Miller-Crews Isaac, Lipshutz Sara E, Fulton Ben, Bertram Jason, Hahn Matthew W, Rosvall Kimberly A
Department of Biology, Indiana University, Bloomington, IN, USA.
Department of Biology, Duke University, Durham, NC, USA.
bioRxiv. 2025 Aug 21:2025.08.21.671601. doi: 10.1101/2025.08.21.671601.
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.
性别差异长期以来一直吸引着科学家，但性别偏向基因表达的进化变化速率尚未得到直接量化。为了解决这个问题，我们利用了雄性和雌性鸣禽的大脑基因表达数据。为此，我们在软件包CAGEE（基因表达进化的计算分析）中引入了无界布朗运动和基因间可变进化速率的新选项。我们将这些新功能应用于10种重点鸣禽物种，其中一半已经趋同进化出专性洞巢习性，这是一种与竞争中性别特异性变化相关的繁殖生态学元素。我们发现，性别偏向程度——以每个基因的雄性：雌性表达比例衡量——在Z染色体上的进化速度是常染色体的两倍，但除此之外，Z基因在雄性和雌性中的表达进化速率并无差异。大多数Z连锁基因在表达上偏向雄性，不过也有一些表现出大致相等的表达模式。这些性别平衡的基因在进化速率上没有偏差，这与某些基因经历平衡选择因而可能进化得更慢的假设相反。最后，基因表达中的性别偏向程度在专性洞巢谱系中进化得更快，这表明性别特异性生态选择的变化塑造了大脑性别差异的进化，或缺乏这种差异的情况。总之，这些工具和结果为性别与基因表达进化之间的相互作用提供了新的见解。
