Genetic and environmental variation in transcriptional expression of seminal fluid proteins

Seminal fluid proteins (SFPs) are crucial mediators of sexual selection and sexual conflict. Recent studies have chiefly focused on environmentally-induced plasticity as one source of variation in SFP expression, particularly in response to differing sperm competition levels. However, understanding the evolution of a trait in heterogenous environments requires estimates of both environmental and genetic sources of variation, as well as their interaction. Therefore, we investigated how environment (specifically mating group size, a good predictor of sperm competition intensity), genotypic and genotype-by-environment interactions affect seminal fluid expression. To do so, we reared 12 inbred lines of a simultaneously hermaphroditic flatworm Macrostomum lignano in groups of either two or eight worms and measured the expression levels of 58 putative SFP transcripts. We then examined the source of variation in the expression of each transcript individually and for multivariate axes extracted from a principal component analysis. We found that mating group size did not affect expression levels according to the single transcript analyses, nor did it affect the first principal component (presumably representing overall investment in seminal fluid production). However, mating group size did affect the relative expression of different transcripts captured by the second principal component (presumably reflecting variation in seminal fluid composition). Most transcripts were genetically variable in their expression level and several exhibited genotype-by-environment interactions; relative composition also showed high genetic variation. Collectively, our results reveal the tightly integrated nature of the seminal fluid transcriptome and provide new insights into the quantitative genetic basis of seminal fluid investment and composition.

精液蛋白（Seminal fluid proteins, SFPs）是介导性选择与性冲突的关键因子。过往研究多将环境诱导的表型可塑性视为精液蛋白表达变异的来源之一，尤其聚焦于其对不同精子竞争水平的响应。然而，要解析异质环境下性状的演化机制，需要同时估算变异的环境来源、遗传来源，以及二者的互作效应。因此，本研究探讨了环境因素（具体为交配群规模，其可有效预测精子竞争强度）、遗传型以及基因型-环境互作如何影响精液蛋白的表达。为此，我们将12个近交系的雌雄同体扁形动物平角涡虫（Macrostomum lignano）分别以每群2只或8只的密度饲养，并检测了58个推定精液蛋白转录本的表达水平。随后，我们分别针对每个转录本的表达变异来源，以及通过主成分分析提取的多元轴进行了分析。单转录本分析结果显示，交配群规模并未显著改变单个转录本的表达水平，对第一主成分（推测对应精液蛋白合成的整体投入量）亦无影响。但交配群规模确实对第二主成分所捕获的不同转录本的相对表达量存在影响，该主成分或反映了精液蛋白组成的变异。多数转录本的表达水平存在遗传变异，且有多个转录本表现出基因型-环境互作效应；相对组成同样呈现出较高的遗传变异。综合来看，本研究结果揭示了精液蛋白转录组的紧密整合特性，并为理解精液蛋白投入与组成的数量遗传基础提供了全新视角。