High Specific Efficiency of Venom of Two Prey-Specialized Spiders

. 2019 Nov 23 ; 11 (12) : . [epub] 20191123

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31771158

The venom of predators should be under strong selection pressure because it is a costly substance and prey may potentially become resistant. Particularly in prey-specialized predators, venom should be selected for its high efficiency against the focal prey. Very effective venom paralysis has been observed in specialized predators, such as spiders preying on dangerous prey. Here, we compared the toxicity of the venoms of two prey-specialized species, araneophagous Palpimanus sp. and myrmecophagous Zodarion nitidum, and their related generalist species. We injected different venom concentrations into two prey types-the prey preferred by a specialist and an alternative prey-and observed the mortality and the paralysis of the prey within 24 h. We found that the venoms of specialists were far more potent towards the preferred prey than alternative prey. The venoms of generalists were similarly potent towards both prey types. In addition, we tested the efficacy of two venom fractions (smaller and larger than 10 kDa) in araneophagous Palpimanus sp. Compounds larger than 10 kDa paralyzed both prey types, but smaller compounds (<10 kDa) were effective only on preferred prey, suggesting the presence of prey-specific compounds in the latter fraction. Our results confirm that prey-specialized spiders possess highly specific venom that allows them to subdue dangerous prey.

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Fry B.G., Roelants K., Champagne D.E., Scheib H., Tyndall J.D., King G.F., Nevalainen T.J., Norman J.A., Lewis R.J., Norton R.S., et al. The toxicogenomic multiverse: Convergent recruitment of proteins into animal venoms. Annu. Rev. Genom. Hum. Genet. 2009;10:483–511. doi: 10.1146/annurev.genom.9.081307.164356. PubMed DOI

Morgenstern D., King G.F. The venom optimization hypothesis revisited. Toxicon. 2013;63:120–128. doi: 10.1016/j.toxicon.2012.11.022. PubMed DOI

Walker A.A., Robinson S.D., Yeates D.K., Jin J., Baumann K., Dobson J., Fry B.G., King G.F. Entomo-venomics: The evolution, biology and biochemistry of insect venoms. Toxicon. 2018;154:5–27. doi: 10.1016/j.toxicon.2018.09.004. PubMed DOI

Casewell N.R., Wüster W., Vonk F.J., Harrison R.A., Fry B.G. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol. Evol. 2013;28:219–229. doi: 10.1016/j.tree.2012.10.020. PubMed DOI

Von Reumont B., Campbell L., Jenner R. Quo vadis venomics? A roadmap to neglected venomous invertebrates. Toxins. 2014;6:3488–3551. doi: 10.3390/toxins6123488. PubMed DOI PMC

Wilson D., Daly N. Venomics: A mini-review. High Throughput. 2018;7:19. doi: 10.3390/ht7030019. PubMed DOI PMC

Chippaux J.P., Williams V., White J. Snake venom variability: Methods of study, results and interpretation. Toxicon. 1991;29:1279–1303. doi: 10.1016/0041-0101(91)90116-9. PubMed DOI

Minton S.A. A note on the venom of an aged rattlesnake. Toxicon. 1975;13:73–74. doi: 10.1016/0041-0101(75)90162-2. PubMed DOI

Fiero M.K., Seifert M.W., Weaver T.J., Bonilla C.A. Comparative study of juvenile and adult prairie rattlesnake (Crotalus viridis viridis) venoms. Toxicon. 1972;10:81–82. doi: 10.1016/0041-0101(72)90095-5. PubMed DOI

Gubenšek F., Sket D., Turk V., Lebez D. Fractionation of Vipera ammodytes venom and seasonal variation of its composition. Toxicon. 1974;12:167–168. doi: 10.1016/0041-0101(74)90241-4. PubMed DOI

Jiménez-Porras J.M. Intraspecific variations in composition of venom of the jumping viper, Bothrops nummifera. Toxicon. 1964;2:187–195. doi: 10.1016/0041-0101(64)90021-2. PubMed DOI

Glenn J.L., Straight R. Mojave rattlesnake Crotalus scutulatus scutulatus venom: Variation in toxicity with geographical origin. Toxicon. 1978;16:81–84. doi: 10.1016/0041-0101(78)90065-X. PubMed DOI

Menezes M.C., Furtado M.F., Travaglia-Cardoso S.R., Camargo A.C., Serrano S.M. Sex-based individual variation of snake venom proteome among eighteen Bothrops jararaca siblings. Toxicon. 2006;47:304–312. doi: 10.1016/j.toxicon.2005.11.007. PubMed DOI

