Hormonally Mediated Increases in Sex-Biased Gene Expression Accompany the Breakdown of Between-Sex Genetic Correlations in a Sexually Dimorphic Lizard

Abstract

The evolution of sexual dimorphism is predicted to occur through reductions in between-sex genetic correlations (r_mf) for shared traits, but the physiological and genetic mechanisms that facilitate these reductions remain largely speculative. Here, we use a paternal half-sibling breeding design in captive brown anole lizards (Anolis sagrei) to show that the development of sexual size dimorphism is mirrored by the ontogenetic breakdown of r_mf for body size and growth rate. Using transcriptome data from the liver (which integrates growth and metabolism), we show that sex-biased gene expression also increases dramatically between ontogenetic stages bracketing this breakdown of r_mf. Ontogenetic increases in sex-biased expression are particularly evident for genes involved in growth, metabolism, and cell proliferation, suggesting that they contribute to both the development of sexual dimorphism and the breakdown of r_mf. Mechanistically, we show that treatment of females with testosterone stimulates the expression of male-biased genes while inhibiting the expression of female-biased genes, thereby inducing male-like phenotypes at both organismal and transcriptomic levels. Collectively, our results suggest that sex-specific modifiers such as testosterone can orchestrate sex-biased gene expression to facilitate the phenotypic development of sexual dimorphism while simultaneously reducing genetic correlations that would otherwise constrain the independent evolution of the sexes.