Sexually Antagonistic Coevolution in a Mating System: Combining Experimental and Comparative Approaches to Address Evolutionary Processes

Abstract

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 (Ͼ 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.Key words. Arms races, Gerridae, macroevolution, mating systems, sexual conflict, sexual selection. Research on sexual selection and mating systems is increasingly focused on sexual conflict and the resulting potential for antagonistic coevolution between the sexes. A diverse array of male and female traits (morphological, behavioral, and physiological) that further the interests of one sex over the other have the potential to coevolve antagonistically. These include subtle signal-reception systems involving ejaculate components of males and receptors in females (e.g., Chapman et al. 1995;Wolfner 1997;Clark et al. 1999; Andrés and Arnqvist 2001), coercive behaviors (reviewed in CluttonBrock and Parker 1995), and overt grasping and antigrasping structures of males and females (e.g., Arnqvist 1989a; Thornhill and Sauer 1991;Arnqvist and Rowe 1995;Sakaluk et al. 1995). Sexual conflict is now viewed as having the potential to be a preeminent force driving the evolution of mating rate and those traits affecting this rate (Parker 1979;Gowat...

Female Polymorphism, Frequency Dependence, and Rapid Evolutionary Dynamics in Natural Populations

“…Recent empirical work on several different taxa (Bergsten et al 2001;Arnqvist andRowe 2002a, 2002b;Rowe and Arnqvist 2002) suggests that sexual conflict may have important evolutionary consequences in natural populations. The results in this study add further evidence to this but do also suggest that the evolutionary dynamics of sexual conflict may include a strong frequency-dependent component.…”

Evolution of genitalia: theories, evidence, and new directions

“…Dorsally projecting spines near the female's genitalia are elongated to different degrees in different species, and have independently become especially elongate in Gerris incognitus and Gerris odontogaster. Longer female spines impede male attempts to clamp the tip of the female's abdomen with his genitalia (Arnqvist and Rowe 2002a, b;Rowe and Arnqvist 2002). Such clamping helps the male hold onto the female during her energetic struggles when he mounts, and is a necessary prelude to intromission.…”

Detecting sexually antagonistic coevolution with population crosses

“…Conflicts occur over a wide variety of traits, including mating rate (Rowe et al 1994;Choe & Crespi 1997;, oviposition rate (Chapman et al 1995;Eberhard 1996) and offspring provisioning (Trivers 1972;Haig 2000). Traits apparently coevolving to further the interests of one sex over the other in these conflicts include grasping and antigrasping structures (Bergsten et al 2001;Arnqvist & Rowe 2002a), male seminal signals and female receptors (Chapman 2001;Swanson & Vacquier 2002), reproductive tract morphology (Presgraves et al 1999;Miller & Pitnick 2002;Miller & Pitnick 2003) and mating behaviours (Rowe & Arnqvist 2002). A central prediction of sexually antagonistic coevolution is that these traits will evolve very rapidly, thereby generating divergence in isolated populations and perhaps speciation (Rice 1998;Howard et al 1998;Parker & Partridge 1998;Gavrilets 2000;Gavrilets et al 2001;Gavrilets & Waxman 2002).…”