Abstract
Sex chromosomes are unique genomic regions with sex-specific or sex-biased inherent patterns and are expected to be more frequently subject to sex-specific selection. Substantial knowledge on the evolutionary patterns of sex-linked genes have been gained from the studies on the male heterogametic systems (XY male, XX female), but the understanding of the role of sex-specific selection in the evolution of female-heterogametic sex chromosomes (ZW female, ZZ male) is limited. Here we collect the W-linked genes of 27 birds, covering the three major avian clades: Neoaves (songbirds), Galloanserae (chicken), and Palaeognathae (ratites and tinamous). We find that the avian W chromosomes exhibit very conserved gene content despite their independent evolution of recombination suppression. The retained W-linked genes have higher dosage-sensitive and higher expression level than the lost genes, suggesting the role of purifying selection in their retention. Moreover, they are not enriched in ancestrally female-biased genes, and have not acquired new ovary-biased expression patterns after becoming W-linked. They are broadly expressed across female tissues, and the expression profile of the W-linked genes in females is not deviated from that of the homologous Z-linked genes. Together, our new analyses suggest that female-specific positive selection on the avian W chromosomes is limited, and the gene content of the W chromosomes is mainly shaped by purifying selection.
Highlights
Sex chromosomes evolve in a distinctive manner from the rest of the genome, of which one (Y or W) chromosome is sex-limited except for the pseudoautosomal regions (PAR), while the other homologous (X or Z) chromosome is biasedly inherited in one of the sexes
We focused on the genes that are homologous to the bird sex-linked genes, and because they are autosomal in green anole, their expression represents the ancestral expression in the bird proto-sex chromosomes
To investigate the extent of the W chromosome decay, first we demarcated the boundary of the pseudoautosomal regions (PARs) and the differentiation regions (DRs) according to the female coverage along the Z
Summary
Sex chromosomes evolve in a distinctive manner from the rest of the genome, of which one (Y or W) chromosome is sex-limited except for the pseudoautosomal regions (PAR), while the other homologous (X or Z) chromosome is biasedly inherited in one of the sexes. Once the sex-linked regions cease homologous recombination on the Y or W chromosome in the heterogametic sex, they are usually subject to functional degeneration [1]. The degeneration process can be caused by various evolutionary mechanisms including genetic hitchhiking [2], Muller’s ratchet [3], and background selection [4]. Due to the sex-limited or biased inheritance, sex chromosomes are hypothesized to be a preferred genomic location for the sexual antagonistic (SA) alleles to accumulate [9,10].
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