Evolutionary Ecology

, Volume 29, Issue 5, pp 627–641 | Cite as

The evolution of mutualism from reciprocal parasitism: more ecological clothes for the Prisoner’s Dilemma

  • Janis Antonovics
  • Joana Bergmann
  • Stefan Hempel
  • Erik Verbruggen
  • Stavros Veresoglou
  • Matthias Rillig
Original Paper


Many mutualisms involve reciprocal exploitation, such that each species in a mutualism is a consumer of a resource provided by the other. Frequently, such mutualisms are reformed each generation, and where they involve close physiological contact, such as between mycorrhizal fungi and plants, they can be considered as examples of reciprocal parasitism. Here we place such interactions in the framework of the Prisoner’s Dilemma, and examine the conditions for the spread of mutualism using a population genetics model analogous to that used for understanding the genetic and numerical dynamics of host-parasite interactions. Genetic variants within each of two species determine whether the interaction is mutualistic or selfish, the latter being represented by resistance to being exploited or parasitized. We assume that there are fitness costs to resistance which are present even in the absence of the interaction. Just as in host-parasite interactions, we examine the effect of assuming that encounter rates between potential mutualists (and therefore entry into the Prisoner’s Dilemma ‘game’) depend on the density and frequency of the different types interacting individuals. These elements of ecological realism greatly facilitate the evolution of mutualism even in the absence of spatial structure or iterative encounters. Moreover, stable genetic polymorphisms for resistant (selfish) and susceptible (mutualistic) alleles can be maintained, something that is not possible with the classical Prisoner’s Dilemma formulation. The sensitivity of the outcomes to levels of density-dependence and mortality rate suggests environmental as well as genetic processes are likely to be important in determining directions in this pathway to mutualism.


Defection Co-operation Cheating Symbiosis Genetic polymorphism Disease resistance Pair formation 



J.A. is grateful for support from the Humboldt Foundation and for NSF Grant DEB-1115899 as part of the joint NSF-NIH Ecology of Infectious Disease program.

Supplementary material

10682_2015_9775_MOESM1_ESM.docx (204 kb)
Supplementary material 1 (DOCX 204 kb)


