Mating Preferences of Selfish Sex Chromosomes

Abstract

The evolution of female mating preferences for harmful male traits is a central paradox of sexual selection. Two dominant explanations of this paradox8,10 are Fisher’s runaway process, based on genetic correlations between preference and trait, and Zahavi’s handicap principle, where the trait is an honest costly signal of male quality. However, both require an exogenous initial spread of the female preferences before harmful male traits can evolve. Here, I present a novel mechanism for the evolution of female preferences for harmful male traits, based on the distinct evolutionary interests of sex chromosomes. I demonstrate that female-biased genetic elements, including the W and X sex chromosomes, will evolve mating preferences for males who display traits that reduce fitness in males but increase fitness in female offspring. W-linked preferences, in particular, 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.