Parasites of mutualisms

Abstract

Cooperation invites cheating, and nowhere is this more apparent than when different species cooperate, known as mutualism. In almost all mutualisms studied, specialist parasites have been identified that purloin the benefits that one mutualist provides another. Explaining how parasites are kept from driving mutualisms extinct remains an unsolved problem because existing theories explaining the maintenance of cooperation do not apply to parasites of mutualisms. Nonetheless, these theories can be summarized in such a way as to suggest how mutualisms can persist in the face of parasites. (1) For cooperation to occur, the recipient of a benefit must reciprocate, and the recriprocated benefit must be captured by the initial giver or its offspring. (2) For cooperation to persist, the mutualism must be re-assembled each generation. Because most mutualisms are of the “by-product‘ type, broadly defined, the first condition is normally always fulfilled. Thus, the maintenance of mutualism usually requires enforcement of the second condition: reliable re-assembly. Hence, I argue that the persistence of mutualism is best understood by using theories of species coexistence, because each mutualist can be considered a resource for the other, and species coexistence theory explains how multiple taxa (e.g. parasites and mutualists) can stably partition a resource over multiple generations. This approach connects the study of mutualism to theories of population regulation and helps to identify key factors that have promoted the evolution, maintenance and breakdown of mutualism. I discuss how these ideas might apply to and be tested in ant-plant, fig-wasp and yucca-moth mutualisms.