Feminization of sex-biased gene expression in a parthenogenetic stick insect suggests unresolved sexual antagonism in early development

Abstract

Sexual antagonism arises when males and females experience opposing selection on traits controlled by shared genetic architectures. For gene expression, such conflicts are typically resolved through the evolution of sex-biased regulation. Although sexual antagonism is often assumed to peak in adults, its developmental dynamics remain poorly understood. We investigated the ontogeny of sex-biased gene expression in the sexual stick insect Timema poppense and contrasted it with its parthenogenetic sister species to identify signatures of unresolved antagonism. Using RNA-seq across somatic tissues (brain, gut, legs, antennae) and reproductive tracts throughout post-embryonic development, we found that sex-biased expression in T. poppense is limited in somatic tissues but extensive in reproductive tracts from the earliest stages. Nearly half of the expressed genes are already sex-biased in first-instar gonads, with male- and female-biased genes largely stage-specific. Parthenogenetic females show masculinized expression in somatic tissues throughout development and in adult reproductive tracts, consistent with decay of sexual traits in the absence of mating. By contrast, they show feminized early gonadal expression, likely reflecting unresolved antagonism in the sexual ancestor. Our results reveal the ontogeny of sexual dimorphism in a hemimetabolous insect and suggest that focusing solely on adults underestimates the prevalence of unresolved sexual antagonism.