Female-specific and dosage selections restore genes through transpositions onto the degenerated songbird W chromosomes

Abstract

Sex chromosomes are usually suppressed for homologous recombination, which leads to the loss of functional genes on the Y or W chromosomes. It remains unclear how species like birds with a ZW sex system cope with the consequential gene expression imbalance, usually in the absence of global dosage compensation mechanism. Here we tackle this conundrum by reporting 14 genes recently transposed from the Z to the W chromosomes of three songbird lineages, after analyzing a total of 12 songbird species genomes. These transpositions are estimated to have occurred within 9 million years. Besides the expected signatures of functional degeneration in some genes on the non-recombining W chromosomes, the other retained genes after transposition are enriched for haploinsufficient genes or housekeeping genes. Several genes show biased expression in ovaries of birds or lizard, or function in female germ cells. These results, together with the reported X-to-Y transpositions provide direct evidence that sex-specific and dosage selections may have recurrently driven the restoration of genes on the Y or W chromosomes, and suggest their evolutionary processes are more dynamic than simply becoming completely degenerated.