Sexual conflict and the gender load: correlated evolution between population fitness and sexual dimorphism in seed beetles

Abstract

Although males and females share much of the same genome, selection is often distinct in the two sexes. Sexually antagonistic loci will in theory cause a gender load in populations, because sex-specific selection on a given trait in one sex will compromise the adaptive evolution of the same trait in the other sex. However, it is currently not clear whether such intralocus sexual conflict (ISC) represents a transient evolutionary state, where conflict is rapidly resolved by the evolution of sexual dimorphism (SD), or whether it is a more chronic impediment to adaptation. All else being equal, ISC should manifest itself as correlated evolution between population fitness and SD in traits expressed in both sexes. However, comparative tests of this prediction are problematic and have been unfeasible. Here, we assess the effects of ISC by comparing fitness and SD across distinct laboratory populations of seed beetles that should be well adapted to a shared environment. We show that SD in juvenile development time, a key life-history trait with a history of sexually antagonistic selection in this model system, is positively related to fitness. This effect is due to a correlated evolution between population fitness and development time that is positive in females but negative in males. Loosening the genetic bind between the sexes has evidently allowed the sexes to approach their distinct adaptive peaks.

Figure 1.

Schematic illustration of the gender load. Because of differences in the optimal life-history trade-offs between the sexes, male (dashed line) and female (solid line) fitness functions typically differ. Whenever the evolution of SD in a trait expressed in both sexes is constrained, males (dark grey distribution) and females (light grey distribution) will be unable to reach their optimal sex-specific phenotypes. This results in a population fitness (W*) that is lower than that achieved when both sexes are free to evolve to reside on their adaptive peaks (W_max). Although sexually antagonistic selection (arrows) will act to increase SD in an evolutionary tug-of-war known as intralocus sexual conflict, the genetic bind between the sexes causes a fitness depression constituting the gender load (GL), or SD load (Rice 1992). Thus, the evolution of increased SD should be associated with elevated population fitness. This key prediction is, however, contingent upon all else being equal, which complicates the interpretation of comparative tests of this prediction.

Figure 2.

The relationship between SD and population fitness in seed beetles. Here, population fitness is plotted against SD in juvenile development time across populations, measured as the SD index (SDI = F/M − 1; r_p = 0.65, p_dir = 0.011; randomization test based on 10 000 random permutations). Line represents conventional linear regression.

Figure 3.

The relationship between male and female development time (in days) and population fitness in seed beetles. Note that elevated population fitness is associated with a relatively long development time in females and a relatively short development time in males.