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Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster.

ABSTRACT: The coordinated introduction of sperm and eggs is a prerequisite of high fertilization efficiency. In Drosophila melanogaster, as in most internally fertilizing animals, mated females store sperm prior to fertilization. Yet the regulation of sperm exit from these storage sites is poorly understood. To test one likely factor that could coordinate gamete availability, we quantified sperm exit from storage in three types of female: genetically matched females that were normal or eggless, and an additional wild-type control. Long-term depletion of sperm stores in normal females and eggless females occurs at similar rates. However, soon after mating, egg presence appears to accelerate the transition from one storage stage to the next. Since male ejaculate components and female factors contribute to sperm depletion, opportunities exist for both cooperation and conflict between the sexes in sperm storage dynamics.

SUBMITTER: Bloch Qazi MC

PROVIDER: S-EPMC1617180 | biostudies-literature | 2006 Mar

REPOSITORIES: biostudies-literature

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Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster.

Bloch Qazi Margaret C MC Wolfner Mariana F MF

Biology letters 20060301 1

The coordinated introduction of sperm and eggs is a prerequisite of high fertilization efficiency. In Drosophila melanogaster, as in most internally fertilizing animals, mated females store sperm prior to fertilization. Yet the regulation of sperm exit from these storage sites is poorly understood. To test one likely factor that could coordinate gamete availability, we quantified sperm exit from storage in three types of female: genetically matched females that were normal or eggless, and an add ...[more]

PMID: 17148345

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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.

Project description:BackgroundFemale sperm storage (FSS), the maintenance of sperm inside the female reproductive tract for an extended period of time, is pervasive among organisms with internal fertilization. Because FSS enables asynchronous mating and fertilization, it could be extremely important to reproduction. However, the physiological mechanisms underlying prolonged preservation and maintenance are poorly understood. Here, we used chicken, a typical oviparous animal, to determine the mechanisms ensuring sperm functionality in sperm storage tubules (SSTs).ResultsWe performed an insemination experiment on over two thousand hens at two periods, and found that the FSS capabilities varied widely among individuals. Except for the differences in the SST density between the two groups with distinct FSS abilities, we quantitatively profiled small-molecule metabolites derived from SST cells, and identified 28 metabolites with differential expression. In particular, high levels of lipids, fatty acids and lipid peroxidation product were observed in hens with low FSS capability. Pathway analysis showed that these differential metabolites were significantly enriched in the biosynthesis of unsaturated fatty acids. Moreover, we detected the total antioxidant capacity and lipid peroxidation level of SSTs, and found that chickens with a lower FSS ability had a significantly higher content of lipid peroxidation end-product, which was 2.4-fold greater than chickens with a higher FSS capability, and no significant difference was found in the total antioxidant capacity between these two groups.ConclusionsOur findings reveal that the long-term storage of sperm and the maintenance of their function in the female reproductive tract require an adequate microenvironment. The superabundance of fatty acids secreted by SST cells had detrimental effects on sperm storage in the female reproductive tract. Lipid peroxidation produces toxic biological substances that may cause irreversible damage to resident spermatozoa, resulting in short-term sperm retention and decreased fertility. Our findings provide new avenues for studying sperm storage and sustaining fertility.

Dataset Information

Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster.

Publications

Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster.

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