Temporal genomic evolution of bird sex chromosomes

Sex chromosomes exhibit many unusual patterns in sequence and gene expression relative to autosomes. Birds have evolved a female heterogametic sex system (male ZZ, female ZW), through stepwise suppression of recombination between chrZ and chrW. To address the broad patterns and complex driving forces of Z chromosome evolution, we analyze here 45 newly available bird genomes and four species' transcriptomes, over their course of recombination loss between the sex chromosomes.

We show Z chromosomes in general have a significantly higher substitution rate in introns and synonymous protein-coding sites than autosomes, driven by the male-to-female mutation bias ('male-driven evolution' effect). Our genome-wide estimate reveals that the degree of such a bias ranges from 1.6 to 3.8 among different species. G + C content of third codon positions exhibits the same trend of gradual changes with that of introns, between chrZ and autosomes or regions with increasing ages of becoming Z-linked, therefore codon usage bias in birds is probably driven by the mutational bias. On the other hand, Z chromosomes also evolve significantly faster at nonsynonymous sites relative to autosomes ('fast-Z' evolution). And species with a lower level of intronic heterozygosities tend to evolve even faster on the Z chromosome. Further analysis of fast-evolving genes' enriched functional categories and sex-biased expression patterns support that, fast-Z evolution in birds is mainly driven by genetic drift. Finally, we show in species except for chicken, gene expression becomes more male-biased within Z-linked regions that have became hemizygous in females for a longer time, suggesting a lack of global dosage compensation in birds, and the reported regional dosage compensation in chicken has only evolved very recently.

In conclusion, we uncover that the sequence and expression patterns of Z chromosome genes covary with their ages of becoming Z-linked. In contrast to the mammalian X chromosomes, such patterns are mainly driven by mutational bias and genetic drift in birds, due to the opposite sex-biased inheritance of Z vs. X.