Theoretical Ecology

, Volume 11, Issue 2, pp 141–149 | Cite as

When is overkill optimal? Tritrophic interactions reveal new insights into venom evolution

  • Alex N. GangurEmail author
  • Jamie E. Seymour
  • Michael J. Liddell
  • David Wilson
  • Michael J Smout
  • Tobin D. Northfield


Organisms embedded within food webs must balance arms races with their predators and prey. For venom users, venom may mediate each arms race, but the dynamical evolutionary changes in venom production in response to the two arms races are still poorly understood. Here, we use a simple model to evaluate the evolutionary response of a venomous consumer to the presence of an apex generalist predator and evolution of the consumer’s prey. We find that introduction of the apex predator can weaken the arms race between the two lower trophic levels. In addition, when consumer prey capture and predator defense venoms functionally overlap, a reduced evolutionary response in the prey population can drive investment in venom used for prey capture going beyond what is optimal for subduing prey. These dynamics suggest that interactions with multiple trophic levels can substantially alter the venom complexity in predatory venomous animals and may explain the paradox of the overkill hypothesis.


Predator Prey Coevolution Food web Arms race 

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  1. Abrams PA (1991) The effects of interacting species on predator-prey coevolution. Theor Popul Biol 39(3):241–262. CrossRefGoogle Scholar
  2. Abrams PA (2001) Modelling the adaptive dynamics of traits involved in inter- and intraspecific interactions: an assessment of three methods. Ecol Lett 4(2):166–175. CrossRefGoogle Scholar
  3. Adler M, Anjum M, Berg OG, Andersson DI, Sandegren L (2014) High fitness costs and instability of gene duplications reduce rates of evolution of new genes by duplication-divergence mechanisms. Mol Biol Evol 31(6):1526–1535. CrossRefPubMedGoogle Scholar
  4. Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28(4):219–229. CrossRefPubMedGoogle Scholar
  5. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung G-H, Spatafora JW, Straus NA (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299(5605):386–388. CrossRefPubMedGoogle Scholar
  6. Dawkins R and Krebs JR (1979) Arms races between and within species. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 205: 489–511.
  7. Dercole F, Ferriere R, Rinaldi S (2010) Chaotic Red Queen coevolution in three-species food chains. Proc R Soc B 277(1692):2321–2330. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dietl GP and Kelley PH (2002) The fossil record of predator-prey arms races: coevolution and escalation hypotheses. Paleontological Society Papers 8: 353–374Google Scholar
  9. Drabeck DH, Dean AM, Jansa SA (2015) Why the honey badger don’t care: convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites. Toxicon 99:68–72. CrossRefPubMedGoogle Scholar
  10. Dutertre S, Jin A-H, Vetter I, Hamilton B, Sunagar K, Lavergne V, Dutertre V, Fry BG, Antunes A, Venter DJ (2014) Evolution of separate predation-and defence-evoked venoms in carnivorous cone snails. Nat Commun 5:3521. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ and Norton RS (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genom Hum Genet 10: 483–511.
  12. Hayes WK (1992) Prey-handling and envenomation strategies of prairie rattlesnakes (Crotalus v. viridis) feeding on mice and sparrows. J Herpetol 26(4):496–499. CrossRefGoogle Scholar
  13. Hayes WK, Herbert SS, Harrison JR, Wiley KL (2008) Spitting versus biting: differential venom gland contraction regulates venom expenditure in the black-necked spitting cobra, Naja nigricollis nigricollis. J Herpetol 42(3):453–460. CrossRefGoogle Scholar
  14. Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD (2003) 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 100(3):922–927. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jansa SA and Voss RS (2011) Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS One 6(6):e20997.
  16. Kuhn-Nentwig L, Stöcklin R and Nentwig W (2011) Venom composition and strategies in spiders: is everything possible? Adv. Insect Physiol 40: 1Google Scholar
  17. Li M, Fry BG, Kini RM (2005) Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J Mol Evol 60(1):81–89. CrossRefPubMedGoogle Scholar
  18. McCue MD (2006) Cost of producing venom in three North American pitviper species. Copeia 2006: 818–825.[818:COPVIT]2.0.CO;2
  19. Mebs D (2001) Toxicity in animals. Trends in evolution? Toxicon 39(1):87–96. CrossRefPubMedGoogle Scholar
  20. Moran Y, Praher D, Schlesinger A, Ayalon A, Tal Y, Technau U (2013) Analysis of soluble protein contents from the nematocysts of a model sea anemone sheds light on venom evolution. Mar Biotechnol 15(3):329–339. CrossRefPubMedGoogle Scholar
  21. Morgenstern D and King GF (2013) The venom optimization hypothesis revisited. Toxicon 63:120–128.
  22. Nersesian CL, Banks PB, McArthur C (2011) Titrating the cost of plant toxins against predators: determining the tipping point for foraging herbivores. J Anim Ecol 80(4):753–760. CrossRefPubMedGoogle Scholar
  23. Nisani Z, Boskovic DS, Dunbar SG, Kelln W, Hayes WK (2012) Investigating the chemical profile of regenerated scorpion (Parabuthus transvaalicus) venom in relation to metabolic cost and toxicity. Toxicon 60(3):315–323. CrossRefPubMedGoogle Scholar
  24. Philpot VB and Stjernholm RL (1984) Resistance of reptiles to venoms. In: Hoff GL (ed) Diseases of amphibians and reptiles. Springer US, pp. 693–701.
  25. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  26. Rowe AH, Xiao Y, Rowe MP, Cummins TR, Zakon HH (2013) Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin. Science 342(6157):441–446. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Sasa M (1999) Diet and snake venom evolution: can local selection alone explain intraspecific venom variation? Toxicon 37(2):249–252CrossRefPubMedGoogle Scholar
  28. Smith MT, Ortega J, Beaupre SJ (2014) Metabolic cost of venom replenishment by Prairie Rattlesnakes (Crotalus viridis viridis). Toxicon 86:1–7. CrossRefPubMedGoogle Scholar
  29. Sunagar K and Moran Y (2015) The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLoS Genet 11(10):e1005596.
  30. Vermeij GJ (1982) Unsuccessful predation and evolution. Am Nat 120(6):701–720. CrossRefGoogle Scholar
  31. Voss RS (2013) Opossums (Mammalia: Didelphidae) in the diets of Neotropical pitvipers (Serpentes: Crotalinae): evidence for alternative coevolutionary outcomes? Toxicon 66:1–6. CrossRefPubMedGoogle Scholar
  32. Wade MJ (2007) The co-evolutionary genetics of ecological communities. Nat Rev Genet 8(3):185–195. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Alex N. Gangur
    • 1
    Email author
  • Jamie E. Seymour
    • 2
  • Michael J. Liddell
    • 1
  • David Wilson
    • 2
  • Michael J Smout
    • 2
  • Tobin D. Northfield
    • 1
  1. 1.Centre for Tropical Environmental and Sustainability Science and College of Science and EngineeringJames Cook UniversityCairnsAustralia
  2. 2.Centre for Biodiscovery and Molecular Development of Therapeutics, Australian Institute for Tropical Health and MedicineJames Cook UniversityCairnsAustralia

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