Evolution of sex-biased gene expression during transitions to separate sexes in the Silene genus.

Abstract

Sexual dimorphism is widespread among species with separate sexes, and its extent is thought to be governed by the differential expression of thousands of genes between males and females (known as Sex-Biased Genes, hereafter SBGs). SBGs have been studied in numerous species, but rarely through comparative approaches, which limits our understanding of their evolution, especially during multiple, independent transitions to separate sexes. We sequenced the transcriptomes of nine dioecious species (with separate males and females), two gynodioecious species (with separate females and hermaphrodites) and two hermaphrodite species from the Silene genus. Our dataset encompasses three independent transitions to dioecy, ranging from less than 1 million years ago (Mya) to about 11 Mya. We found that the number of both female and male-biased genes positively correlates with the age of separate sexes, with species with older sex separation exhibiting the most numerous sex-biased genes. More specifically, male-biased expression tends to emerge early, as soon as females coexist with hermaphrodites (gynodioecy). Numbers of female-biased genes are rare at first, and their numbers only increase after a transition to separate males and females (dioecy). Additionally, we found that both positive selection and genetic drift contribute to the evolution of SBGs. Overall, this study provides new insights into the mechanisms underlying sex-biased gene evolution during transitions to separate sexes.