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A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.

ABSTRACT: Female sperm storage is common among organisms with internal fertilization. It is important for extended fertility and, in cases of multiple mating, for sperm competition. The physiological mechanisms by which females store and manage stored sperm are poorly understood. Here, we report that the biogenic amines tyramine (TA) and octopamine (OA) in Drosophila melanogaster females play essential roles in sperm storage. D. melanogaster females store sperm in two types of organs, a single seminal receptacle and a pair of spermathecae. We examined sperm storage parameters in females mutant in enzymes required for the biochemical synthesis of tyrosine to TA and TA to OA, respectively. Postmating uterine conformational changes, which are associated with sperm entry and accumulation into storage, were unaffected by the absence of either TA or OA. However, sperm release from storage requires both TA and OA; sperm were retained in storage in both types of mutant females at significantly higher levels than in control flies. Absence of OA inhibited sperm depletion only from the seminal receptacle, whereas absence of both OA and TA perturbed sperm depletion from both storage organ types. We find innervation of the seminal receptacle and spermathecae by octopaminergic-tyraminergic neurons. These findings identify a distinct role for TA and OA in reproduction, regulating the release of sperm from storage, and suggest a mechanism by which Drosophila females actively regulate the release of stored sperm.

SUBMITTER: Avila FW

PROVIDER: S-EPMC3311333 | biostudies-literature | 2012 Mar

REPOSITORIES: biostudies-literature

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A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.

Avila Frank W FW Bloch Qazi Margaret C MC Rubinstein C Dustin CD Wolfner Mariana F MF

Proceedings of the National Academy of Sciences of the United States of America 20120305 12

Female sperm storage is common among organisms with internal fertilization. It is important for extended fertility and, in cases of multiple mating, for sperm competition. The physiological mechanisms by which females store and manage stored sperm are poorly understood. Here, we report that the biogenic amines tyramine (TA) and octopamine (OA) in Drosophila melanogaster females play essential roles in sperm storage. D. melanogaster females store sperm in two types of organs, a single seminal rec ...[more]

PMID: 22393023

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Project description:BackgroundMale-derived seminal fluid proteins (SFPs) that enter female fruitflies during mating induce a myriad of physiological and behavioral changes, optimizing fertility of the mating pair. Some post-mating changes in female Drosophila melanogaster persist for ~10-14 days. Their long-term persistence is because the seminal protein that induces these particular changes, the Sex Peptide (SP), is retained long term in females by binding to sperm, with gradual release of its active domain from sperm. Several other "long-term response SFPs" (LTR-SFPs) "prime" the binding of SP to sperm. Whether female factors play a role in this process is unknown, though it is important to study both sexes for a comprehensive physiological understanding of SFP/sperm interactions and for consideration in models of sexual conflict.ResultsWe report here that sperm in male ejaculates bind SP more weakly than sperm that have entered females. Moreover, we show that the amount of SP, and other SFPs, bound to sperm increases with time and transit of individual seminal proteins within the female reproductive tract (FRT). Thus, female contributions are needed for maximal and appropriate binding of SP, and other SFPs, to sperm. Towards understanding the source of female molecular contributions, we ablated spermathecal secretory cells (SSCs) and/or parovaria (female accessory glands), which contribute secretory proteins to the FRT. We found no dramatic change in the initial levels of SP bound to sperm stored in mated females with ablated or defective SSCs and/or parovaria, indicating that female molecules that facilitate the binding of SP to sperm are not uniquely derived from SSCs and parovaria. However, we observed higher levels of SP (and sperm) retention long term in females whose SSCs and parovaria had been ablated, indicating secretions from these female tissues are necessary for the gradual release of Sex Peptide's active region from stored sperm.ConclusionThis study reveals that the SP-sperm binding pathway is not entirely male-derived and that female contributions are needed to regulate the levels of SP associated with sperm stored in their storage sites.

Dataset Information

A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.

Publications

A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.

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