Multiple gene movements into and out of haploid sex chromosomes

BACKGROUND: Long-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. RESULTS: A 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. CONCLUSION: This 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 MATERIAL: The online version of this article (doi:10.1186/s13059-017-1201-7) contains supplementary material, which is available to authorized users.