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Genetic and environmental variation in transcriptional expression of seminal fluid proteins.

ABSTRACT: 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), genotype 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.

SUBMITTER: Patlar B

PROVIDER: S-EPMC6461930 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Seminal fluid contains some of the fastest evolving proteins currently known. These seminal fluid proteins (Sfps) play crucial roles in reproduction, such as supporting sperm function, and particularly in insects, modifying female physiology and behavior. Identification of Sfps in small animals is challenging, and often relies on samples taken from the female reproductive tract after mating. A key pitfall of this method is that it might miss Sfps that are of low abundance because of dilution in the female-derived sample or rapid processing in females. Here we present a new and complementary method, which provides added sensitivity to Sfp identification. We applied label-free quantitative proteomics to Drosophila melanogaster, male reproductive tissue - where Sfps are unprocessed, and highly abundant - and quantified Sfps before and immediately after mating, to infer those transferred during copulation. We also analyzed female reproductive tracts immediately before and after copulation to confirm the presence and abundance of known and candidate Sfps, where possible. Results were cross-referenced with transcriptomic and sequence databases to improve confidence in Sfp detection. Our data were consistent with 125 previously reported Sfps. We found nine high-confidence novel candidate Sfps, which were both depleted in mated versus, unmated males and identified within the reproductive tract of mated but not virgin females. We also identified 42 more candidates that are likely Sfps based on their abundance, known expression and predicted characteristics, and revealed that four proteins previously identified as Sfps are at best minor contributors to the ejaculate. The estimated copy numbers for our candidate Sfps were lower than for previously identified Sfps, supporting the idea that our technique provides a deeper analysis of the Sfp proteome than previous studies. Our results demonstrate a novel, high-sensitivity approach to the analysis of seminal fluid proteomes, whose application will further our understanding of reproductive biology.

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Genetic and environmental variation in transcriptional expression of seminal fluid proteins.

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