The venom optimization hypothesis revisited

Toxicon

Volumn 63, Issue 1, 2013, Pages 120-128

  Morgenstern, David ^a   King, Glenn F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Scorpion; Snake; Spider; Venom; Venom metering; Venom optimization hypothesis

Indexed keywords

VENOM;

ANIMAL BEHAVIOR; BIOCHEMISTRY; BITES AND STINGS; ENVENOMATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EVOLUTION; NONHUMAN; POISONOUS ANIMAL; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; TAXONOMY;

ADAPTATION, PHYSIOLOGICAL; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ENERGY METABOLISM; EVOLUTION, MOLECULAR; LONGEVITY; NUTRITIONAL REQUIREMENTS; PHYLOGENY; POISONS; SCORPION VENOMS; SCORPIONS; SNAKE VENOMS; SNAKES; SPIDER VENOMS; SPIDERS; VENOMS;

ANIMALIA; ARANEAE; SCORPIONES;

EID: 84872144447     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2012.11.022     Document Type: Review

References (84)

1. Allon N., Kochva E. The quantities of venom injected into prey of different size by Vipera palaestinae in a single bite. J. Exp. Zool. 1974, 188:71-75.
2. Alves De Rezende N., Maia Torres F., Borges Dias M., Campolina D., Chavez-Olortegui C., Faria Santos Amaral C. South American rattlesnake bite (Crotalus durissus sp) without envenoming: insights on diagnosis and treatment. Toxicon 1998, 36:2029-2032.
3. Binford G.J., Bodner M.R., Cordes M.H.J., Baldwin K.L., Rynerson M.R., Burns S.N., Zobel-Thropp P.A. Molecular evolution, functional variation, and proposed nomenclature of the gene family that includes sphingomyelinase D in sicariid spider venoms. Mol. Biol. Evol. 2009, 26:547-566.
4. Boevé J.L. Injection of venom into an insect prey by the free hunting spider Cupiennius salei (Araneae, Ctenidae). J. Zool. 1994, 234:165-175.
5. Boevé J.L., Kuhn-Nentwig L., Keller S., Nentwig W. Quantity and quality of venom released by a spider (Cupiennius salei, Ctenidae). Toxicon 1995, 33:1347-1357.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Bub K., Bowerman R.F. Prey capture by the scorpion Hadrurus arizonensis Ewing (Scorpiones: Vaejovidae). J. Arachnol. 1979, 7:243-253.
8. Cascardi J., Young B.A., Husic H.D., Sherma J. Protein variation in the venom spat by the red spitting cobra, Naja pallida (Reptilia: Serpentes). Toxicon 1999, 37:1271-1279.
9. Casper G.S. Prey capture and stinging behavior in the emperor scorpion, Pandinus imperator (Koch) (Scorpiones, Scorpionidae). J. Arachnol. 1985, 13:277-283.
10. Catterall W.A., Cestèle S., Yarov-Yarovoy V., Yu F.H., Konoki K., Scheuer T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49:124-141.
11. Cavalieri M., Corvaja N., Grasso A. Immunocytological localization by monoclonal antibodies of α-latrotoxin in the venom gland of the spider Latrodectus tredecimguttatus. Toxicon 1990, 28:341-346.
12. Cushing B.S., Matherne A. Stinger utilization and predation in the scorpion Paruroctonus boreus. West. North. Am. Naturalist 1980, 40:193-195.
13. dos Santos V.L., Franco C.R., Viggiano R.L., da Silveira R.B., Cantão M.P., Mangili O.C., Veiga S.S., Gremski W. Structural and ultrastructural description of the venom gland of Loxosceles intermedia (brown spider). Toxicon 2000, 38:265-285.
14. Edmunds M.C., Sibly R.M. Optimal sting use in the feeding behavior of the scorpion Hadrurus spadix. J. Arachnol. 2010, 38:123-125.
15. Escoubas P., Sollod B., King G.F. Venom landscapes: mining the complexity of spider venoms via a combined cDNA and mass spectrometric approach. Toxicon 2006, 47:650-663.
16. Freeman M., Kellaway C.H. The venom yields of common Australian poisonous snakes in captivity. Med. J. Aust. 1934, 2:373-377.
17. Fry B.G., Roelants K., Champagne D.E., Scheib H., Tyndall J.D.A., King G.F., Nevalainen T.J., Norman J.A., Lewis R.J., Norton R.S., Renjifo C., de la Vega R.C. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genom. Hum. Genet. 2009, 10:483-511.
