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Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract.

ABSTRACT: Upon mating, regions of the female reproductive tract mature and alter their function [1-3], for example to facilitate storage of sperm or control the release of eggs [4-6]. The female's nervous system and neuromodulators play important roles in her responses to mating [7-13]. However, it is difficult to reconcile the reproductive tract's many changing but coordinated events with the small set of neuromodulators present [14-18]. We hypothesized that each part of the reproductive tract contains a characteristic combination of neuromodulators that confer unique identities on each region and that postmating changes in these combinations coordinate subsequent actions. We examined the presence, locations, and levels of neuromodulators and related molecules ("signaling molecules") in the reproductive tract of Drosophila melanogaster females before and after mating: the biogenic amine octopamine, which regulates ovulation rate in Drosophila and locusts [7, 14-20]; serotonin, which regulates muscle contraction in locust oviducts [21]; and the FMRF amide dromyosuppressin, which regulates contraction of Drosophila heart muscle [22] and may regulate muscle contractions in the reproductive tract, if it is expressed there. We find that separate aspects of mating (sperm, seminal proteins, and physical effects) independently modulate the release of signaling molecules. Each reproductive tract subregion displays a characteristic combination of signaling molecule release, resulting in a unique functional identity. These patterns, and thus functions, change reproducibly after mating. Thus, one event (mating) promotes new combinations of signaling molecules that endow different parts of the reproductive tract with unique temporal and spatial identities that facilitate many aspects of fertilization.

SUBMITTER: Heifetz Y

PROVIDER: S-EPMC4020355 | biostudies-other | 2014 Mar

REPOSITORIES: biostudies-other

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Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract.

Heifetz Yael Y Lindner Moshe M Garini Yuval Y Wolfner Mariana F MF

Current biology : CB 20140313 7

Upon mating, regions of the female reproductive tract mature and alter their function [1-3], for example to facilitate storage of sperm or control the release of eggs [4-6]. The female's nervous system and neuromodulators play important roles in her responses to mating [7-13]. However, it is difficult to reconcile the reproductive tract's many changing but coordinated events with the small set of neuromodulators present [14-18]. We hypothesized that each part of the reproductive tract contains a ...[more]

PMID: 24631240

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Project description:The Aedes aegypti mosquito is a significant public health threat, as it is the main vector of dengue and chikungunya viruses. Disease control efforts could be enhanced through reproductive manipulation of these vectors. Previous work has revealed a relationship between male seminal fluid proteins transferred to females during mating and female post-mating physiology and behavior. To better understand this interplay, we used short-read RNA sequencing to identify gene expression changes in the lower reproductive tract of females in response to mating. We characterized mRNA expression in virgin and mated females at 0, 6 and 24 hours post-mating (hpm) and identified 364 differentially abundant transcripts between mating status groups. Surprisingly, 60 transcripts were more abundant at 0 hpm compared to virgin females, suggesting transfer from males. Twenty of these encode known Ae. aegypti seminal fluid proteins. Transfer and detection of male accessory gland-derived mRNA in females at 0 hpm was confirmed by measurement of eGFP mRNA in females mated to eGFP-expressing males. In addition, 150 transcripts were up-regulated at 6 hpm and 24 hpm, while 130 transcripts were down-regulated at 6 hpm and 24 hpm. Gene Ontology (GO) enrichment analysis revealed that proteases, a protein class broadly known to play important roles in reproduction, were among the most enriched protein classes. RNAs associated with immune system and antimicrobial function were also up-regulated at 24 hpm. Collectively, our results suggest that copulation initiates broad transcriptome changes across the mosquito female reproductive tract, "priming" her for important subsequent processes of blood feeding, egg development and immune defense. Our transcriptome analysis provides a vital foundation for future studies of the consequences of mating on female biology and will aid studies seeking to identify specific gene families, molecules and pathways that support key reproductive processes in the female mosquito.

Dataset Information

Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract.

Publications

Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract.

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