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Roles of female and male genotype in post-mating responses in Drosophila melanogaster

ABSTRACT: Purpose: Mating induces a multitude of changes in female behavior, physiology and gene expression. Interactions between female and male genotype lead to variation in post-mating phenotypes and reproductive success. So far, few female molecules responsible for these interactions have been identified. Methods: We used Drosophila melanogaster from five geographically dispersed populations to investigate such female x male genotypic interactions at the female transcriptomic and phenotypic levels. Methods: Females from each line were singly-mated to males from the same five lines, for a total of 25 combinations. To assess whether female x male genotypic interactions affect the female post-mating transcriptome, next-generation RNA sequencing was performed on virgin and mated females at 5 to 6 hours post-mating. Results: Seventy-seven genes showed strong variation in mating-induced expression changes in a female x male genotype-dependent manner. These genes were enriched for immune response and odorant-binding functions, and for expression exclusively in the head. Conclusions: The transcriptional variation found in specific functional classes of genes might be a read-out of female x male compatibility at a molecular level. Understanding the roles these genes play in the female post-mating response will be crucial to better understand the evolution of post-mating responses and related conflicts between the sexes.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE104706 | GEO | 2017/10/10

SECONDARY ACCESSION(S): PRJNA413545

REPOSITORIES: GEO

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Project description:Male-derived accessory gland proteins (Acps) that are transferred to females during mating have profound effects on female reproductive physiology including increased ovulation, mating inhibition, and effects on sperm utilization and storage. The extreme rates of evolution seen in Acps may be driven by sperm competition and sexual conflict, processes which may ultimately drive complex interactions between female- and male-derived molecules and sperm. However, little is known of how gene expression in female reproductive tissues changes in response to the presence of male molecules and sperm. To characterize this response, we conducted parallel genomic and proteomic analyses of gene expression in the reproductive tract of 3-day-old unmated and mated female Drosophila melanogaster. Using DNA microarrays, we identified 539 transcripts that are differentially expressed in unmated vs. mated females and revealed a striking peak in differential expression at 6 hrs postmating and a marked shift from primarily down-regulated to primarily up-regulated transcripts within 3 hrs after mating. Combining two-dimensional gel electrophoresis and liquid chromatography mass spectrometry analyses, we identified 84 differentially expressed proteins at 3 hrs postmating, including proteins which appeared to undergo post-translational modification. Together, our observations define transcriptional and translational response to mating within the female reproductive tract and suggest a bimodal model of postmating gene expression initially correlated with mating and the final stages of female reproductive tract maturation and later with the declining presence of male reproductive molecules and with sperm maintenance and utilization. Experiment Overall Design: Three-day-old mated and unmated females were dissected to remove the lower reproductive tract (upper uterus, sperm-storage organs, and accessory glands). Mated females were dissected either immediately following mating (0 hr) or at 3, 6, or 24 hrs following the termination of mating. Tracts of 12-40 females of like category were pooled and total RNA extracted via a TRIzol-based protocol. Processing and labeling of transcript was performed by the Molecular Biology Core Facility at the Medical College of Georgia. Arrays from mated females at the different timepoints were compared to unmated females.

Project description:In internally fertilizing organisms, mating involves a series of highly coordinated molecular interactions between the sexes that occur within the female reproductive tract. In species with promiscuous mating systems, traits involved in postcopulatory interactions are expected to evolve rapidly, potentially leading to postmating-prezygotic (PMPZ) reproductive isolation between diverging populations. Here, we use a novel study design to investigate the postmating transcriptional response of Drosophila mojavensis female reproductive tracts following copulation with either conspecific or heterospecific (D. arizonae) males at three time points postmating. Relatively few genes (15 total) were transcriptionally regulated in the female lower reproductive tract in response to conspecific mating. Heterospecifically-mated females exhibited significant perturbations in the expression of the majority of these genes, and also downregulated transcription of a number of others, including several involved in mitochondrial function. These striking regulatory differences indicate failed postcopulatory molecular interactions between the sexes consistent with the strong PMPZ isolation observed for this cross. We also report, for the first time, the transfer of male mRNA transcripts to females during copulation. These included transcripts from male accessory-gland proteins (ACPs), a finding with potentially broad implications for understanding postcopulatory molecular interactions between the sexes. Dataset from Postmating transcriptional changes in reproductive tracts of con- and heterospecifically-mated Drosophila mojavensis females Bono, JM, Matzkin,LM, Kelleher, ES, and Markow, MA, Proceedings of the National Academy of Sciences, USA. The treatments were con- and heterospecific mated D. mojavensis females. Three different post-copulation times points were assayed, 15 minutes, 2 hours and 6 hours. For each time point there were two independent replicates. Additionally, two replicates of a virgin D. mojavensis female control were assayed. A total of 14 arrays. All RNA extractions were from the lower reproductive tract of females.

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Roles of female and male genotype in post-mating responses in Drosophila melanogaster

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