Daltry J.C., Wüster W., Thorpe R.S. Diet and snake venom evolution. Nature. 1996;379:537–540. doi: 10.1038/379537a0. PubMed DOI

Barlow A., Pook C.E., Harrison R.A., Wüster W. Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc. R. Soc. B. 2009;276:2443–2449. doi: 10.1098/rspb.2009.0048. PubMed DOI PMC

Healy K., Carbone C., Jackson A.L. Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure. Ecol. Lett. 2019;22:527–537. doi: 10.1111/ele.13216. PubMed DOI

McCue M.D. Cost of producing venom in three North American pitviper species. Copeia. 2006;2006:818–825. doi: 10.1643/0045-8511(2006)6[818:COPVIT]2.0.CO;2. DOI

Nisani Z., Dunbar S.G., Hayes W.K. Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae) Comp. Biochem. Physiol. A. 2007;147:509–513. doi: 10.1016/j.cbpa.2007.01.027. PubMed DOI

Pintor A.F., Krockenberger A.K., Seymour J.E. Costs of venom production in the common death adder (Acanthophis antarcticus) Toxicon. 2010;56:1035–1042. doi: 10.1016/j.toxicon.2010.07.008. PubMed DOI

Smith M.T., Ortega J., Beaupre S.J. Metabolic cost of venom replenishment by Prairie Rattlesnakes (Crotalus viridis viridis) Toxicon. 2014;86:1–7. doi: 10.1016/j.toxicon.2014.04.013. PubMed DOI

Arbuckle K., de la Vega R.C.R., Casewell N.R. Coevolution takes the sting out of it: Evolutionary biology and mechanisms of toxin resistance in animals. Toxicon. 2017;140:118–131. doi: 10.1016/j.toxicon.2017.10.026. PubMed DOI

Church J.E., Hodgson W.C. The pharmacological activity of fish venoms. Toxicon. 2002;40:1083–1093. doi: 10.1016/S0041-0101(02)00126-5. PubMed DOI

Peiren N., Vanrobaeys F., de Graaf D.C., Devreese B., Van Beeumen J., Jacobs F.J. The protein composition of honeybee venom reconsidered by a proteomic approach. Biochim. Biophys. Acta. 2005;1752:1–5. doi: 10.1016/j.bbapap.2005.07.017. PubMed DOI

De Graaf D.C., Aerts M., Danneels E., Devreese B. Bee, wasp and ant venomics pave the way for a component-resolved diagnosis of sting allergy. J. Proteom. 2009;72:145–154. doi: 10.1016/j.jprot.2009.01.017. PubMed DOI

Da Silva N.J., Aird S.D. Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2001;128:425–456. doi: 10.1016/S1532-0456(00)00215-5. PubMed DOI

Gibbs H.L., Mackessy S.P. Functional basis of a molecular adaptation: Prey-specific toxic effects of venom from Sistrurus rattlesnakes. Toxicon. 2009;53:672–679. doi: 10.1016/j.toxicon.2009.01.034. PubMed DOI

Pawlak J., Mackessy S.P., Fry B.G., Bhatia M., Mourier G., Fruchart-Gaillard C., Servent D., Ménez R., Stura E., Ménez A., et al. Denmotoxin, a three-finger toxin from the colubrid snake Boiga dendrophila (Mangrove Catsnake) with bird-specific activity. J. Biol. Chem. 2006;281:29030–29041. doi: 10.1074/jbc.M605850200. PubMed DOI

Fainzilber M., Gordon D., Hasson A., Spira M.E., Zlotkin E. Mollusc-specific toxins from the venom of Conus textile neovicarius. Eur. J. Biochem. 1991;202:589–595. doi: 10.1111/j.1432-1033.1991.tb16412.x. PubMed DOI

Krasnoperov V.G., Shamotienko O.G., Grishin E.V. A crustacean-specific neurotoxin from the venom of the black widow spider Latrodectus mactans tredecimguttatus. Bioorg. Khim. 1990;16:1567–1569. PubMed

Phuong M.A., Mahardika G.N., Alfaro M.E. Dietary breadth is positively correlated with venom complexity in cone snails. BMC Genom. 2016;17:401. doi: 10.1186/s12864-016-2755-6. PubMed DOI PMC

