Mating Regulates Neuromodulator Ensembles at Nerve Termini Innervating the Drosophila Reproductive Tract

Heifetz, Yael; Lindner, Moshe; Garini, Yuval; Wolfner, Mariana F.

doi:10.1016/j.cub.2014.02.042

Cited by 72 publications

(90 citation statements)

References 37 publications

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“…In doubly -mated Drosophila females, the timing of MP ejection influences paternity-the later that MP ejection occurs, the more progeny are sired by a second mating male (Lüpold et al 2013). Female molecular contributions to MP formation and/or ejection may be found among secreted components of the female reproductive tract (Allen and Spradling 2008;Prokupek et al 2009;Schnakenberg et al 2011;Wong et al 2012;Sun and Spradling 2013), neuromodulators (Avila et al 2012;Heifetz et al 2014), and/or innervation (Middleton et al 2006;Rubinstein and Wolfner 2013) required for fertility. In particular, a recent study showed that the activity of the neuropeptide diuretic hormone 44 in a subset of doublesex-expressing neurons is required for MP ejection (Lee et al 2015).…”

Section: Discussionmentioning

confidence: 99%

Retention of Ejaculate by Drosophila melanogaster Females Requires the Male-Derived Mating Plug Protein PEBme

et al. 2015

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Within the mated reproductive tracts of females of many taxa, seminal fluid proteins (SFPs) coagulate into a structure known as the mating plug (MP). MPs have diverse roles, including preventing female remating, altering female receptivity postmating, and being necessary for mated females to successfully store sperm. The Drosophila melanogaster MP, which is maintained in the mated female for several hours postmating, is comprised of a posterior MP (PMP) that forms quickly after mating begins and an anterior MP (AMP) that forms later. The PMP is composed of seminal proteins from the ejaculatory bulb (EB) of the male reproductive tract. To examine the role of the PMP protein PEBme in D. melanogaster reproduction, we identified an EB GAL4 driver and used it to target PEBme for RNA interference (RNAi) knockdown. PEBme knockdown in males compromised PMP coagulation in their mates and resulted in a significant reduction in female fertility, adversely affecting postmating uterine conformation, sperm storage, mating refractoriness, egg laying, and progeny generation. These defects resulted from the inability of females to retain the ejaculate in their reproductive tracts after mating. The uncoagulated MP impaired uncoupling by the knockdown male, and when he ultimately uncoupled, the ejaculate was often pulled out of the female. Thus, PEBme and MP coagulation are required for optimal fertility in D. melanogaster. Given the importance of the PMP for fertility, we identified additional MP proteins by mass spectrometry and found fertility functions for two of them. Our results highlight the importance of the MP and the proteins that comprise it in reproduction and suggest that in Drosophila the PMP is required to retain the ejaculate within the female reproductive tract, ensuring the storage of sperm by mated females.KEYWORDS mating plug; sperm storage; PEBme; Drosophila reproduction I N numerous species comprising diverse taxa, a solidified structure forms inside the female reproductive tract during (or shortly after) mating that is referred to as the mating plug (MP; also called the copulatory plug; we will refer to these structures collectively as MPs). MPs are largely a coagulation of male seminal fluid components. In species that produce a MP, its role in reproduction varies. In some species, MP formation is thought to guard against sperm competition. For example, in primates, MPs are seen most often in species whose females mate multiply (Dixson and Anderson 2002). Primate MPs have been suggested to prevent remating (Dorus et al. 2004), thus acting as a form of passive mate guarding (Dunham and Rudolf 2009). In the mouse, perturbing (Murer et al. 2001) or preventing (Dean 2013) MP formation reduces male fertility; in the absence of MP formation, sperm migration to the sites of fertilization is impaired (Dean 2013) receptivity in the short term (Polak et al. 1998;Bretman et al. 2010). In bumblebees, MPs physically switch off receptivity Sauter et al. 2001) and have functions related to sperm competition (Duvo...

