Sex-biased gene expression under sexually antagonistic and sex-limited selection

Sex differences in gene expression are ubiquitous, evolve quickly, and are expected to underlie phenotypic sexual dimorphism. Despite long-standing interest, the impact of sex-specific selection on the transcriptome remains poorly understood. Here, we test fundamental questions on the role of constraints on gene expression evolution arising from the mode of selection and genetic architecture. We also test the relationship between sex-specific selection, sex-biased expression and sexual dimorphism (SD). We assess these using body size selection lines in the seed beetle, Callosobruchus maculatus , that have evolved variation in SD in response to sex-specific selection; either sex-limited (SL) or sexually antagonistic (SA). We find that the evolution of male-optimal smaller size is associated with an excess of expression changes of transcripts with male-biased expression, and female-optimal larger size with a deficit of changes at transcripts with female-biased expression. Expression changes are more constrained under SA selection, and especially in females, reflecting phenotypic evolution in these lines. Although SD in size has changed most under SA selection, we show that similar SL selection on males, but not females, has resulted in more sex-biased transcripts. Consequently, we find no clear transcriptome-wide association between sex-bias and SD. Overall, sex-biased transcripts show lower cross-sex correlations in expression changes than unbiased transcripts. In the light of these unique experimental insights into how sex-specific selection on size changes adult transcription, our findings have strong implications for inferring selection history and mode from patterns of sex-biased gene expression in natural populations.