Evolution of sex-biased genes in Drosophila species with neo-sex chromosomes: potential contribution to reducing sexual conflict

An advantage of sex chromosomes is the potential to reduce sexual conflict because they provide a basis for selection to operate separately on females and males. However, evaluating the relationship between sex chromosomes and sexual conflict is challenging owing to the difficulty in measuring sexual conflict and substantial divergence between species with and without sex chromosomes. We therefore examined sex-biased gene expression as a proxy for sexual conflict in three sets of Drosophila species with and without young sex chromosomes, the so-called neo-sex chromosomes. In all sets, we detected more sex-biased genes in the species with neo-sex chromosomes than in the species without neo-sex chromosomes in larvae, pupae, and adult somatic tissues but not in gonads. In particular, many unbiased genes became either female- or male-biased after linkage to the neo-sex chromosomes in larvae, despite the low sexual dimorphism in larvae. However, sexual dimorphism at the adult stage can be a consequence of sexual conflict at the larval stage. For example, larval body size and rate of development are likely targets of sexually antagonistic selection (i.e., large size and rapid development are selected for in females but selected against in males). Indeed, genes involved in metabolism, a key determinant of the rate of development in many animals, were enriched in the genes that acquired sex-biased expression on the neo-sex chromosomes at the larval stage. These results indicate that acquiring neo-sex chromosomes may have contributed to a reduction in sexual conflict, particularly at the larval stage, in Drosophila.