite of the gray monitor (Varanus griseus). Izv. Akad. Nauk Turkm. SSR. Ser. Biol. Nauk 87, 78 (1987)
    Google Scholar
  25. Gorelov, Y. U. K. About the toxicity of the saliva of the gray monitor. Izv. Akad. Nauk Turkm. SSR. Ser. Biol. Nauk 71, 74 (1971)
    Google Scholar
  26. Pregill, G. K., Gauthier, J. A. & Greene, H. W. The evolution of Helodermatid squamates, with description of a new taxon and an overview of Varanoidea. Trans. San Diego Soc. Nat. Hist. 21, 167–202 (1986)
    Google Scholar
  27. Norell, M. A., McKenna, M. C. & Novacek, M. J. Estesia mongoliensis, a new fossil varanoid from the Late Cretaceous Barun Goyot Formation of Mongolia. Am. Mus. Novit. 3045, 1–24 (1992)
    Google Scholar
  28. Evans, S. E. At the feet of the dinosaurs: the origin, evolution and early diversification of squamate reptiles (Lepidosauria: Diapsida). Biol. Rev. Cambr. 78, 513–551 (2003)
    Article Google Scholar
  29. Guex, N. & Peitsch, M. C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714–2723 (1997)
    Article CAS Google Scholar
  30. Koradi, R., Billeter, M. & Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14(1M), 51–55 (1996)
    Article CAS Google Scholar

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Acknowledgements

We thank the following persons and institutions who helped us or contributed tissue samples used in this study: A. Fry, Alice Springs Reptile Centre, Australian Reptile Park, M. A. G. de Bakker, R. L. Bezy, B. Branch, J. Campbell, N. Clemann, C. Clemente, C. Cicero, K. Daoues, A. S. Delmas, B. Demeter, J. Haberfield, A. Hassanin, Healesville Sanctuary, M. Hird, Louisiana State University Museum of Zoology, P. Moler, T. Moncuit, P. Moret, National Museum of Natural History Naturalis Leiden (J. W. Arntzen), T. Pappenfus, J.-C. Rage, C. Skliris, J. Smith, S. Sweet, Ultimate Reptiles (South Australia), University of California Museum of Vertebrate Zoology (Berkeley), J. Walker, R. Waters, J. Weigel and B. Wilson. We also thank A. Webb and T. Purcell for providing HPLC access; N. Williamson for help with preliminary mass spectrometry characterization; E. V. Grishin for help in obtaining the references in Russian; S. Edwards for comments; and T. van Wagner and V. Wexler for artwork. This work was funded by the Service de Systématique moléculaire of the Muséum National d'Histoire Naturelle, Institut de Systématique (N.V.) and by grants from the Australian Academy of Science (B.G.F.), Australian Geographic Society (B.G.F.), Australia & Pacific Science Foundation (B.G.F.), Australian Research Council (B.G.F.), CASS Foundation (B.G.F.), Commonwealth of Australia Department of Health and Aging (B.G.F.), Ian Potter Foundation (B.G.F.), International Human Frontiers Science Program Organisation (B.G.F.), Leiden University (F.J.V., M.K.R.), NASA Astrobiology Institute (S.B.H.), National Science Foundation (S.B.H.) and University of Melbourne (B.G.F.). We thank the relevant wildlife departments for granting the scientific permits for field collection of required specimens.

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Authors and Affiliations

  1. Australian Venom Research Unit, Level 8, School of Medicine, University of Melbourne, Victoria, 3010, Parkville, Australia
    Bryan G. Fry & S. F. Ryan Ramjan
  2. Population and Evolutionary Genetics Unit, Museum Victoria, GPO Box 666E, Victoria, 3001, Melbourne, Australia
    Bryan G. Fry & Janette A. Norman
  3. Department of Biology and Astrobiology Research Center, 208 Mueller Lab, Pennsylvania State University, University Park, Pennsylvania, 16802-5301, USA
    Nicolas Vidal & S. Blair Hedges
  4. UMS 602, Taxonomie et collections, Reptiles-Amphibiens, Département Systématique et Évolution, Muséum National d'Histoire Naturelle, 25 Rue Cuvier, 75005, Paris, France
    Nicolas Vidal
  5. Institute of Biology, Leiden University, Kaiserstraat 63, PO Box 9516, 2300 RA, Leiden, The Netherlands
    Freek J. Vonk & Michael K. Richardson
  6. Department of Structural Biology and Bioinformatics, University of Geneva and Swiss Institute of Bioinformatics, Centre Médical Universitaire, 1 Rue Michel-Servet, 1211 4, Geneva, Switzerland
    Holger Scheib
  7. SBC Lab AG, Seebüelstrasse 26, 8185, Winkel, Switzerland
    Holger Scheib
  8. Monash Venom Group, Department of Pharmacology, Monash University, Clayton, 3800, Victoria, Australia
    Sanjaya Kuruppu & Wayne. C. Hodgson
  9. Molecular and Health Technologies, CSIRO, 343 Royal Parade, Victoria, 3010, Parkville, Australia
    Kim Fung
  10. Department of Pathology, University of Melbourne, Victoria, 3010, Parkville, Australia
    Vera Ignjatovic & Robyn Summerhayes
  11. Murdoch Children's Research Institute, Royal Children's Hospital, Flemington Road, Victoria, 3052, Parkville, Australia
    Vera Ignjatovic & Robyn Summerhayes
  12. Department of Zoology, Tel Aviv University, 69978, Tel Aviv, Israel
    Elazar Kochva

Authors

  1. Bryan G. Fry
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  2. Nicolas Vidal
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  3. Janette A. Norman
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  4. Freek J. Vonk
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  5. Holger Scheib
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  6. S. F. Ryan Ramjan
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  7. Sanjaya Kuruppu
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  8. Kim Fung
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  9. S. Blair Hedges
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  10. Michael K. Richardson
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  11. Wayne. C. Hodgson
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  12. Vera Ignjatovic
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  13. Robyn Summerhayes
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  14. Elazar Kochva
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Corresponding author

Correspondence toBryan G. Fry.

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Competing interests

The sequences of the cDNA clones have been deposited in GenBank (accession numbers DQ139877–DQ139931 and DQ184481), as have the nuclear gene sequences (DQ119594–DQ119641). Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains 13 Supplementary Figures, including the molecular phylogenetic analysis of squamate nuclear genes, the phylogenetic analyses and sequence alignments of the toxin types analysed in this study as well as the liquid chromatography-mass spectrometry analysis of Varanus varius (Lace monitor) venom. (PDF 1238 kb)

Supplementary Methods

This file contains detailed descriptions of materials and methods not already described in the main article. (DOC 52 kb)

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Fry, B., Vidal, N., Norman, J. et al. Early evolution of the venom system in lizards and snakes.Nature 439, 584–588 (2006). https://doi.org/10.1038/nature04328

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