  1. Aguilar-Trigueros CA, Powell JR, Anderson IC, Antonovics J, Rillig MC (2014) Ecological understanding of root-infecting fungi using trait-based approaches. Trends Plant Sci 19:432–438CrossRefPubMedGoogle Scholar
  2. Antonovics J, Thrall PH (1994) The cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc R Soc Lond B 257:105–110CrossRefGoogle Scholar
  3. Antonovics J, Iwasa Y, Hassell MP (1995) A generalized model of parasitoid, venereal, and vector-based transmission processes. Am Nat 145:661–675CrossRefGoogle Scholar
  4. Baker C, Antonovics J (2012) Evolutionary determinants of genetic variation in susceptibility to infectious diseases in humans. Plos One 7:e29089PubMedCentralCrossRefPubMedGoogle Scholar
  5. Biere A, Antonovics J (1996) Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution 50:1098–1110CrossRefGoogle Scholar
  6. Boots M, Haraguchi Y (1999) The evolution of costly resistance in host-parasite systems. Am Nat 153:359–370CrossRefGoogle Scholar
  7. Boots M, White A, Best A, Bowers R (2014) How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites. Evolution 68:1594–1606PubMedCentralCrossRefPubMedGoogle Scholar
  8. Bowers RG, Boots M, Begon M (1994) Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proc R Soc Lond B 257:247–253CrossRefGoogle Scholar
  9. Boyd R, Richerson PJ (1992) Punishment allows the evolution of cooperation (or anything else) in sizeable groups. Ethol Sociobiol 13:171–195CrossRefGoogle Scholar
  10. Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217CrossRefPubMedGoogle Scholar
  11. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  12. Chaverri P, Samuels GJ (2013) Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution 67:2823–2837PubMedGoogle Scholar
  13. Connor RC (1995) The benefits of mutualism: a conceptual framework. Biol Rev 70:427–457CrossRefGoogle Scholar
  14. Darwin C (1859) On the origin of species by means of natural selection. John Murray, LondonGoogle Scholar
  15. De Mazancourt C, Schwartz MW (2010) A resource ratio theory of competition. Ecol Lett 13:349–359CrossRefPubMedGoogle Scholar
  16. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680PubMedCentralCrossRefPubMedGoogle Scholar
  17. Dreber A, Rand DG, Fudenberg D, Nowak MA (2008) Winners don’t punish. Nature 452:348–351PubMedCentralCrossRefPubMedGoogle Scholar
  18. Egger KN (2006) The surprising diversity of ascomycetous mycorrhizas. New Phytol 170:421–423CrossRefPubMedGoogle Scholar
  19. Fehr E, Gächter S (2002) Altruistic punishment in humans. Nature 415:137–140CrossRefPubMedGoogle Scholar
  20. Fenton A, Antonovics J, Brockhurst MA (2009) Inverse gene-for-gene infection genetics and coevolutionary dynamics. Am Nat 174:E230–E242CrossRefPubMedGoogle Scholar
  21. Genkai-Kato M, Yamamura N (1999) Evolution of mutualistic symbiosis without vertical transmission. Theor Popul Biol 55:309–323CrossRefPubMedGoogle Scholar
  22. Gimelfarb A (1988) Processes of pair formation leading to assortative mating in biological populations: encounter-mating model. Am Nat 131:865–884CrossRefGoogle Scholar
  23. Gorton AJ, Heath KD, Pilet-Nayel ML, Baranger A, Stinchcombe JR (2012) Mapping the genetic basis of symbiotic variation in legume-rhizobium interactions in Medicago trunculata. G3: Genes Genomes Genet 2:1291–1303CrossRefGoogle Scholar
  24. Hacskaylo E (1972) Mycorrhiza: the ultimate in reciprocal parasitism. BioScience 22:577–583CrossRefGoogle Scholar
  25. Hadeler KP (1989) Pair formation in age structured populations. Acta Appl Math 14:91–102CrossRefPubMedGoogle Scholar
  26. Heath KD, Tiffin P (2007) Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc Lond B 274:1905–1912CrossRefGoogle Scholar
  27. Heil M, Gonzalez-Teuber M, Clement LW, Kautz S, Verhaagh M, Bueno JCS (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096PubMedCentralCrossRefPubMedGoogle Scholar
  28. Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602CrossRefPubMedGoogle Scholar
  29. Herre EA, Knowlton N, Mueller U, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53CrossRefPubMedGoogle Scholar
  30. Holland JN, DeAngelis DL (2010) A consumer-resource approach to density-dependent population dynamics of mutualism. Ecology 91:1286–1295CrossRefPubMedGoogle Scholar
  31. Hom EFY, Murray AW (2014) Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345:94–98PubMedCentralCrossRefPubMedGoogle Scholar
  32. Irwin R, Bronstein JL, Manson JS, Richardson LE (2010) Nectar-robbing: ecological and evolutionary perspectives. Ann Rev Ecol Evol Syst 41:271–292CrossRefGoogle Scholar
  33. Jansen VAA, van Baalen M (2006) Altruism through beard chromodynamics. Nature 440:663–666CrossRefPubMedGoogle Scholar
