Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1666, 2009, Pages 2443-2449

  Barlow, Axel ^a   Pook, Catharine E ^a   Harrison, Robert A ^b   Wüster, Wolfgang ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

Adaptation; Coevolution; Diet; Echis; Snake venom

Indexed keywords

VIPER VENOM;

ADAPTATION; ARTHROPOD; COEVOLUTION; DIETARY SHIFT; EVOLUTIONARY BIOLOGY; MITOCHONDRION; NATURAL SELECTION; PHYLOGENY; SNAKE; STOMACH CONTENT; TOXICITY; VENOM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHROPOD; ARTICLE; CELL NUCLEUS; CHEMICAL COMPOSITION; COEVOLUTION; DIET; EVOLUTIONARY ADAPTATION; FOOD INTAKE; INTESTINE; LD 50; MITOCHONDRION; NONHUMAN; PHYLOGENY; PREY; PRIORITY JOURNAL; SCORPION; SEQUENCE ANALYSIS; SNAKE; STOMACH;

ARTHROPODA; ECHIS; SCORPIONES; VIPERINAE;

EID: 66749139721     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0048     Document Type: Article

References (42)

1. Andrade, D. V. & Abe, A. S. 1999 Relationship of venom ontogeny and diet in Bothrops. Herpetologica 55, 200-204.
2. Biardi, J. E., Chien, D. C. & Coss, R. G. 2006 California ground squirrel (Spermophilus beecheyi ) defences against rattlesnake venom digestive and hemostatic toxins. J. Chem. Ecol. 31, 2501-2518. (doi:10.1007/s10886-005- 7610-1)
3. Cherlin, V. A. 1990 Taxonomic review of the snake genus Echis (Viperidae). II. An analysis of taxonomy and descriptions of new forms. Proc. Zool. Inst. Leningrad 207, 193-223.
4. Chippaux, J. P., Williams, V. & White, J. 1991 Snake venom variability: methods of study, results and interpretation. Toxicon 29, 1279-1303. (doi:10.1016/0041-0101(91)90116-9)
5. Creer, S., Chou, W.-H., Malhotra, A. & Thorpe, R. S. 2002 Offshore insular variation in the diet of the Taiwanese bamboo viper Trimeresurus stejnegeri (Schmidt). Zool. Sci. 19, 907-931. (doi:10.2108/zsj.19.907) (Pubitemid 35358214)
6. Creer, S., Malhotra, A., Thorpe, R. S., Stocklin, R., Favreau, P. & Chou, W.-H. 2003 Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDITOF-MS) and isoelectric focusing. J. Mol. Evol. 56, 317-329. (doi:10.1007/s00239-002-2403-4)
7. Daltry, J. C., Wüster, W. & Thorpe, R. S. 1996 Diet and snake venom evolution. Nature 379, 537-540. (doi:10.1038/379537a0) (Pubitemid 26049579)
8. Gasperetti, J. 1988 The snakes of Arabia. Fauna Saudi Arabia 9, 169-450.
9. Gillissen, A., Theakston, D. J., Barth, J., May, B., Krieg, M. & Warrell, D. A. 1994 Neurotoxicity, haemostatic disturbances and haemolytic anaemia after a bite by a Tunisian saw-scaled or carpet viper (Echis 'pyramidum' complex): failure of antivenom treatment. Toxicon 32, 937-944. (doi:10.1016/0041-0101(94)90372-7) (Pubitemid 24248620)
10. Hayes, W. K., Lavin-Murcio, P. & Kardong, K. V. 1995 Northern Pacific rattlesnakes (Crotalus viridis oreganus) meter venom when feeding on prey of different sizes. Copeia 1995, 337-343. (doi:10.2307/1446896)
11. Heatwole, H. & Poran, N. S. 1995 Resistances of sympatric and allopatric eels to sea snake venoms. Copeia 1995, 136-147. (doi:10.2307/1446808)
12. Jorge da Silva Jr, N. & Aird, S. D. 2001 Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comp. Biochem. Physiol. 128, 425-456. (doi:10.1016/S1096-4959(00)00347-X)
13. Kordiš, D. & Gubenšek, F. 2000 Adaptive evolution of animal toxin multigene families. Gene 261, 43-52. (doi:10.1016/S0378-1119(00)) (Pubitemid 32106652)
14. Lenk, P., Kalyabina, S., Wink, M. & Joger, U. 2001 Evolutionary relationships among the true vipers (Reptilia: Viperidae) inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 19, 94-104. (doi:10.1006/mpev.2001.0912)
15. Li, M., Fry, B. G. & Manjunatha Kini, R. 2005 Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii ). J. Mol. Evol. 60, 81-89. (doi:10.1007/s00239-004-0138-0)
16. Lynch, V. J. 2007 Inventing an arsenal: adaptive evolution and neofunctionalisation of venom phospholipase A2 genes. BMC Evol. Biol. 7, 2. (doi:10.1186/1471-2148-7-2)
17. Mackessy, S. P. 1988 Venom ontogeny in the Pacific rattlesnakes Crotalus viridis helleri and Crotalus v. oreganus. Copeia 1988, 92-101. (doi:10.2307/1445927)
18. Mackessy, S. P., Sixberry, N. M., Heyborne, W. H. & Fritts, T. 2006 Venom of the brown tree snake, Boiga irregularis: ontogenetic shifts and taxa-specific toxicity. Toxicon 47, 537-548. (doi:10.1016/j.toxicon.2006.01.007)
