Theoretical Ecology

, Volume 6, Issue 4, pp 443–456 | Cite as

Coevolution of resource trade-offs driving species interactions in a host–parasite network: an exploratory model

  • C. Finn McQuaidEmail author
  • Nicholas F. Britton
Original Paper


Patterns of specialization asymmetry, where specialist species interact mainly with generalists while generalists interact with both generalists and specialists, are often observed in mutualistic and antagonistic bipartite ecological networks. These have been explained in terms of the relative abundance of species, using a null model that assigns links in proportion to abundance, but doubts have been raised as to whether this offers a complete explanation. In particular, host–parasite networks offer a variety of examples in which the reverse patterns are observed. We propose that the link between specificity and species richness may also be driven by the coevolution of hosts and parasites, as hosts allocate resources to optimize defense against parasites, and parasites to optimize attack on hosts. In this hypothesis, species interactions are a result of resource allocations. This novel concept, linking together many different arguments for network structures, is introduced through the adaptive dynamics of a simple ecological toy system of two hosts and two parasites. We analyze the toy model and its functionality, demonstrating that coevolution leads to specialization asymmetry in networks with closely related parasites or fast host mutation rates, but not in networks with more distantly related species. Having constructed the toy model and tested its applicability, our model can now be expanded to the full problem of a larger system.


Coevolution Nestedness Trade-off Parasite Food web 



C.F. McQuaid is a Commonwealth Scholar, funded by the Department for International Development, UK.


