AbstractHormones mediate sexual dimorphism by regulating sex-specific patterns of gene expression, but it is unclear how much of this regulation involves sex-specific hormone levels versus sex-specific transcriptomic responses to the same hormonal signal. Moreover, transcriptomic responses to hormones can evolve, but the extent to which hormonal pleiotropy in gene regulation is conserved across closely related species is not well understood. We addressed these issues by elevating testosterone levels in juvenile females and males of three Sceloporus lizard species before sexual divergence in circulating testosterone and then characterizing transcriptomic responses in the liver. In each species, more genes were responsive to testosterone in males than in females, suggesting that early developmental processes prime sex-specific transcriptomic responses to testosterone later in life. However, overall transcriptomic responses to testosterone were concordant between sexes, with no genes exhibiting sex-by-treatment interactions. By contrast, hundreds of genes exhibited species-by-treatment interactions, particularly when comparing distantly related species with different patterns of sexual dimorphism, suggesting evolutionary lability in gene regulation by testosterone. Collectively, our results indicate that early organizational effects may lead to sex-specific differences in the magnitude, but not the direction, of transcriptomic responses to testosterone and that the hormone-genome interface accrues regulatory changes over evolutionary time.
Keywords: evolutionary endocrinology; evolutionary potential hypothesis; organizational/activational hypothesis; pleiotropy; sexual dimorphism.