19. Mallow, D., Ludwig, D. & Nilson, G. 2003 True vipers: natural history and toxinology of old world vipers. Malabar, FL: Krieger.
20. Mebs, D. 2001 Toxicity in animals. Trends in evolution? Toxicon 39, 87-96. (doi:10.1016/S0041-0101(00)00155-0)
21. McCue, M. D. 2006 Cost of producing venom in three North American pitviper species. Copeia 2006, 818-825. (doi:10.1643/0045-8511(2006)6[818: COPVIT]2.0.CO;2)
22. Nylander, J. A. A. 2004 MRMODELTEST v. 2. Uppsala, Sweden: Evolutionary Biology Centre, Uppsala University. Program distributed by the author.
23. Pawlak, J. et al. 2006 Denmotoxin, a three-finger toxin from the colubrid snake Boiga dendrophila (mangrove catsnake) with bird-specific activity. J. Biol. Chem. 281, 29 030-29 041. (doi:10.1074/jbc.M605850200)
24. Poran, N. S., Coss, R. G. & Benjamini, E. 1987 Resistance of California ground squirrels (Spermophilus beecheyi ) to the venom of the northern Pacific rattlesnake (Crotalus viridis oreganus): a study of adaptive variation. Toxicon 25, 767-777. (doi:10.1016/0041-0101(87)90127-9) (Pubitemid 18035906)
25. Prendini, L., Crowe, T. M. & Wheeler, W. C. 2003 Systematics and biogeography of the family Scorpionidae (Chelicerata: Scorpiones) with a discussion on phylogenetic methods. Invert. Systemat. 17, 185-259. (doi:10.1071/IS02016)
26. Revault, P. 1996 Ecology of Echis ocellatus and peri-urban bites in Ouagadougou. Toxicon 34, 144. (doi:10.1016/0041-0101(96)83655-5)
27. Ronquist, F. & Huelsenbeck, J. P. 2003 MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. (doi:10.1093/bioinformatics/btg180) (Pubitemid 37038874)
28. Sasa, M. 1999a Diet and snake venom evolution: can local selection alone explain intraspecifc venom variation? Toxicon 37, 249-252. (doi:10.1016/S0041- 0101(98)00121-4)
29. Sasa, M. 1999b Reply. Toxicon 37, 259-260. (doi:10.1016/S0041-0101(98) 00123-8)
30. Schaeffer Jr, R. C. 1987 Heterogeneity of Echis venoms from different sources. Toxicon 25, 1343-1346. (doi:10.1016/0041-0101(87)90012-2)
31. Shine, R., Branch, W. R., Harlow, P. S. & Webb, J. K. 1998 Reproductive biology and food habits of horned adders, Bitis caudalis (Viperidae), from southern Africa. Copeia 1998, 391-401. (doi:10.2307/1447433)
32. Starkov, V. G., Osipov, A. V. & Utkin, Y. N. 2007 Toxicity of venoms from vipers of Pelias group to crickets Gryllus assimilis and its relation to snake entomophagy. Toxicon 49, 995-1001. (doi:10.1016/j.toxicon.2007.01.010)
33. Swofford, D. L. 2002 PAUP* - phylogenetic analysis using parsimony (*and other methods) Beta version 4.0b10. Sunderland, MA: Sinauer.
34. Theakston, R. D. G. & Reid, H. A. 1983 Development of simple standard assay procedures for the characterization of snake venoms. Bull. World Health Organ. 61, 949-956.
35. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994 CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. (doi:10.1093/nar/22.22.4673)
36. Tsairi, H. & Bouskila, A. 2004 Ambush site selection of a desert snake (Echis coloratus) at an oasis. Herpetologica 60, 13-23. (doi:10.1655/20-47) (Pubitemid 38231531)
37. Warrell, D. A., Davidson, N. McD., Greenwood, B. M., Ormerod, L. D., Pope, H. M., Watkins, B. J. & Prentice, C. R. M. 1977 Poisoning by bites of the saw-scaled or carpet viper (Echis carinatus) in Nigeria. Q. J. Med. 46, 33-62.
38. Wüster, W., Golay, P. & Warrell, D. A. 1997 Synopsis of recent developments in venomous snake systematics. Toxicon 35, 319-340. (doi:10.1016/S0041-0101(96)00152-3) (Pubitemid 27102254)
39. Wüster, W., Daltry, J. C. & Thorpe, R. S. 1999 Can diet explain intraspecific venom variation? Reply to Sasa. Toxicon 37, 253-258. (doi:10.1016/S0041-0101(98)00248-7)
40. Wüster, W., Duarte, M. R. & Salomão, M. D. G. 2005 Morphological correlates of incipient arboreality and ornithophagy in island pitvipers, and the phylogenetic position of Bothrops insularis. J. Zool. Lond. 266, 1-10. (doi:10.1017/S0952836904006247)
41. Wüster, W., Peppin, L., Pook, C. E. & Walker, D. E. 2008 A nesting of vipers: phylogeny, historical biogeography and patterns of diversification of the Viperidae (Squamata: Serpentes). Mol. Phylogenet. Evol. 49, 445-459. (doi:10.1016/j.ympev.2008.08.019)
42. Zhang, D.-X. & Hewit, G. M. 1996 Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol. Evol. 11, 247-251. (doi:10.1016/0169- 5347(96)10031-8)