Social Epistasis Amplifies the Fitness Costs of Deleterious Mutations, Engendering Rapid Fitness Decline Among Modernized Populations

Abstract

Deleterious mutations are typically understood exclusively in terms of their harmful effects on carrier organisms. But there are convincing reasons to think that such adverse effects are not confined to the individual level. We argue that in social species, interorganismal gene-gene interactions, which in previous literatures have been termed social epistasis, allow genomes carrying deleterious mutations to reduce via group-level pleiotropy the fitness of others, including noncarriers. This fitness reduction occurs by way of degradation of group-level processes that optimize the reproductive ecology of a population for intergroup competition through, among other mechanisms, suppression of free-riding. Such damage to group regulatory processes suggests a hidden role for the accumulation of behavior-altering "spiteful" mutations in the dynamics of the demographic transition—these mutations may have contributed to the maladaptive outcomes of this process, such as widespread subreplacement fertility. A structured population model is presented describing aspects of this social epistasis amplification model. This phenomenon is also considered as a potential explanation for the results of Calhoun’s mouse utopia experiments, which provide an opportunity to directly test a major prediction stemming from the model.