Mating environments mediate the evolution of behavioral isolation during ecological speciation.

The evolution of behavioral isolation is often the first step toward speciation. While past studies show that behavioral isolation will sometimes evolve as a by-product of divergent ecological selection, we lack a more nuanced understanding of factors that may promote or hamper its evolution. The environment in which mating occurs may be important in mediating whether behavioral isolation evolves for two reasons. Ecological speciation could occur as a direct outcome of different sexual interactions being favored in different mating environments. Alternatively, mating environments may vary in the constraint they impose on traits underlying mating interactions, such that populations evolving in a "constraining" mating environment would be less likely to evolve behavioral isolation than populations evolving in a less constraining mating environment. In the latter, mating environment is not the direct cause of behavioral isolation but rather permits its evolution only if other drivers are present. We test these ideas with a set of 28 experimental fly populations, each of which evolved under one of two mating environments and one of two larval environments. Counter to the prediction of ecological speciation by mating environment, behavioral isolation was not maximal between populations evolved in different mating environments. Nonetheless, mating environment was an important factor as behavioral isolation evolved among populations from one mating environment but not among populations from the other. Though one mating environment was conducive to the evolution of behavioral isolation, it was not sufficient: assortative mating only evolved between populations adapting to different-larval environments within that mating environment, indicating a role for ecological speciation. Intriguingly, the mating environment that promoted behavioral isolation is characterized by less sexual conflict compared to the other mating environment. Our results suggest that mating environments play a key role in mediating ecological speciation via other axes of divergent selection.

Competition for mates and the improvement of nonsexual fitness.

Competition for mates can be a major source of selection, not just on secondary sexual traits but across the genome. Mate competition strengthens selection on males via sexual selection, which typically favors healthy, vigorous individuals and, thus, all genetic variants that increase overall quality. However, recent studies suggest another major effect of mate competition that could influence genome-wide selection: Sexual harassment by males can drastically weaken selection on quality in females. Because of these conflicting effects, the net effect of mate competition is uncertain, although perhaps not entirely unpredictable. We propose that the environment in which mate competition occurs mediates the importance of sexual selection relative to sexual conflict and, hence, the net effect of mate competition on nonsexual fitness. To test this, we performed experimental evolution with 63 fruit fly populations adapting to novel larval conditions where each population was maintained with or without mate competition. In half the populations with mate competition, adults interacted in simple, high-density environments. In the remainder, adults interacted in more spatially complex environments in which male-induced harm is reduced. Populations evolving with mate competition in the complex environment adapted faster to novel larval environments than did populations evolving without mate competition or with mate competition in the simple environment. Moreover, mate competition in the complex environment caused a substantial reduction in inbreeding depression for egg-to-adult viability relative to the other two mating treatments. These results demonstrate that the mating environment has a substantial and predictable effect on nonsexual fitness through adaptation and purging.