How sex shapes transcriptome evolution in the songbird brain

Sex differences have captivated scientists for a long time, yet the evolutionary rate of change in sex-biased gene expression has not been directly quantified. To address this issue, we leverage brain gene expression data from male and female songbirds. To do this, we introduce new options for unbounded Brownian motion and variable evolutionary rates among genes in the software package CAGEE (Computational Analysis of Gene Expression Evolution). We applied these new features to 10 focal songbird species, half of which have convergently evolved obligate cavity-nesting, an element of reproductive ecology linked to sex-specific changes in competition. We find that the degree of sex bias - measured as the male:female ratio in expression for each gene - evolves twice as fast on the Z chromosome vs. autosomes, but otherwise, Z gene expression does not evolve at different rates in males vs. females. Most Z-linked genes are male-biased in their expression, though some exhibit roughly equal patterns of expression. These sex-balanced genes are not skewed in their rate of evolution, contrary to the hypothesis that some genes experience selection for balance and therefore may evolve more slowly. Finally, the degree of sex bias in gene expression evolves more quickly along obligate-cavity nesting lineages, suggesting that changes in sex-specific ecological selection shape the evolution of brain sex differences, or lack thereof. Together, these tools and results provide new insights on the interplay between sex and gene expression evolution.