18. Furry K., Swain T., Chiszar D. Strike-induced chemosensory searching and trail following by prairie rattlesnakes (Crotalus viridis) preying upon deer mice (Peromyscus maniculatus): chemical discrimination among individual mice. Herpetologica 1991, 47:69-78.
19. Gans C., Kochva E. The accessory gland in the venom apparatus of viperid snakes. Toxicon 1965, 3:61-63.
20. Hayes W.K. Prey-handling and envenomation strategies of prairie rattlesnakes (Crotalus v. viridis) feeding on mice and sparrows. J. Herpetol. 1992, 26:496-499.
21. Hayes W.K. Factors associated with the mass of venom expended by prairie rattlesnakes (Crotalus v. viridis) feeding on mice. Toxicon 1992, 30:449-460.
22. Hayes W.K. Effects of hunger on striking, prey-handling, and venom expenditure of prairie rattlesnakes (Crotalus v. viridis). Herpetologica 1993, 49:305-310.
23. Hayes W.K. Venom metering by juvenile prairie rattlesnakes, Crotalus v. viridis: effects of prey size and experience. Anim. Behav. 1995, 50:33-40.
24. Hayes W.K., Lavín-Murcio P., Kardong K.V. Northern pacific rattlesnakes (Crotalus viridis oreganus) meter venom when feeding on prey of different sizes. Copeia 1995, 1995:337-343.
25. Hayes W.K., Herbert S.S., Rehling G., Gennaro J. Factors that influence venom expenditure in viperids and other snake species during predatory and defensive contexts. Biology of the Vipers 2002, 207-234. Eagle Mountain Publishing, Eagle Mountain, Utah. G.W. Schuett, M. Hoggren, M.E. Douglas, H.W. Greene (Eds.).
26. Hayes W.K. The snake venom-metering controversy: levels of analysis, assumptions, and evidence. The Biology of Rattlesnakes 2008, 191-220. Loma Linda University Press, Loma Linda. W.K. Hayes, K.R. Beaman, M.D. Cardwell, S.P. Bush (Eds.).
27. Herzig V., Wood D.L.A., Newell F., Chaumeil P.-A., Kaas Q., Binford G.J., Nicholson G.M., Gorse D., King G.F. ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures. Nucl. Acids Res. 2011, 39:D653-D657.
28. Hostettler S., Nentwig W. Olfactory information saves venom during prey-capture of the hunting spider Cupiennius salei (Araneae: Ctenidae). Funct. Ecol. 2006, 20:369-375.
29. Inceoglu B., Lango J., Jing J., Chen L., Doymaz F., Pessah I.N., Hammock B.D. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:922-927.
30. Jorge M.T., Ribeiro L.A., O'Connell J.L. Prognostic factors for amputation in the case of envenoming by snakes of the Bothrops genus (Viperidae). Ann. Trop. Med. Parasitol. 1999, 93:401-408.
31. Juarez P., Comas I., Gonzalez-Candelas F., Calvete J.J. Evolution of snake venom disintegrins by positive Darwinian selection. Mol. Biol. Evol. 2008, 25:2391-2407.
32. Jungo F., Bougueleret L., Xenarios I., Poux S. The UniProtKB/Swiss-Prot Tox-Prot program: a central hub of integrated venom protein data. Toxicon 2012, 60:551-557.
33. King G.F. The wonderful world of spiders: preface to the special Toxicon issue on spider venoms. Toxicon 2004, 43:471-475.
34. V channels. Channels 2008, 2:100-116.
35. King G.F. Venoms as a platform for human drugs: translating toxins into therapeutics. Exp. Opin. Biol. Ther. 2011, 11:1469-1484.
36. King G.F., Hardy M.C. Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Annu. Rev. Entomol. 2013, 58:475-496.
37. Kordis D., Gubensek F. Adaptive evolution of animal toxin multigene families. Gene 2000, 261:43-52.
38. Kouyoumdjian J.A., Polizelli C. Snake bites by Bothrops moojeni: correlation of the clinical picture with the snake size. Rev. Inst. Med. Trop. Sao Paulo 1989, 31:84-90.
39. Kovoor J. Etude histochimique des glandes a venin des Buthidae (Arachnida, Scorpiones). Ann. Sci. Nat. Zool. 1973, 15:201-220.
