Explaining Mutualism Variation: A New Evolutionary Paradox?

Abstract

The paradox of mutualism is typically framed as the persistence of interspecific cooperation, despite the potential advantages of cheating. Thus, mutualism research has tended to focus on stabilizing mechanisms that prevent the invasion of low-quality partners.These mechanisms alone cannot explain the persistence of variation for partner quality observed in nature, leaving a large gap in our understanding of how mutualisms evolve. Studying partner quality variation is necessary for applying genetically explicit models to predict evolution in natural populations, a necessary step for understanding the origins of mutualisms as well as their ongoing dynamics. An evolutionary genetic approach, which is focused on naturally occurring mutualist variation, can potentially synthesize the currently disconnected fields of mutualism evolution and coevolutionary genetics. We outline explanations for the maintenance of genetic variation for mutualism and suggest approaches necessary to address them. K E Y W O R D S :Coevolution, cooperation, partner choice, partner fidelity feedback, public goods, quantitative genetics, screening.The evolutionary paradox of interspecific mutualisms, as typically posed, refers to the apparent disagreement between theoretical predictions that (all else being equal) selection should favor cheaters, and empirical observations of generally positive interactions and long-term cooperation between species. Theoretical and empirical studies alike, motivated by this seeming paradox, have made much progress toward understanding the selective mechanisms that favor interspecific mutualism and thus explaining the long-term persistence of mutualisms despite the potential fitness advantages of cheating (Bshary and Grutter 2002;Kiers et al. 2003;Sachs et al. 2004;Heath and Tiffin 2009;Leigh 2010;Archetti et al. 2011b;Jander et al. 2012). Here we argue, however, that we are missing a fundamental aspect of mutualism evolution that would allow faster progress toward understanding the more general question of how mutualisms evolve, in the larger context of species interactions, as opposed to simply what selects for cooperative mutualist partners. We suggest that a critical question in mutualism evolution is what maintains genetic variation for partner quality in mutualisms?Answering this question will require researchers to apply evolutionary genetic methods to the study of genetic variation in mutualisms. Viewing mutualistic interactions through the lens of the maintenance of genetic variation, a classic framework shared by all of evolutionary biology, can (1) bridge the divide between the largely disconnected fields of coevolutionary genetics and mutualism evolution; and (2) provide a more predictive understanding of how mutualisms evolve. Given the importance of these interactions to natural and managed systems, including human health, a predictive understanding of mutualism evolution is an important goal. We first define what we mean by "genetic variation in mutualism," then describe why we believe that it i...

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