Evolutionary dynamics of sex-biased gene expression in a young XY system: Insights from the brown alga genus Fucus

Abstract

ABSTRACTThe sex-dependent regulation of gene expression is considered to be an underlying cause of often extensive, sexually dimorphic traits between males and females. Although the nature and degree of sex-biased gene expression has been well-documented in several animal and plant systems, far less is known about the commonality, conservation, recruitment mechanisms and evolution of sex-biased genes in more distant eukaryotic groups. Brown algae are of particular interest for empirical studies on the evolution of sex-biased gene expression, as they have been evolving independently from animals and plants for over one billion years. Here we focus on two brown algal dioecious species, Fucus serratus and Fucus vesiculosus, where male heterogamety (XX/XY) has recently emerged. Using RNA-seq, we study sex-biased gene expression and discuss different evolutionary forces responsible for the evolution of sex-biased genes. We find that both species evolved masculinized transcriptomes, with sex-biased genes allocated mainly to male reproductive tissue, but virtually absent in vegetative tissues. Conserved male-biased genes were enriched in functions related to gamete production, along with sperm competition and include two flagellar proteins under positive selection. In contrast to female-biased genes, which show high turnover rates, male-biased genes reveal remarkable conservation of bias and expression levels between the two species. As observed in other XY systems, male-biased genes also display accelerated rates of coding sequence evolution compared to female-biased or unbiased genes. Our results imply that evolutionary forces affect male and female sex-biased genes differently on structural and regulatory levels. Similar to evolutionarily distant plant and animal lineages, sex-biased gene expression in Fucus evolved during the transition to dioecy to resolve intra-locus sexual conflict arising from anisogamy.