How Genotype-by-Environment Interactions Can Maintain Variation in Mutualisms

AbstractCoevolution requires reciprocal genotype-by-genotype (G × G) interactions for fitness, which occur when the fitness of a genotype in one species depends on the genotype it interacts with in another species and vice versa. However, in mutualisms, when G × G interactions are mutually beneficial, simple models predict that the resulting positive feedbacks will erode genetic variation. Here, we explore how genotype-by-environment (G × E) interactions, which occur when the fitnesses of different genotypes respond differently to different environments, and G × G × E interactions, which occur when the environment changes the outcome of G × G interactions, maintain variation in mutualisms. We build a spatial population genetic model in which the fitnesses of two partners depend on mutually beneficial G × G, G × E, and G × G × E interactions. Our analysis shows that variation will always be maintained via migration-selection balance with stronger G × E than G × G interactions. However, strong G × G interactions can erode variation by allowing genotypically matched partners to fix, and, more surprisingly, weak G × G interactions can erode variation by allowing genotypically mismatched partners to fix at high dispersal rates, leading to apparent maladaptation between partners. We parameterize our model using data from three published reciprocal transplant experiments, infer the relative strengths of G × E and G × G, and discuss the implications for the maintenance of genetic variation.