  34. Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275CrossRefGoogle Scholar
  35. Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474CrossRefGoogle Scholar
  36. Kostitzin VA (1935) Symbiosis, parasitism, and evolution. Reprinted in Scudo FM, Ziegler JR (1978) The golden age of theoretical ecology, 1923–1940. Lect Notes Biomath 22:369–408Google Scholar
  37. Law R, Dieckmann U (1998) Symbiosis through exploitation and the merger of lineages in evolution. Proc R Soc Lond B 265:1245–1253CrossRefGoogle Scholar
  38. Lewis HM, Dumbrell AJ (2013) Evolutionary games of cooperation: insights through integration of theory and data. Ecol Complex. doi: 10.1016/j.ecocom.2013.02.007 Google Scholar
  39. Maynard Smith J (1979) Game theory and the evolution of behaviour. Proc R Soc Lond B 205:475–488CrossRefGoogle Scholar
  40. Merckx V, Freudenstein JV (2010) Evolution of mycoheterotrophy in plants: a phylogenetic perspective. New Phytol 185:605–609CrossRefPubMedGoogle Scholar
  41. Noë R, van Hoof J, Hammerstein P (2001) Economics in nature. Social dilemmas, mate choice and biological markets. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  42. Nowak MA (2006) Five rules for the evolution of co-operation. Science 314:1560–1563PubMedCentralCrossRefPubMedGoogle Scholar
  43. Pande S, Merker H, Bohl K, Reichelt M, Schuster S, de Figueiredo LF, Kaleta C, Kost C (2014) Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J 8:953–962PubMedCentralCrossRefPubMedGoogle Scholar
  44. Ronsheim M (1997) Distance-dependent performance of asexual progeny in Allium vineale. Am J Bot 84:1279–1284CrossRefPubMedGoogle Scholar
  45. Sachs JL, Simms EL (2008) The origins of uncooperative rhizobia. Oikos 117:961–966Google Scholar
  46. Sachs JL, Skophammer RG, Regus JU (2011) Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci USA 108(Suppl. 2):10800–10807PubMedCentralCrossRefPubMedGoogle Scholar
  47. Sasaki A (2000) Host-parasite coevolution in a multilocus gene-for-gene system. Proc R Soc Lond B 257:2183–2188CrossRefGoogle Scholar
  48. Scheuring I (2005) The iterated continuous Prisoner’s Dilemma game cannot explain the evolution of interspecific mutualism in unstructured populations. J Theor Biol 232:99–104CrossRefPubMedGoogle Scholar
  49. Soetaert K, Petzoldt T, Setzer RW (2010) Solving differential equations in R: package deSolve. J Stat Softw 33:1–25Google Scholar
  50. Tan J, Zuniga C, Zengler K (2015) Unraveling interactions in microbial communities—from co-cultures to microbiomes. J Microbiol 53:295–305CrossRefPubMedGoogle Scholar
  51. Tanouchi Y, Smith RP, You L (2012) Engineering microbial systems to explore ecological and evolutionary dynamics. Curr Opin Biotech 23:791–797PubMedCentralCrossRefPubMedGoogle Scholar
  52. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263CrossRefPubMedGoogle Scholar
  53. Tschirren B, Andersson M, Scherman K, Westerdahl H, Raberg L (2012) Contrasting patterns of diversity and population differentiation at the innate immunity gene toll-like receptor 2 (TLR2) in two sympatric rodent species. Evolution 66:720–731CrossRefPubMedGoogle Scholar
  54. van Baalen M, Jansen AA (2001) Dangerous liaisons: the ecology of private interest and public good. Oikos 95:211–224CrossRefGoogle Scholar
  55. Veiga RSL, Faccio A, Genre A, Pieterse CM, Bonfante P, van der Heiden MGA (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937PubMedGoogle Scholar
  56. Veldre V, Abarenkov K, Bahram M, Martos F, Selosse M, Tamm H, Koljalg U, Tedersoo L (2013) Evolution of nutritional modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) as revealed from publicly available ITS sequences. Fungal Ecol 6:256–268CrossRefGoogle Scholar
  57. Vila-Aiub MM, Neve P, Roux F (2011) A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:386–394PubMedCentralPubMedGoogle Scholar
  58. Wang Z, Wu M (2014) Phylogenomic reconstruction indicates mitochondrial ancestor was an energy parasite. Plos One 9:e11685Google Scholar
  59. Webster JP, Woolhouse MEJ (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proc R Soc Lond B 266:391–396CrossRefGoogle Scholar
  60. West SA, El Mouden C, Gardner A (2011) Sixteen common misconceptions about the evolution of co-operation in humans. Evol Hum Behav 32:231–262CrossRefGoogle Scholar
  61. Wilkinson DM (1997) The role of seed dispersal in the evolution of mycorrhizae. Oikos 78:394–396CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Institut für BiologieFreie Universität BerlinBerlinGermany
  2. 2.Biology DepartmentUniversity of VirginiaCharlottesvilleUSA
  3. 3.Department of BiologyUniversity of Antwerp, PLECOWilrijkBelgium

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