Pekár S., Bočánek O., Michálek O., Petráková L., Haddad C.R., Šedo O., Zdráhal Z. Venom gland size and venom complexity—essential trophic adaptations of venomous predators: A case study using spiders. Mol. Ecol. 2018;27:4257–4269. doi: 10.1111/mec.14859. PubMed DOI

Pekár S., Líznarová E., Bočánek O., Zdráhal Z. Venom of prey-specialized spiders is more toxic to their preferred prey: A result of prey-specific toxins. J. Anim. Ecol. 2018;87:1639–1652. doi: 10.1111/1365-2656.12900. PubMed DOI

World Spider Catalog. Version 20.5. Natural History Museum Bern. [(accessed on 26 September 2019)]; doi: 10.24436/2. Available online: http://wsc.nmbe.ch. DOI

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. doi: 10.1146/annurev-ento-120811-153650. PubMed DOI

Michálek O., Řezáč M., Líznarová E., Symondson W.O., Pekár S. Silk versus venom: Alternative capture strategies employed by closely related myrmecophagous spiders. Biol. J. Linn. Soc. 2019;126:545–554. doi: 10.1093/biolinnean/bly181. DOI

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. PubMed

Kuhn-Nentwig L., Schaller J., Nentwig W. Biochemistry, toxicology and ecology of the venom of the spider Cupiennius salei (Ctenidae) Toxicon. 2004;43:543–553. doi: 10.1016/j.toxicon.2004.02.009. PubMed DOI

Petráková L., Líznarová E., Pekár S., Haddad C.R., Sentenská L., Symondson W.O.C. Discovery of a monophagous true predator, a specialist termite-eating spider (Araneae: Ammoxenidae) Sci. Rep. 2015;5:14013. doi: 10.1038/srep14013. PubMed DOI PMC

Pekár S., Coddington J.A., Blackledge T.A. Evolution of stenophagy in spiders (Araneae): Evidence based on the comparative analysis of spider diets. Evolution. 2012;66:776–806. doi: 10.1111/j.1558-5646.2011.01471.x. PubMed DOI

Pekár S., Šobotník J., Lubin Y. Armoured spiderman: Morphological and behavioural adaptations of a specialised araneophagous predator (Araneae: Palpimanidae) Naturwissenschaften. 2011;98:593–603. doi: 10.1007/s00114-011-0804-1. PubMed DOI

Pekár S., Král J., Lubin Y. Natural history and karyotype of some ant-eating zodariid spiders (Araneae, Zodariidae) from Israel. J. Arachnol. 2005;33:50–63. doi: 10.1636/S03-2. DOI

Pekár S., Toft S., Hrušková M., Mayntz D. Dietary and prey-capture adaptations by which Zodarion germanicum, an ant-eating spider (Araneae: Zodariidae), specialises on the Formicinae. Naturwissenschaften. 2008;95:233–239. doi: 10.1007/s00114-007-0322-3. PubMed DOI

Poran N.S., Coss R.G., Benjami E.L.I. Resistance of California ground squirrels (Spermophilus beecheyi) to the venom of the northern Pacific rattlesnake (Crotalus viridis oreganus): A study of adaptive variation. Toxicon. 1987;25:767–777. doi: 10.1016/0041-0101(87)90127-9. PubMed DOI

Smiley-Walters S.A., Farrell T.M., Gibbs H.L. The importance of species: Pygmy rattlesnake venom toxicity differs between native prey and related non-native species. Toxicon. 2018;144:42–47. doi: 10.1016/j.toxicon.2018.01.022. PubMed DOI

Pekár S., Šedo O., Líznarová E., Korenko S., Zdráhal Z. David and Goliath: Potent venom of an ant-eating spider (Araneae) enables capture of a giant prey. Naturwissenschaften. 2014;101:533–540. doi: 10.1007/s00114-014-1189-8. PubMed DOI

Kuhn-Nentwig L., Bücheler A., Studer A., Nentwig W. Taurine and histamine: Low molecular compounds in prey hemolymph increase the killing power of spider venom. Naturwissenschaften. 1998;85:136–138. doi: 10.1007/s001140050471. PubMed DOI

Pekár S., Toft S. Can ant-eating Zodarion spiders (Araneae: Zodariidae) develop on a diet optimal for euryphagous arthropod predators? Physiol. Entomol. 2009;34:195–201. doi: 10.1111/j.1365-3032.2009.00672.x. DOI

Adams M.E. Agatoxins: Ion channel specific toxins from the American funnel web spider, Agelenopsis aperta. Toxicon. 2004;43:509–525. doi: 10.1016/j.toxicon.2004.02.004. PubMed DOI

Pekár S. Predatory behavior of two European ant-eating spiders (Araneae, Zodariidae) J. Arachnol. 2004;32:31–42. doi: 10.1636/S02-15. DOI

Kuhn-Nentwig L., Stöcklin R., Nentwig W. Spider Physiology and Behaviour. Volume 1. Elsevier; London, UK: 2011. Venom composition and strategies in spiders: Is everything possible; pp. 2–86.

