Code and data from Genetic constraints on microevolutionary divergence of sex-biased gene expression

The evolution of sex-specific phenotypes is an important dimension of diversification and local adaptation. The sex-dependent regulation of gene expression is considered a key genomic mechanism facilitating sex-dependent adaptation. In many species, genes with male-biased expression evolve faster in DNA sequence and expression level than genes with female-biased or sexually monomorphic expression. While positive selection may be responsible for rapid DNA sequence evolution, why expression of male-biased genes also evolves rapidly remains unclear. Beyond sex differences in selection, some aspects to the genetic architecture of gene expression could contribute to the rapid evolution of male-biased gene expression. First, male-biased genes might simply have greater standing genetic variance than female-biased genes. Second, male-biased genes could be less constrained by pleiotropy, either within or between sexes. Here, we evaluate these alternative explanations on an intraspecific scale using a series of quantitative genetic experiments conducted on natural variation in male and female gene expression in the fly Drosophila serrata. Male-biased genes had significantly higher genetic variance than female-biased genes and were generally more narrowly expressed across tissues, suggesting lower within individual pleiotropy. However, consistent with stronger constraints due to between-sex pleiotropy, their between-sex genetic correlations, rMF, were higher than female-biased genes and more strongly negatively associated with sex bias. Using an extensive clinal dataset, we tested whether sex differences in gene expression divergence among populations have been shaped by pleiotropy. Here, too male-biased gene divergence was more strongly associated with between-sex pleiotropy than female-biased gene divergence. Systematic differences in genetic variance and pleiotropy may be important factors influencing sex-specific adaptation arising through changes in gene expression. This article is part of the theme issue ‘Linking local adaptation with the evolution of sex differences’.

性别特异性表型的演化是物种分化与本地适应的重要维度。基因表达的性别依赖调控被认为是推动性别依赖型适应的关键基因组机制。在诸多物种中，雄性偏向表达基因的DNA序列与表达水平演化速率均快于雌性偏向表达或性别单态表达的基因。尽管正选择或许是DNA序列快速演化的诱因，但雄性偏向基因的表达何以同样演化迅速，目前仍不明晰。
除选择作用存在性别差异外，基因表达遗传架构的若干特征或许也会推动雄性偏向基因表达的快速演化。其一，雄性偏向基因可能本身较雌性偏向基因拥有更高的固有遗传方差；其二，无论在性别内部还是性别之间，雄性偏向基因所受的多效性约束均可能更弱。
本研究以种内尺度对上述两类替代性解释展开评估，基于对锯缘果蝇（Drosophila serrata）雌雄基因表达自然变异开展的一系列数量遗传实验。结果显示，雄性偏向基因的遗传方差显著高于雌性偏向基因，且其在组织中的表达范围普遍更窄，提示其个体内多效性更低。
然而，与性别间多效性带来的更强约束相符的是，雌雄间遗传相关系数（rMF）高于雌性偏向基因，且与性别偏向程度呈现更强的负相关关系。
本研究借助一套大规模渐变群数据集，检验了种群间基因表达分化的性别差异是否受到多效性的塑造。结果同样表明，相较于雌性偏向基因的表达分化，雄性偏向基因的表达分化与性别间多效性的关联更为显著。
遗传方差与多效性的系统性差异，或许是通过基因表达变化实现性别特异性适应的重要影响因素。本文属于“联结本地适应与性别差异演化”主题专刊的一部分。