How sex shapes transcriptome evolution in the songbird brain

Abstract Sex differences have long captivated scientists, yet the evolutionary rate of change in sex-biased gene expression has not been directly quantified. To address this issue, we introduce new options in CAGEE (Computational Analysis of Gene Expression Evolution), specifically unbounded Brownian motion and variable evolutionary rates among genes. We applied these features to brain transcriptomes of ten songbird species, half of which convergently evolved obligate cavity-nesting, an element of reproductive ecology linked to sex-specific changes in competitive behavior. We find that the degree of sex-bias – measured as male:female expression ratio for each gene – evolves twice as fast on the Z chromosome versus autosomes, but Z gene expression does not evolve at different rates among sexes. Most Z-linked genes are male-biased in their expression, but not all. These sex-balanced genes are not skewed in their rate of evolution, contrary to the hypothesis that some genes experience selection for balance and consequently evolve more slowly. Finally, the degree of sex-bias in gene expression evolves more quickly along obligate-cavity nesting lineages, suggesting that sex-specific selection may shape the evolution of brain sex differences, or lack thereof. Together, these results provide new insights into the interplay between sex and gene expression evolution.