Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds

Abstract

AbstractSongbirds have a species number almost equivalent to that of mammals, and are classic models for studying mechanisms of speciation and sexual selection. Sex chromosomes are hotspots of both processes, yet their evolutionary history in songbirds remains unclear. To elucidate that, we characterize female genomes of 11 songbird species having ZW sex chromosomes, with 5 genomes of bird-of-paradise species newly produced in this work. We conclude that songbird sex chromosomes have undergone at least four steps of recombination suppression before their species radiation, producing a gradient pattern of pairwise sequence divergence termed ‘evolutionary strata’. Interestingly, the latest stratum probably emerged due to a songbird-specific burst of retrotransposon CR1-E1 elements at its boundary, or chromosome inversion on the W chromosome. The formation of evolutionary strata has reshaped the genomic architecture of both sex chromosomes. We find stepwise variations of Z-linked inversions, repeat and GC contents, as well as W-linked gene loss rate that are associated with the age of strata. Over 30 W-linked genes have been preserved for their essential functions, indicated by their higher and broader expression of orthologs in lizard than those of other sex-linked genes. We also find a different degree of accelerated evolution of Z-linked genes vs. autosomal genes among different species, potentially reflecting their diversified intensity of sexual selection. Our results uncover the dynamic evolutionary history of songbird sex chromosomes, and provide novel insights into the mechanisms of recombination suppression.