Complex evolutionary trajectories of sex chromosomes across bird taxa

Introduction Sex chromosomes originate from ordinary autosomes. Ancient sex-specific W or Y chromosomes, like that of female chicken or those of male mammals, usually have lost most functional genes, owing to a loss of recombination with their former homologs, the Z or X chromosomes. Such a recombination restriction occurred in a stepwise manner along most of the sex chromosomes in parallel in birds and mammals (creating so-called “evolutionary strata”), apart from small pseudoautosomal regions (PARs) that maintain recombination. Sex chromosomes of some basal birds like ostrich and emu have exceptionally large recombining PARs, but little is known about the genomic composition of most bird species’ sex chromosomes. Evolutionary strata of avian sex chromosomes. Bird sex chromosomes suppressed homologous recombination through shared or lineage-specific chromosomal inversions. Each defines an “evolutionary stratum” that exhibits a distinctive level of Z/W sequence divergence from neighboring strata. We demarcated and dated each stratum and show that bird sex chromosomes harbor great diversity regarding the lengths of recombining regions (green bars with crosses), or the degree of Z/W differentiation (scaled from gray to black). Rationale Here we use the newly available genomes of 17 species spanning the entire avian phylogeny to decipher the genomic architecture and evolutionary history of bird sex chromosomes. We demarcate the PAR and the nonrecombining differentiated region between Z/W of each species by their different read depths relative to autosomes. We further assemble numerous W-linked genomic regions, whose abundance and sequence divergence level with Z chromosome reflect their ages of recombination loss. Results We surprisingly find that more than half of the studied species have a W chromosome that is not completely degenerated. Besides ostrich and emu, some Neognathae species like tropicbird and killdeer also have long PARs. The nonrecombining regions between Z/W of many species exhibit a complex pattern of “evolutionary strata,” resulting from the suppression of recombination in a stepwise and independent manner among some lineages. We conclude that the first evolutionary stratum that contains the putative male-determining gene DMRT1 formed through a Z-linked chromosome inversion in an ancestor of all birds. This was followed by one stratum formed in the ancestor of Neognathae, one stratum in the ancestor of Neoaves, and independent emergence of more recent strata in most species. Many W-linked genes have disrupted protein function or reduced gene expression, and the rate of functional decay significantly slows down in older strata. Conclusion Our study uncovered an unexpected complexity of avian sex chromosomes, due to the lineage-specific recombination suppressions and different tempo of W degeneration. In contrast to mammals, some birds never experienced global recombination arrest, or differentiate at a very low rate between Z/W even after the recombination loss. This may relate to different intensities of sexual selection across bird species and explain their lack of a general chromosome-wide dosage compensation mechanism. Cite this article as Q. Zhou et al., Science 346, 1246338 (2014). DOI: 10.1126/science.1246338 Sex-specific chromosomes, like the W of most female birds and the Y of male mammals, usually have lost most genes owing to a lack of recombination. We analyze newly available genomes of 17 bird species representing the avian phylogenetic range, and find that more than half of them do not have as fully degenerated W chromosomes as that of chicken. We show that avian sex chromosomes harbor tremendous diversity among species in their composition of pseudoautosomal regions and degree of Z/W differentiation. Punctuated events of shared or lineage-specific recombination suppression have produced a gradient of “evolutionary strata” along the Z chromosome, which initiates from the putative avian sex-determining gene DMRT1 and ends at the pseudoautosomal region. W-linked genes are subject to ongoing functional decay after recombination was suppressed, and the tempo of degeneration slows down in older strata. Overall, we unveil a complex history of avian sex chromosome evolution.