A requirement for the neuromodulators octopamine and tyramine in
            <i>Drosophila melanogaster</i>
            female sperm storage

Avila, Frank W.; Qazi, Margaret C. Bloch; Rubinstein, C. Dustin; Wolfner, Mariana F.

doi:10.1073/pnas.1117689109

Cited by 63 publications

(90 citation statements)

References 66 publications

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“…These neurons also produce the OA metabolic precursor, tyramine, which can also affect behaviors (16,(47)(48)(49). Although we have shown that ovulin acts through OA neuronal signaling, we cannot exclude the possibility that ovulin might act through tyramine signaling in OA neurons.…”

Section: Resultsmentioning

confidence: 83%

Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling

Rubinstein

Wolfner

2013

Proc. Natl. Acad. Sci. U.S.A.

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126

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Across animal taxa, seminal proteins are important regulators of female reproductive physiology and behavior. However, little is understood about the physiological or molecular mechanisms by which seminal proteins effect these changes. To investigate this topic, we studied the increase in Drosophila melanogaster ovulation behavior induced by mating. Ovulation requires octopamine (OA) signaling from the central nervous system to coordinate an egg's release from the ovary and its passage into the oviduct. The seminal protein ovulin increases ovulation rates after mating. We tested whether ovulin acts through OA to increase ovulation behavior. Increasing OA neuronal excitability compensated for a lack of ovulin received during mating. Moreover, we identified a mating-dependent relaxation of oviduct musculature, for which ovulin is a necessary and sufficient male contribution. We report further that oviduct muscle relaxation can be induced by activating OA neurons, requires normal metabolic production of OA, and reflects ovulin's increasing of OA neuronal signaling. Finally, we showed that as a result of ovulin exposure, there is subsequent growth of OA synaptic sites at the oviduct, demonstrating that seminal proteins can contribute to synaptic plasticity. Together, these results demonstrate that ovulin increases ovulation through OA neuronal signaling and, by extension, that seminal proteins can alter reproductive physiology by modulating known female pathways regulating reproduction. In Drosophila melanogaster, the suite of seminal proteins has been identified, as have many seminal protein-dependent postmating responses, including changes in egg production and laying, remating behavior, locomotion, feeding, and in ovulation rate (reviewed in refs. 2 and 3). For example, the Drosophila seminal protein ovulin elevates ovulation rate to maximal levels during the 24 h following mating (4, 5), and the seminal protein sex peptide (SP) suppresses female mating receptivity and increases egg-laying behavior for several days after mating (6-10). However, although a receptor for SP has been identified (11), along with elements of the neural circuit in which it is required (12-14), SP's mechanism of action has not yet been linked to regulatory networks known to control postmating behaviors. Thus, a crucial question remains: how do male-derived seminal proteins interact with regulatory networks in females to trigger postmating responses?We addressed this question by examining the stimulation of Drosophila ovulation by the seminal protein ovulin. In insects, ovulation, defined here as the release of an egg from the ovary to the uterus, is among the best understood reproductive processes in terms of its physiology and neurogenetics (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27). In D. melanogaster, ovulation requires input from neurons in the abdominal ganglia that release the catecholaminergic neuromodulators octopamine (OA) and tyramine (17,18,28). Drosophila ovulation also requires an OA receptor, OA receptor in mushro...

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Section: Resultsmentioning

confidence: 83%

Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling

Rubinstein

Wolfner

2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

126

155

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“…While these experiments do not shed light on the specific mechanism(s) in which the female nervous system affects sperm competition, they suggest that females are not passive players in sperm storage. This point is underscored by recent work showing that proper sperm storage requires the neuromodulators octopamine and tyramine within the female (Avila et al 2012). Also the male-derived accessory gland protein, Acp36DE interacts with unknown female factors to bias sperm competition.…”

Section: Discussionmentioning

confidence: 87%

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

2013

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Sperm competition arises as a result of complex interactions among male and female factors. While the roles of some male factors are known, little is known of the molecules or mechanisms that underlie the female contribution to sperm competition. The genetic tools available for Drosophila allow us to identify, in an unbiased manner, candidate female genes that are critical for mediating sperm competition outcomes. We first screened for differences in female sperm storage and use patterns by characterizing the natural variation in sperm competition in a set of 39 lines from the sequenced Drosophila Genetic Reference Panel (DGRP) of wild-derived inbred lines. We found extensive female variation in sperm competition outcomes. To generate a list of candidate female genes for functional studies, we performed a genome-wide association mapping, utilizing the common single-nucleotide polymorphisms (SNPs) segregating in the DGRP lines. Surprisingly, SNPs within ion channel genes and other genes with roles in the nervous system were among the top associated SNPs. Knockdown studies of three candidate genes (para, Rab2, and Rim) in sensory neurons innervating the female reproductive tract indicate that some of these candidate female genes may affect sperm competition by modulating the neural input of these sensory neurons to the female reproductive tract. More extensive functional studies are needed to elucidate the exact role of all these candidate female genes in sperm competition. Nevertheless, the female nervous system appears to have a previously unappreciated role in sperm competition. Our results indicate that the study of female control of sperm competition should not be limited to female reproductive tract-specific genes, but should focus also on diverse biological pathways. I N many organisms, sperm competition is an important source of reproductive variation and is critical to the reproductive success of both males and females. Sperm competition occurs when a female mates with and stores sperm from multiple males. Multiple mating creates a situation in which the males' sperm "compete" for successful fertilizations. While the ultimate outcome of a sperm competition depends on a complex interaction between male and female factors, the sexes often have different interests. Males are essentially in competition with other males, and while natural selection drives males to become better competitors with each other, it may result in males damaging the female through toxicity of seminal proteins (Wigby and Chapman 2004;Mueller et al. 2007). On the other hand, females benefit from simply being able to produce the most and highest-fitness offspring, and this may entail a specific response to male-produced molecules that influence sperm competition. The sexual conflict that arises from these different evolutionary goals of males and females implies that the genetic response to selection on sperm competition may be totally distinct in males and females. It remains largely unknown what genes drive this sexual antagon...

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“…These dsx + Tdc2 + neurons innervate the sperm storage organs, raising the possibility that they control SP availability in the female reproductive tract rather than SP signaling within the central nervous system. Octopamine is known to regulate sperm storage within females (Avila et al, 2012), and SP binds to and is gradually released from sperm (Peng et al, 2005). Hence, these dsx + Tdc2 + octopaminergic neurons could act genetically upstream of SP.…”

Section: Discussionmentioning

confidence: 99%

Ascending SAG Neurons Control Sexual Receptivity of Drosophila Females

Feng

Palfreyman

Häsemeyer

et al. 2014

Neuron

151

226

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Mating induces pronounced changes in female reproductive behavior, typically including a dramatic reduction in sexual receptivity. In Drosophila, postmating behavioral changes are triggered by sex peptide (SP), a male seminal fluid peptide that acts via a receptor (SPR) expressed in sensory neurons (SPSNs) of the female reproductive tract. Here, we identify second-order neurons that mediate the behavioral changes induced by SP. These SAG neurons receive synaptic input from SPSNs in the abdominal ganglion and project to the dorsal protocerebrum. Silencing SAG neurons renders virgin females unreceptive, whereas activating them increases the receptivity of females that have already mated. Physiological experiments demonstrate that SP downregulates the excitability of the SPSNs, and hence their input onto SAG neurons. These data thus provide a physiological correlate of mating status in the female central nervous system and a key entry point into the brain circuits that control sexual receptivity.

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

Cited by 63 publications

References 66 publications

Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling

Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

Ascending SAG Neurons Control Sexual Receptivity of Drosophila Females

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