Kuzmenkov A.I., Sachkova M.Y., Kovalchuk S.I., Grishin E.V., Vassilevski A.A. Lachesana tarabaevi, an expert in membrane-active toxins. Biochem. J. 2016;473:2495–2506. doi: 10.1042/BCJ20160436. PubMed DOI

Herzig V., King G.F., Undheim E.A. Can we resolve the taxonomic bias in spider venom research? Toxicon X. 2019;1:100005. doi: 10.1016/j.toxcx.2018.100005. PubMed DOI PMC

Skejic J., Steer D.L., Dunstan N., Hodgson W.C. Venoms of related mammal-eating species of taipans (Oxyuranus) and brown snakes (Pseudonaja) differ in composition of toxins involved in mammal poisoning. bioRxiv. 2018:378141. doi: 10.1101/378141. DOI

Jenner R.A., von Reumont B.M., Campbell L.I., Undheim E.A. Parallel evolution of complex centipede venoms revealed by comparative proteotranscriptomic analyses. Mol. Biol. Evol. 2019:msz181. doi: 10.1093/molbev/msz181. PubMed DOI PMC

Chandler D., Bailey A.S., Tatchell G.M., Davidson G., Greaves J., Grant W.P. The development, regulation and use of biopesticides for integrated pest management. Philos. Trans. R. Soc. B. 2011;366:1987–1998. doi: 10.1098/rstb.2010.0390. PubMed DOI PMC

Schultz T.R. In search of ant ancestors. Proc. Natl. Acad. Sci. USA. 2000;97:14028–14029. doi: 10.1073/pnas.011513798. PubMed DOI PMC

Vander Meer R.K., Jaffe K., Cedeno A. Applied Myrmecology: A World Perspective. Westview Press; Boulder, CO, USA: 1990. pp. 3–70.

Ward D., Lubin Y. Habitat selection and the life history of a desert spider, Stegodyphus lineatus (Eresidae) J. Anim. Ecol. 1993;62:353–363. doi: 10.2307/5366. DOI

Pompozzi G., García L.F., Petráková L., Pekár S. Distinct feeding strategies of generalist and specialist spiders. Ecol. Entomol. 2019;44:129–139. doi: 10.1111/een.12683. DOI

Kuhn-Nentwig L., Schaller J., Nentwig W. Purification of toxic peptides and the amino acid sequence of CSTX-1 from the multicomponent venom of Cupiennius salei (Araneae: Ctenidae) Toxicon. 1994;32:287–302. doi: 10.1016/0041-0101(94)90082-5. PubMed DOI

Friedel T., Nentwig W. Immobilizing and lethal effects of spider venoms on the cockroach and the common mealbeetle. Toxicon. 1989;27:305–316. doi: 10.1016/0041-0101(89)90178-5. PubMed DOI

Eggs B., Wolff J.O., Kuhn-Nentwig L., Gorb S.N., Nentwig W. Hunting without a web: How lycosoid spiders subdue their prey. Ethology. 2015;121:1166–1177. doi: 10.1111/eth.12432. DOI

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2018. [(accessed on 15 March 2018)]. Available online: https://www.R-project.org/

Venables W.N., Ripley B.D. Modern Applied Statistics with S. 4th ed. Springer; New York, NY, USA: 2002.

Smiley-Walters S.A., Farrell T.M., Gibbs H.L. Evaluating local adaptation of a complex phenotype: Reciprocal tests of pigmy rattlesnake venoms on treefrog prey. Oecologia. 2017;184:739–748. doi: 10.1007/s00442-017-3882-8. PubMed DOI

Halekoh U., Højsgaard S., Yan J. The R package geepack for generalized estimating equations. J. Stat. Softw. 2006;15:1–11. doi: 10.18637/jss.v015.i02. DOI

Pekár S., Brabec M. Generalized estimating equations: A pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology. 2018;124:86–93. doi: 10.1111/eth.12713. DOI

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