40. Kuhn-Nentwig L., Stocklin R., Nentwig W. Venom composition and strategies in spiders: is everything possible?. Advances in Insect Physiology 2011, vol. 60:1-86. Academic Press, Burlington.
41. Li M., Fry B.G., Kini R.M. Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J. Mol. Evol. 2005, 60:81-89.
42. Malli H., Imboden H., Kuhn-Nentwig L. Quantifying the venom dose of the spider Cupiennius salei using monoclonal antibodies. Toxicon 1998, 36:1959-1969.
43. Malli H., Kuhn-Nentwig L., Imboden H., Nentwig W. Effects of size, motility and paralysation time of prey on the quantity of venom injected by the hunting spider Cupiennius salei. J. Exp. Biol. 1999, 202:2083-2089.
44. Malli H., Kuhn-Nentwig L., Imboden H., Moon M.J., Wyler T. Immunocytochemical localization and secretion process of the toxin CSTX-1 in the venom gland of the wandering spider Cupiennius salei (Araneae: Ctenidae). Cell. Tissue Res. 2000, 299:417-426.
45. McCue M.D., Mason R. Cost of producing venom in three North American pitviper species. Copeia 2006, 2006:818-825.
46. Minton S.A. Venomous bites by nonvenomous snakes: an annotated bibliography of colubrid envenomation. J. Wilderness Med. 1990, 1:119-127.
47. Miranda F., Kupeyan C., Rochat H., Rochat C., Lissitzky S. Purification of animal neurotoxins. Eur. J. Biochem. 1970, 16:514-523.
48. Mirtschin P.J., Dunstan N.L., Hough B.J., Hamilton E., Klein S. Venom yields from Australian and some other species of snakes. Ecotoxicology 2006, 15:531-538.
49. Morrison J.J., Pearn J.H., Coulter A.R. The mass of venom injected by two Elapidae: the Taipan (Oxyuranus scutellatus) and the Australian Tiger snake (Notechis scutatus). Toxicon 1982, 20:739-745.
50. Morrison J.J., Pearn J.H., Charles N.T., Coulter A.R. Further studies on the mass of venom injected by Elapid snakes. Toxicon 1983, 21:279-284.
51. Nagpal N., Kanwar U. The poison gland in the centipede Otostigmus ceylonicus; morphology and cytochemistry. Toxicon 1981, 19:898-902.
52. Nascimento D.G., Rates B., Santos D.M., Verano-Braga T., Barbosa-Silva A., Dutra A.A.A., Biondi I., Martin-Eauclaire M.F., Lima M.E.D., Pimenta A.M.C. Moving pieces in a taxonomic puzzle: venom 2D-LC/MS and data clustering analyses to infer phylogenetic relationships in some scorpions from the Buthidae family (Scorpiones). Toxicon 2006, 47:628-639.
53. Nicholson G.M., Little M.J., Tyler M., Narahashi T. Selective alteration of sodium channel gating by Australian funnel-web spider toxins. Toxicon 1996, 34:1443-1453.
54. Nisani Z., Dunbar S.G., Hayes W.K. Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 2007, 147:509-513.
55. Nisani Z., Hayes W.K. Defensive stinging by Parabuthus transvaalicus scorpions: risk assessment and venom metering. Anim. Behav. 2011, 81:627-633.
56. Nisani Z., Boskovic D.S., Dunbar S.G., Kelln W., Hayes W.K. Investigating the chemical profile of regenerated scorpion (Parabuthus transvaalicus) venom in relation to metabolic cost and toxicity. Toxicon 2012, 60:315-323.
57. Nowak M.A., Boerlijst M.C., Cooke J., Smith J.M. Evolution of genetic redundancy. Nature 1997, 388:167-171.
58. Oron U., Bdolah A. Regulation of protein synthesis in the venom gland of Viperid snakes. J. Cell. Biol. 1973, 56:177-190.
59. Pal C., Papp B., Lercher M.J. An integrated view of protein evolution. Nat. Rev. Genet. 2006, 7:337-348.
60. Pe T., Cho K.A. Amount of venom injected by Russell's viper (Vipera russelli). Toxicon 1986, 24:730-733.
61. Perret B.A. Venom regeneration in Tarantula spiders-I. Analysis of venom produced at different time intervals. Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 1977, 56:607-613.
62. Pintor A.F.V., Krockenberger A.K., Seymour J.E. Costs of venom production in the common death adder (Acanthophis antarcticus). Toxicon 2010, 56:1035-1042.
63. Rein J.O. Sting use in two species of Parabuthus scorpions (Buthidae). J. Arachnol. 1993, 21:60-63.