  1. Almeida-Neto M, Guimarães PR Jr, Lewinsohn TM (2007) On nestedness analyses: rethinking matrix temperature and anti-nestedness. Oikos 116:716–722CrossRefGoogle Scholar
  2. Bascompte J (2010) Structure and dynamics of ecological networks. Science 329:765–766PubMedCrossRefGoogle Scholar
  3. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. PNAS 100:9383–9387PubMedCrossRefGoogle Scholar
  4. Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1021PubMedCrossRefGoogle Scholar
  5. Bennett R, Bowers RG (2008) A baseline model for the co-evolution of hosts and pathogens. J Math Biol 57:791–809PubMedCrossRefGoogle Scholar
  6. Best A, White A, Boots M (2009) The implications of coevolutionary dynamics to host–parasite interactions. Am Nat 173(6):779–791PubMedCrossRefGoogle Scholar
  7. Best A, White A, Kisdi E, Antonovics J, Brockhurst M, Boots M (2010) The evolution of host–parasite range. Am Nat 176(1):63–71PubMedCrossRefGoogle Scholar
  8. Caval D, Ferriere R (2010) A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 64:2988–3–9Google Scholar
  9. Chen H-W, Liu W-C, Davis AJ, Jordán F, Hwang M-J, Shao K-T (2008) Network position of hosts in food webs and their parasite diversity. Oikos 117:1847–1855CrossRefGoogle Scholar
  10. Cobey S, Pascual M, Dieckmann U (2010) Ecological factors driving the long-term evolution of influenza’s host range. Proc R Soc B 277:2803–2810PubMedCrossRefGoogle Scholar
  11. de Mazancourt C, Dieckmann U (2004) Trade-off geometries and frequency-dependent selection. Am Nat 164(6):765–778CrossRefGoogle Scholar
  12. Dercole F, Irisson J-O, Rinaldi S (2003) Bifurcation analysis of a predator-prey coevolution model. SIAM J Appl Math 63:1378–1391CrossRefGoogle Scholar
  13. Dieckmann U, Law R (1996) The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol 34:579–612PubMedCrossRefGoogle Scholar
  14. Drossel B, McKane A (2005) Modelling food webs. In: Bornholdt S, Schuster H (eds) Handbook of graphs and networks: from the genome to the internet. Wiley, WeinheimGoogle Scholar
  15. Feliu C, Renaud F, Catzeflis F, Hugot J-P, Durand P, Morand S (1997) A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115:453–466PubMedCrossRefGoogle Scholar
  16. Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS (2011) Statistical structure of host–phage interactions. PNAS 108:E288–E297PubMedCrossRefGoogle Scholar
  17. Geritz S, Kisdi E, Meszéna G, Metz J (1998) Evolutionary singular strategies and the adaptive growth and branching of the evolutionary tree. Evol Ecol 12:35–57CrossRefGoogle Scholar
  18. Graham SP, Hassan HK, Burkett-Cadena ND, Guyer C, Unnasch TR (2009) Nestedness of ectoparasite-vertebrate host networks. PLoS ONE 4:1–8CrossRefGoogle Scholar
  19. Hart BL (1988) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273–294CrossRefGoogle Scholar
  20. Hernandez AD, Sukhdeo MV (2008) Parasites alter the topology of a stream food web across seasons. Oecologia 156:613–624PubMedCrossRefGoogle Scholar
  21. Hurford A, Cownden D, Day T (2010) Next-generation tools for evolutionary invasion analyses. J R Soc Interface 7:561–571PubMedCrossRefGoogle Scholar
  22. Ings TC, Montoya JM, Bascompte J, Blüthgen N, Brown L, Dormann CF, Edwards F, Figueroa D, Jacob U, Jones JI, Lauridsen RB, Ledger ME, Lewis HM, Olsesen JM, van Veen FF, Warren PH, Woodward G (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269PubMedCrossRefGoogle Scholar
  23. Joppa LN, Bascompte JM, Solé RV, Sanderson J, Pimm SL (2009) Reciprocal specialization in ecological networks. Ecol Lett 12:961–969PubMedCrossRefGoogle Scholar
  24. Joppa LN, Montoya JM, Solé R, Sanderson J, Pimm SL (2010) On nestedness in ecological networks. Evol Ecol Res 12:35–46Google Scholar
  25. Kisdi E (2006) Trade-off geometries and the adaptive dynamics of two co-evolving species. Evol Ecol Res 8:959–973Google Scholar
  26. Kopp M, Gavrilets S (2006) Multilocus genetics and the coevolution of quantitative traits. Evolution 60(7):1321–1336PubMedGoogle Scholar
  27. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. PNAS 103(30):11211–11216PubMedCrossRefGoogle Scholar
  28. Law R, Bronstein JL, Ferrière R (2001) On mutualists and exploiters: plant-insect coevolution in pollinating seed-parasite systems. J Theor Biol 212:373–389PubMedCrossRefGoogle Scholar
  29. Lewinsohn TM, Prado PI, Jordano P, Bascompte J, Olesen JM (2006) Structure in plant-animal interaction assemblages. Oikos 113:174–184CrossRefGoogle Scholar
  30. Marcogliese D (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124:S83–S99PubMedCrossRefGoogle Scholar
  31. May R, Anderson R (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219:281–313PubMedCrossRefGoogle Scholar
  32. McGill BJ, Brown JS (2007) Evolutionary game theory and adaptive dynamics of continuous traits. Annu Rev Eco Evol Syst 38:403–435CrossRefGoogle Scholar
  33. McQuaid CF, Britton NF (2013) Host-parasite nestedness: a result of co-evolving trait-values. Ecol Complex 13:53–59CrossRefGoogle Scholar
  34. Møller A, Christe P, Garamszegi L (2005) Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas. J Evol Biol 18:46–59PubMedCrossRefGoogle Scholar
  35. Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442:259–264PubMedCrossRefGoogle Scholar
  36. Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727CrossRefGoogle Scholar
  37. Nuismer SL, Ridenhour BJ, Oswald BP (2007) Antagonistic coevolution mediated by phenotypic differences between quantitative traits. Evolution 61(8):1823–1834PubMedCrossRefGoogle Scholar
  38. Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasite species richness in primates. Am Nat 162:597–614PubMedCrossRefGoogle Scholar
  39. Poitrineau K, Brown S, Hochberg M (2003) Defence against multiple enemies. J Evol Biol 16:1319–1327PubMedCrossRefGoogle Scholar
  40. Poulin R (1997) Parasite faunas of freshwater fish: the relationship between richness and the specificity of parasites. Int J Parasitol 27(9):1091–1098PubMedCrossRefGoogle Scholar
  41. Poulin R (1998) Large-scale patterns of host use by parasites of freshwater fishes. Ecol Lett 1:118–128CrossRefGoogle Scholar
  42. Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776PubMedCrossRefGoogle Scholar
  43. Poulin R (2010) Network analysis shining light on parasite ecology and diversity. Trends Parasitol 26:492–498PubMedCrossRefGoogle Scholar
  44. Poulin R, Guégan J-F (2000) Nestedness, anti-nestedness, and the relationship between prevalence and intensity in ectoparasite assemblages of marine fish: a spatial model of species coexistence. Int J Parasitol 30:1147–1152PubMedCrossRefGoogle Scholar
  45. Poulin R, Leung T (2011) Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166:731–738PubMedCrossRefGoogle Scholar
  46. Poulin R, Morand S (2004) Parasite biodiversity, 1st edn. Smithsonian Institution, Washington D.C., pp 43–52, 86–90, 153–157Google Scholar
  47. Pugliese A (2002) On the evolutionary coexistence of parasite strains. Math Biosci 177–178:355–375PubMedCrossRefGoogle Scholar
  48. Rezende EL, Jordano P, Bascompte J (2007) Effects of phenotypic complementarity and phylogeny on the nested structure of mutualistic networks. Oikos 116:1919–1929CrossRefGoogle Scholar
  49. Rueffler C, Van Dooren TJ, Metz JA (2006) The evolution of resource specialization through frequency-dependent and frequency-independent mechanisms. Am Nat 167:81–93PubMedCrossRefGoogle Scholar
  50. Sasaki A (2000) Host–parasite coevolution in a multilocus gene-for-gene system. Proc R Soc Lond B 267:2183–2188CrossRefGoogle Scholar
  51. Thébault E, Fontaine C (2008) Does asymmetric specialization differ between mutualistic and trophic networks? Oikos 117:555–563CrossRefGoogle Scholar
  52. Thompson JN (2005) The geographic mosaic of coevolution, 1st edn. The University of Chicago Press, Chicago, pp 93–95, 246–259Google Scholar
  53. Valtonen E, Pulkkinen K, Poulin R, Julkunen M (2001) The structure of parasitic component communities in brackish water fishes of the northeastern Baltic Sea. Parasitology 122:471–481PubMedCrossRefGoogle Scholar
  54. Vázquez DP, Aizen MA (2003) Null model analyses of specialization in plant-pollinator interactions. Ecology 84:2493–2501CrossRefGoogle Scholar
  55. Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant-pollinator interactions. Ecology 85(5):1251–1257CrossRefGoogle Scholar
  56. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant-animal mutualistic networks: a review. Ann Bot 103:1445–1457PubMedCrossRefGoogle Scholar
  57. Vázquez DP, Poulin R, Krasnov BR, Shenbrot GI (2005) Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol 74:946–955CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Mathematical SciencesUniversity of BathBathUK

Personalised recommendations