Do populations suffer a fitness cost due to sex differences in selection on shared traits?

Males and females share most of their genome and express many of the same traits, but the values of these shared traits that maximize survival and reproductive success often differ between the sexes. This sexually antagonistic selection can reduce the fitness of a population because genes that are maladaptive when expressed in females are maintained in the population because they are favored in males, and vice versa. This genomic tug-of-war is referred to as intralocus sexual conflict (Fig. 1).

Related Papers

Cox, R.M., and R. Calsbeek. 2009. Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. American Naturalist 173: 176-187.

Cox, R.M. and R. Calsbeek. Sex-specific selection and intraspecific variation in sexual size dimorphism. In press. Evolution.

Check out Ryan Calsbeek’s lab for other papers on sexual conflict and natural selection in the brown anole.

Figure 1. Stages in the evolution of sexual dimorphism in a hypothetical quantitative trait, illustrating the relationship between sexually antagonistic selection (arrows) and intralocus sexual conflict. Counterclockwise from top left: (1) Sexual conflict is absent when males and females share the same trait distribution and fitness surface for that trait. (2) When selection favors different fitness optima in each sex, a genomic “tug-of-war” ensues at the loci for the shared trait. This intralocus sexual conflict reduces the population’s fitness because genetic correlations prevent the phenotype of one or both sexes from evolving to its fitness optimum. (3) Conflict is gradually resolved as the loci subject to sexually antagonistic selection become sex-limited and sexual dimorphism evolves. (4) Conflict is fully resolved when male and female phenotypes reach their respective fitness optima. For sexually monomorphic or dimorphic traits, the intensity of intralocus sexual conflict can be inferred from the strength of sexually antagonistic selection on the phenotype. Modified from Cox & Calsbeek (2009).

Comparative meta-analysis. What aspects of natural and sexual selection generate intralocus sexual conflict? Does the evolution of sexual dimorphism mean that sexual conflict has been resolved? Or are dimorphic traits still subject to antagonistic selection? (Fig. 1). One way to answer these questions is to compare patterns of sexually antagonistic selection and sexual dimorphism in wild populations. Using a data set of selection estimates from 34 different animal species, Ryan Calsbeek and I found that the sexual antagonism is common in wild populations, and that the strongest sexual antagonism results from sex differences in selection on mating success (i.e., sexual selection) (Fig. 2a). Furthermore, sexual antagonism is weakest for monomorphic traits and strongest for highly dimorphic traits, suggesting that conflict often persists despite the evolution of sexual dimorphsim (Fig. 2b).

Sexual conflict in anoles. Ryan Calsbeek and I recently received funding from the National Science Foundation to study intralocus sexual conflict in the brown anole. This species exhibits extreme sexual dimorphism in body size and many other traits. Our long-term selection data from wild populations in The Bahamas reveal that natural selection acts antagonistically on many of these traits. Genetic paternity analyses also suggest that females may be able to mitigate the fitness costs of intralocus sexual conflict by mating with several males and then using sperm from large males to produce sons and sperm from small males to produce daughters. We are currently conducting a series of mate-choice trails that will enable us to determine whether females can sort sperm from alternative males, and to test whether this “cryptic mate choice” improves the fitness of progeny released to the wild.

Figure 2. Summary of 424 selection estimates on 88 traits from 34 wild animal populations. Strength of sexually antagonistic selection is greatest for (A) sexual selection (differential mating success) and net selection (total selection arising from viability, fecundity and mating success) and (B) traits that exhibit strong sexual dimorphism, suggesting unresolved conflict. Modified from Cox & Calsbeek (2009).

Figure 3. The brown anole exhibits extreme sexual size dimorphism that may be tied to underlying intralocus sexual conflict.