Mating preferences of selfish sex chromosomes

The evolution of female mating preferences for harmful male traits is a central paradox of sexual selection^1-9. Two dominant explanations for this paradox^8,10 are Fisher's runaway process, which is based on genetic correlations between preference and trait^1,3,4, and Zahavi's handicap principle, in which the trait is an honest costly signal of male quality^2,6,8,11. However, both of these explanations require the exogenous initial spread of female preferences before harmful male traits can evolve^1-4,6,8,11. Here I present a mechanism for the evolution of female mating preferences for harmful male traits that is based on the selfish evolutionary interests of sex chromosomes. I demonstrate that female-biased genetic elements-such as the W and X sex chromosomes-will evolve mating preferences for males who display traits that reduce their fitness and/or that of their male offspring, but increase fitness in female offspring. In particular, W-linked preferences can cause nearly lethal male traits to sweep to fixation. Sex-linked preferences can drive the evolution of traits such as ornamental handicaps and male parental care, and can explain variation in ornamentation and behaviour across taxa with divergent sex-determining mechanisms.