Genotype-by-environment interactions influence the composition of the Drosophila seminal proteome

Ejaculate proteins are key mediators of post-mating sexual selection and sexual conflict, as they can influence both male fertilization success and female reproductive physiology. However, the extent and sources of genetic variation and condition dependence of the ejaculate proteome are largely unknown. Such knowledge could reveal the targets and mechanisms of post-mating selection and inform about the relative costs and allocation of different ejaculate components, each with its own potential fitness consequences. Here, we used liquid chromatography coupled with tandem mass spectrometry to characterize the whole-ejaculate protein composition across twelve isogenic lines of Drosophila melanogaster that were reared on a high- or low-quality diet. We discovered new proteins in the transferred ejaculate and inferred their origin in the male reproductive system. We further found that the ejaculate composition was mainly determined by genotype identity and genotype-specific responses to larval diet, with no clear overall diet effect. Nutrient restriction increased proteolytic protein activity and shifted the balance between reproductive function and RNA metabolism. Our results open new avenues for exploring the intricate role of genotypes and their environment in shaping ejaculate composition, or for studying the functional dynamics and evolutionary potential of the ejaculate in its multivariate complexity.

射精蛋白（ejaculate proteins）是交配后性选择与性冲突的关键介导因子，其既能影响雄性受精成功率，也可调控雌性生殖生理过程。然而，目前学界对射精蛋白质组（ejaculate proteome）的遗传变异程度、变异来源及其条件依赖性仍知之甚少。掌握此类信息，可揭示交配后选择的作用靶点与调控机制，同时有助于阐明不同射精组分的相对成本与分配策略——每种组分均可能对个体适合度产生独特影响。本研究采用液相色谱-串联质谱联用技术，对饲养于高质量或低质量日粮中的12个黑腹果蝇（Drosophila melanogaster）同基因系的全射精蛋白组成进行了系统表征。我们在雄性转移的射精蛋白中发现了新型蛋白质，并推断了其在雄性生殖系统中的产生部位。进一步分析显示，射精组成主要由基因型特性以及基因型对幼虫日粮的特异性响应所决定，未观察到显著的整体日粮效应。营养限制可提升蛋白水解活性，并改变生殖功能与RNA代谢之间的动态平衡。本研究结果为探索基因型及其所处环境在塑造射精组成中的复杂作用，或是研究射精在多变量复杂性下的功能动态与演化潜力开辟了全新的研究方向。