The evolution of sperm storage organs in Diptera: mating responsiveness, molecular diversity andgene regulation

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The majority of females with internal fertilisation have dedicated organs to store sperm. Thereby, females can disentangle mating activity from fertilisation and egg deposition which is important when both activities happen at different locations or are separated in time. Particularly insect females have evolved highly specialized sperm storage organs. In most insect species, females possess one or several spermathecae, but some Dipteran species have an additional sperm storage organ called a seminal receptacle. While on the surface both organs serve the same function, molecular work showed that they possess distinct expression profiles and thus have taken on different specializations. Further, while in the genus Drosophila most species use both kinds of organs, some species only use one or the other type to store sperm while the remaining type seems to have lost this function and it is unclear if it evolved new functions. While the morphological variation of these organs is well described, the details of reproductive processes leading to fertilization and particularly the molecules involved, their regulation and the possible variation across species are largely unknown. Intriguingly, the specific transcription factor doublesex (dsx), long known for its developmental function in sex differentiation, was found to be expressed in adult Drosophila melanogaster spermathecae. However, its specific role in adults, particularly its possible interplay with both transcriptional regulation of sperm storage organ function and with other gene regulatory mechanisms remains elusive. Here, we propose a collaborative project to study the evolution of sperm storage organs across Diptera to address these open questions. First, we aim to investigate the molecular characteristics of female sperm storage organs by studying the possible conservation of dsx expression in female storage organs, its mating responsiveness and possible function while assessing molecular diversity in reproductive tract secretomes across Drosophila species. We hypothesize that while dsx expression is conserved across the Diptera, the downstream reproductive molecules produced in the respective sperm storage organs are not. Second, we aim to understand the gene regulatory mechanisms underlying the evolution of female reproductive organs in Diptera. We hypothesize that species that use the ancestral spermathecae as main sperm storage organs do not express the same transcription factors or do not have the same accessible chromatin regions compared to species using solely or predominantly the subsequently evolved seminal receptacle after mating. We use a comparative genomics, transcriptomics and epigenomics approach in combination with DNA-protein binding assays and machine learning to establish a framework that can be used for functional and regulatory studies to better understand the complex evolution and interplay of gene regulatory networks before and after mating in Diptera.