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Section: Discussionmentioning

confidence: 99%

Retention of Ejaculate by Drosophila melanogaster Females Requires the Male-Derived Mating Plug Protein PEBme

et al. 2015

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“…However, with the exception of recent work on hormonal changes in the female reproductive tract following copulation (Heifetz et al, 2014), we know almost nothing about how these female traits change dynamically in response to female state or male ejaculatory secretions. For example, are female reproductive adaptations modulated by age or temperature?…”

Section: Introductionmentioning

confidence: 99%

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly

Plakke

Deutsch

Meslin

et al. 2015

Journal of Experimental Biology

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Reproductive traits experience high levels of selection because of their direct ties to fitness, often resulting in rapid adaptive evolution. Much of the work in this area has focused on male reproductive traits. However, a more comprehensive understanding of female reproductive adaptations and their relationship to male characters is crucial to uncover the relative roles of sexual cooperation and conflict in driving co-evolutionary dynamics between the sexes. We focus on the physiology of a complex female reproductive adaptation in butterflies and moths: a stomach-like organ in the female reproductive tract called the bursa copulatrix that digests the male ejaculate (spermatophore). Little is known about how the bursa digests the spermatophore. We characterized bursa proteolytic capacity in relation to female state in the polyandrous butterfly Pieris rapae. We found that the virgin bursa exhibits extremely high levels of proteolytic activity. Furthermore, in virgin females, bursal proteolytic capacity increases with time since eclosion and ambient temperature, but is not sensitive to the pre-mating social environment. Post copulation, bursal proteolytic activity decreases rapidly before rebounding toward the end of a mating cycle, suggesting active female regulation of proteolysis and/or potential quenching of proteolysis by male ejaculate constituents. Using transcriptomic and proteomic approaches, we report identities for nine proteases actively transcribed by bursal tissue and/or expressed in the bursal lumen that may contribute to observed bursal proteolysis. We discuss how these dynamic physiological characteristics may function as female adaptations resulting from sexual conflict over female remating rate in this polyandrous butterfly.

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“…In female flies, modulation of a number of physiological and behavioural responses is induced by the male sex peptide and other seminal fluid components [43][44][45][46][47][48][49]. Neuromodulators mediate behavioural flexibility in response to internal physiological state [1,24] and Drosophila tachykinin or short neuropeptide F were shown to modulate presynaptic activities in olfactory sensory neurons affecting odour-guided behaviour [50,51].…”

Section: Discussionmentioning

confidence: 99%

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

et al. 2015

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Mating has profound effects on animal physiology and behaviour, not only in females but also in males, which we show here for olfactory responses. In cotton leafworm moths, Spodoptera littoralis, odour-mediated attraction to sex pheromone and plant volatiles are modulated after mating, producing a behavioural response that matches the physiological condition of the male insect. Unmated males are attracted by upwind flight to sex pheromone released by calling females, as well as to volatiles of lilac flowers and green leaves of the host plant cotton, signalling adult food and mating sites, respectively. Mating temporarily abolishes male attraction to females and host plant odour, but does not diminish attraction to flowers. This behavioural modulation is correlated with a response modulation in the olfactory system, as shown by electro-physiological recordings from antennae and by functional imaging of the antennal lobe, using natural odours and synthetic compounds. An effect of mating on the olfactory responses to pheromone and cotton plant volatiles but not to lilac flowers indicates the presence of functionally independent neural circuits within the olfactory system. Our results indicate that these circuits interconnect and weigh perception of social and habitat odour signals to generate appropriate behavioural responses according to mating state.

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Mating Regulates Neuromodulator Ensembles at Nerve Termini Innervating the Drosophila Reproductive Tract

Cited by 72 publications

References 37 publications

Retention of Ejaculate by Drosophila melanogaster Females Requires the Male-Derived Mating Plug Protein PEBme

Retention of Ejaculate by Drosophila melanogaster Females Requires the Male-Derived Mating Plug Protein PEBme

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

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