64. Rochelle M.J., Kardong K.V. Constriction versus envenomation in prey capture by the brown tree snake, Boiga irregularis (Squamata: Colubridae). Herpetologica 1993, 49:301-304.
65. Rodríguez-Robles J.A., Leal M. Effects of prey type on the feeding behavior of Alsophis portoricensis (Serpentes: Colubridae). J. Herpetol. 1993, 27:163-168.
66. Rotenberg D., Bamberger E.S., Kochva E. Studies on the ribonucleic acid synthesis in the venom glands of Vipera palaestine. Biochem. J. 1971, 121:609-612.
67. Sakai F., Carneiro S.M., Yamanouye N. Morphological study of accessory gland of Bothrops jararaca and its secretory cycle. Toxicon 2012, 59:393-401.
68. Shaham N., Kochva E. Localization of venom antigens in the venom gland of Vipera palaestinae using a fluorescent-antibody technique. Toxicon 1969, 6:263-264.
69. Shine R., Schwaner T. Prey constriction by venomous snakes: a review, and new data on Australian species. Copeia 1985, 1985:1067-1071.
70. Silva L.M., Carvalho Botelho A.C., Nacif-Pimenta R., Martins G.F., Alves L.C., Brayner F.A., Fortes-Dias C.L., Pimenta P.F.P. Structural analysis of the venom glands of the armed spider Phoneutria nigriventer (Keyserling, 1891): microanatomy, fine structure and confocal observations. Toxicon 2008, 51:693-706.
71. Smith T.L., Kardong K.V., Lavín-Murcio P.A. Persistence of trailing behavior: cues involved in poststrike behavior by the rattlesnake (Crotalus viridis oreganus). Behaviour 2000, 137:691-703.
72. Sollod B.L., Wilson D., Zhaxybayeva O., Gogarten J.P., Drinkwater R., King G.F. Were arachnids the first to use combinatorial peptide libraries?. Peptides 2005, 26:131-139.
73. Thomas L., Tyburn B., Ketterlé J., Biao T., Mehdaoui H., Moravie V., Rouvel C., Plumelle Y., Bucher B., Canonge D., Marie-Nelly C.A., Lang J. Prognostic significance of clinical grading of patients envenomed by Bothrops lanceolatus in Martinique. Trans. Roy. Soc. Trop. Med. Hyg. 1998, 92:542-545.
74. Tian C., Yuan Y., Zhu S. Positively selected sites of scorpion depressant toxins: possible roles in toxin functional divergence. Toxicon 2008, 51:555-562.
75. Tun P., Ba A., Aye Aye M., Tin Nu S., Warrell D.A. Bites by Russell's vipers (Daboia russelii siamensis) in Myanmar: effect of the snake's length and recent feeding on venom antigenaemia and severity of envenoming. Trans. Roy. Soc. Trop. Med. Hyg. 1991, 85:804-808.
76. Weinberger H., Moran Y., Gordon D., Turkov M., Kahn R., Gurevitz M. Positions under positive selection-key for selectivity and potency of scorpion α-toxins. Mol. Biol. Evol. 2010, 27:1025-1034.
77. Wigger E., Kuhn-Nentwig L., Nentwig W. The venom optimisation hypothesis: a spider injects large venom quantities only into difficult prey types. Toxicon 2002, 40:749-752.
78. Wood D.L., Miljenovic T., Cai S., Raven R.J., Kaas Q., Escoubas P., Herzig V., Wilson D., King G.F. ArachnoServer: a database of protein toxins from spiders. BMC Genomics 2009, 10:375.
79. Wullschleger B., Nentwig W. Influence of venom availability on a spider's prey-choice behaviour. Funct. Ecol. 2002, 16:802-807.
80. Yahel-Niv A., Zlotkin E. Comparative studies on venom obtained from individual scorpions by natural stings. Toxicon 1979, 17:435-446.
81. Young B.A., Lee C.E., Daley K.M. Do snakes meter venom?. Bioscience 2002, 52:1121-1126.
82. Young B.A., Kardong K.V. Mechanisms controlling venom expulsion in the western diamondback rattlesnake, Crotalus atrox. J. Exp. Zool. Part A 2007, 307A:18-27.
83. Zlotkin E., Shulov A.S. A simple device for collecting scorpion venom. Toxicon 1969, 7:331-332.
84. Zlotkin E., Rochat H., Kopeyan, Miranda F., Lissitzky S. Purification and properties of the insect toxin from the venom of the scorpion Androctonus australis Hector. Biochimie 1971, 53:1073-1078.