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Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization

Authors

  • Régis Ferrière,

    Corresponding author
    1. Laboratoire d'Ecologie, Unit of Mathematical Eco-Evolutionary Biology, Ecole Normale Supérieure, 46 rue d'Ulm, 75230 Paris Cedex 05, France
    2. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
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    • These authors contributed equally to this work.

  • Mathias Gauduchon,

    1. Laboratoire d'Ecologie, Unit of Mathematical Eco-Evolutionary Biology, Ecole Normale Supérieure, 46 rue d'Ulm, 75230 Paris Cedex 05, France
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    • These authors contributed equally to this work.

  • Judith L. Bronstein

    1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
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E-mail: regis.ferriere@ens.fr

Abstract

Mutualisms are ubiquitous in nature, as is their exploitation by both conspecific and heterospecific cheaters. Yet, evolutionary theory predicts that cheating should be favoured by natural selection. Here, we show theoretically that asymmetrical competition for partners generally determines the evolutionary fate of obligate mutualisms facing exploitation by third-species invaders. When asymmetry in partner competition is relatively weak, mutualists may either exclude exploiters or coexist with them, in which case their co-evolutionary response to exploitation is usually benign. When asymmetry is strong, the mutualists evolve towards evolutionary attractors where they become extremely vulnerable to exploiter invasion. However, exploiter invasion at an early stage of the mutualism's history can deflect mutualists’ co-evolutionary trajectories towards slightly different attractors that confer long-term stability against further exploitation. Thus, coexistence of mutualists and exploiters may often involve an historical effect whereby exploiters are co-opted early in mutualism history and provide lasting ‘evolutionary immunization’ against further invasion.

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