Rapid Adaptation to Mammalian Sociality via Sexually Selected Traits

Abstract

Background: Laboratory studies show that the sexual selection via mate choice and intrasexual competition can profoundly affect the development and fitness of offspring. Less is known, however, about the total effects of sexual selection on offspring in normal social conditions. For many animals, opportunity for mating success is determined by complex social interactions, such as dominance hierarchies. Social selection is an extended view of sexual selection that incorporates competition during sexual and nonsexual interactions, and predicts complex evolutionary dynamics. Whether social selection improves or constrains offspring fitness is controversial. Results: To characterize the consequences of social selection, we introduced wild-derived mice to seminatural competition for three consecutive generations (promiscuous lineage). In parallel, we bred a control lineage in cages using random mate assignment (monogamous lineage). A direct competition experiment using second-generation animals revealed that promiscuous line males had greater reproductive success than monogamous line males (particularly during extrapair matings), in spite of higher mortality and equivalent success in social dominance and sperm competition. There were no major female fitness effects, though promiscuous line females had fewer litters than monogamous line females. We confirmed a behavioral sexual attraction mechanism by showing that, when given a choice, females had both odor and mating preferences for promiscuous line over monogamous line males. Conclusions: Our study demonstrates novel evidence for the strength of sexual selection under normal social conditions, and shows rapid male adaptation to sociality driven largely by sexual trait expression, with tradeoffs in survivorship and female fecundity. The speed at which these phenotypes emerged suggests the possibility of transgenerational inheritance. Mouse population densities fluctuate dramatically in nature, and we propose that sexually selected phenotypes arise dynamically during periods of social competition.