Males and females often have marked phenotypic differences, and the expression of these dissimilarities invariably involves sex differences in gene expression. Sex-biased gene expression has been well characterized in animal species, where a high proportion of the genome may be differentially regulated in males and females during development. Male-biased genes tend to evolve more rapidly than female-biased genes, implying differences in the strength of the selective forces acting on the two sexes. Analyses of sex-biased gene expression have focused on organisms that exhibit separate sexes during the diploid phase of the life cycle (diploid sexual systems), but the genetic nature of the sexual system is expected to influence the evolutionary trajectories of sex-biased genes. We analyze here the patterns of sex-biased gene expression in Ectocarpus, a brown alga with haploid sex determination (dioicy) and a low level of phenotypic sexual dimorphism. In Ectocarpus, female-biased genes were found to be evolving as rapidly as male-biased genes. Moreover, genes expressed at fertility showed faster rates of evolution than genes expressed in immature gametophytes. Both male- and female-biased genes had a greater proportion of sites experiencing positive selection, suggesting that their accelerated evolution is at least partly driven by adaptive evolution. Gene duplication appears to have played a significant role in the generation of sex-biased genes in Ectocarpus, expanding previous models that propose this mechanism for the resolution of sexual antagonism in diploid systems. The patterns of sex-biased gene expression in Ectocarpus are consistent both with predicted characteristics of UV (haploid) sexual systems and with the distinctive aspects of this organism's reproductive biology.

BackgroundLong-term evolution of sex chromosomes is a dynamic process shaped by gene gain and gene loss. Sex chromosome gene traffic has been studied in XY and ZW systems but no detailed analyses have been carried out for haploid phase UV sex chromosomes. Here, we explore sex-specific sequences of seven brown algal species to understand the dynamics of the sex-determining region (SDR) gene content across 100 million years of evolution.ResultsA core set of sex-linked genes is conserved across all the species investigated, but we also identify modifications of both the U and the V SDRs that occurred in a lineage-specific fashion. These modifications involve gene loss, gene gain and relocation of genes from the SDR to autosomes. Evolutionary analyses suggest that the SDR genes are evolving rapidly and that this is due to relaxed purifying selection. Expression analysis indicates that genes that were acquired from the autosomes have been retained in the SDR because they confer a sex-specific role in reproduction. By examining retroposed genes in Saccharina japonica, we demonstrate that UV sex chromosomes have generated a disproportionate number of functional orphan retrogenes compared with autosomes. Movement of genes out of the UV sex chromosome could be a means to compensate for gene loss from the non-recombining region, as has been suggested for Y-derived retrogenes in XY sexual systems.ConclusionThis study provides the first analysis of gene traffic in a haploid UV system and identifies several features of general relevance to the evolution of sex chromosomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1201-7) contains supplementary material, which is available to authorized users.