Gene Expression and the Evolution of Reduced Sexual Dimorphism in a Threespine Stickleback Color Trait

Abstract

Elucidating the processes and mechanisms responsible for sexual dimorphism has been a central task for evolutionary biologists since Darwin first proposed the concept of sexual selection. However, our understanding of the genetic basis for variation in sexual dimorphism remains notably incomplete. Here we used a well-established evolutionary model, the threespine stickleback, to examine the genomic basis for variation in orange-red throat coloration, a trait long thought confined to males, and outline broad genetic patterns among and between populations where females have adopted this male-typical trait. Specifically, RNA-Seq was performed on stickleback throat and brain tissues from five populations: two expressing standard sexual dimorphism for throat coloration (red males and relatively dull females) and three expressing chromatic monomorphism (two where both sexes express red throat coloration, one where both largely lack this trait). We find that chromatically monomorphic populations show an overall decrease in sexually dimorphic gene expression, in both populations in throat tissue and in only one in brain tissue, relative to fish from standard sexually dimorphic populations. Variation in this trait is substantial between populations, tissues, and sets of sex-biased genes, and populations with red females appear to have independently converged onto a similar phenotype by separate genetic mechanisms. Additionally, we identified roles for melanin signaling pathways in throat tissue and, although no carotenoid pathways were enriched, a handful of carotenoid related genes were differentially expressed. These results appear to suggest that an overall decrease in sexual dimorphism, replicated independently in two geographically distinct populations, accompanies the rise of a male-typical trait in female sticklebacks.