A Cost of Sexual Attractiveness to High-Fitness Females

Abstract

Females are frequently harassed and harmed by males attempting to obtain matings. When these males are also “choosy” with their courtship, there may be negative consequences to the species' ability to adaptively evolve.

Abstract

Adaptive mate choice by females is an important component of sexual selection in many species. The evolutionary consequences of male mate preferences, however, have received relatively little study, especially in the context of sexual conflict, where males often harm their mates. Here, we describe a new and counterintuitive cost of sexual selection in species with both male mate preference and sexual conflict via antagonistic male persistence: male mate choice for high-fecundity females leads to a diminished rate of adaptive evolution by reducing the advantage to females of expressing beneficial genetic variation. We then use a Drosophila melanogaster model system to experimentally test the key prediction of this theoretical cost: that antagonistic male persistence is directed toward, and harms, intrinsically higher-fitness females more than it does intrinsically lower-fitness females. This asymmetry in male persistence causes the tails of the population's fitness distribution to regress towards the mean, thereby reducing the efficacy of natural selection. We conclude that adaptive male mate choice can lead to an important, yet unappreciated, cost of sex and sexual selection.

Author Summary

In many species, females are frequently subject to harassing courtship from males attempting to mate with them. These persistent male behaviors can result in females incurring substantial direct fitness costs. We set out to examine how these costs may influence adaptive potential in a species that also exhibits male mate choice, i.e., a preference by males for females exhibiting certain traits. We found that harmful courtship behaviors were directed predominantly towards females of greater reproductive potential (and away from females of lesser potential), resulting in a reduction in the variation of lifetime reproductive successes among females in the population. This change in distribution of realized fitnesses represents a previously unappreciated consequence of sexual conflict–adaptive male mate preference can slow the rate of accumulation of beneficial mutations and speed the rate of accumulation of harmful mutations, thereby creating a “sexual conflict adaptive load” within a species.