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

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Abstract

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.

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Acknowledgments

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.

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  1. Janis Antonovics

    Present address: Biology Department, University of Virginia, Charlottesville, VA, 22904, USA

Authors and Affiliations

  1. Institut für Biologie, Freie Universität Berlin, 14195, Berlin, Germany

    Janis Antonovics, Joana Bergmann, Stefan Hempel, Erik Verbruggen, Stavros Veresoglou & Matthias Rillig

  2. Department of Biology, University of Antwerp, PLECO, Universiteitsplein 1, 2610, Wilrijk, Belgium

    Erik Verbruggen

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  1. Janis Antonovics
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Correspondence to Janis Antonovics.

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Antonovics, J., Bergmann, J., Hempel, S. et al. The evolution of mutualism from reciprocal parasitism: more ecological clothes for the Prisoner’s Dilemma. Evol Ecol 29, 627–641 (2015). https://doi.org/10.1007/s10682-015-9775-6

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