Abstract

Genetic variation in male traits and the female preferences for those traits allows for the evolution of sexual behavior. Trait-preference combinations are thought to improve the effectiveness of runaway sexual selection within a species, and are considered necessary for the induction of divergence between species. Novel traits, or variants of existing traits, and their associated preferences in the opposite sex are more likely to be maintained if they are genetically linked in proximity on a chromosome (the genetic coupling hypothesis), yet there is little empirical evidence that this genetic linkage occurs. Here we show for the first time that natural genetic variation at a single-linked region can induce both species-specific female choosiness and the male trait they are discriminating against. We found this effect in two separate regions of the genome, demonstrating that this linkage may be common. In contrast, female choosiness and male unattractiveness could not be alleviated by a single region. The close linkage of these loci and the strength of their effect provide an evolutionary means by which this preference-trait combination could arise and be maintained, thus enabling a more rapid route for runaway sexual selection, and providing empirical evidence supporting the genetic coupling hypothesis.

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