Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes

Abstract

We combined experimental and comparative techniques to study the evolution of mating behaviors within in a clade of 15 water striders (Gerris spp.). Superfluous multiple mating is costly to females in this group, and consequently there is overt conflict between the sexes over mating. Two alternative hypotheses that could generate interspecific variation in mating behaviors are tested: interspecific variation in optimal female mating rate versus sexually antagonistic coevolution of persistence and resistance traits. These potentially coevolving traits include male grasping and female antigrasping structures that further the interests of one sex over the other during premating struggles. Both processes are known to play a role in observed behavioral variation within species. We used two large sets of experiments to quantify behavioral differences among species, as well as their response to an environmentally (sex-ratio) induced change in optimal female mating rate. Our analysis revealed a large degree of continuous interspecific variation in all 20 quantified behavioral variables. Nevertheless, species shared the same set of behaviors, and each responded in a qualitatively similar fashion to sex-ratio alterations. A remarkably large proportion (> 50%) of all interspecific variation in the magnitude of behaviors, including their response to sex ratio, could be captured by a single multivariate axis. These data suggest tight coevolution of behaviors within a shared mating system. The pattern of correlated evolution was best accounted for by antagonistic coevolution in the relative abilities of each sex to control the outcome of premating struggles. In species where males have a relative advantage, mating activity is high, and the opposite is found in species where females have gained a relative advantage. Our analyses also suggested that evolution has been unconstrained by history, with no consistent evolutionary tendency toward or away from male or female relative advantage.