Coevolutionary Arms Races and the Conditions for the Maintenance of Mutualism

Abstract

Empirical evidence suggests that coevolutionary arms races between flowering plants and their pollinators can occur in wild populations. In extreme cases, trait escalation may result in evolutionary switching from mutualism to parasitism. However, theoretical approaches to studying coevolution typically assume fixed types of ecological interactions and ignore the evolution of absolute fitness. Here, we introduce a novel approach to track the evolution of absolute fitness as a framework to determine when escalatory coevolution results in a switch from mutualism to parasitism. We apply our approach to two previously studied mechanisms mediating selection as a function of phenotype. Our results demonstrate that interactions mediated by a “bigger-is-better” mechanism evolve toward parasitism. In contrast, generalizing the classical trait-matching mechanism so that the fitness of each species is optimized when trait values mismatch by a particular amount, we find theoretical support for indefinite trait exaggeration that preserves mutualistic interactions. Building on our results, we discuss the consequences of coevolutionary arms races for the maintenance of cheating. Moving beyond pairwise interactions, we consider the ramifications of coevolution in a South African pollination network for the evolution of parasitism. Future work extending our approach beyond pairwise interactions can lead to a framework for understanding the evolution of parasitism in mutualistic networks and further insights into the structure and dynamic nature of ecological communities in general.