Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

Avila, Frank W.; Ram, K. Ravi; Qazi, Margaret C. Bloch; Wolfner, Mariana F.

doi:10.1534/genetics.110.119735

Cited by 136 publications

(193 citation statements)

References 46 publications

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“…release of sperm from storage [28] Cell communication; epithelium morphogenesis; cell surface receptor linked signal transduction. Depletion of sperm from female storage sites is significantly slower in the absence of SP.…”

Section: Resultsmentioning

confidence: 99%

“…reduced female receptivity, increased egg laying, feeding and antimicrobial peptide production, and altered sleep patterns and water balance [20][21][22][23][24][25][26]. It also adheres to sperm and influences the rate of sperm release from storage [27,28]. The receptor for SP [29] is expressed in the female brain, nervous system and reproductive system, and responses to SP depend upon a circuit of neurons that express the sex determination genes doublesex [30] and fruitless [29].…”

Section: Introductionmentioning

confidence: 99%

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Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

et al. 2012

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Seminal fluid proteins (Sfps) alter female behaviour and physiology and can mediate sexual conflict. In Drosophila melanogaster, a single Sfp, the sex peptide (SP), triggers remarkable post-mating responses in females, including altered fecundity, feeding, immunity and sexual receptivity. These effects can favour the evolutionary interests of males while generating costs in females. We tested the hypothesis that SP is an upstream master-regulator able to induce diverse phenotypes through efficient induction of widespread transcriptional changes in females. We profiled mRNA responses to SP in adult female abdomen (Abd) and headþthorax (HT) tissues using microarrays at 3 and 6 h following mating. SP elicited a rich, subtle signature of temporally and spatially controlled mRNAs. There were significant alterations to genes linked to egg development, early embryogenesis, immunity, nutrient sensing, behaviour and, unexpectedly, phototransduction. There was substantially more variation in the direction of differential expression across time points in the HT versus Abd. The results support the idea that SP is an important regulator of gene expression in females. The expression of many genes in one sex can therefore be under the influence of a regulator expressed in the other. This could influence the extent of sexual conflict both within and between loci.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

et al. 2012

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“…First, Fricke et al (2009) presented evidence that SP might have a role in sperm competition. Second, SP function is required for proper release of stored sperm from female sperm storage organs (Avila et al 2010). Inappropriate release of sperm from storage organs can have a direct effect on sperm usage and P1 scores (Avila and Wolfner 2009;Ram and Wolfner 2009).…”

Section: Discussionmentioning

confidence: 99%

The Genetic Basis for Male × Female Interactions Underlying Variation in Reproductive Phenotypes of Drosophila

2010

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In Drosophila, where females mate multiply, sperm competition contributes strongly to fitness variability among males. Males transfer ''Acp'' seminal proteins to females during mating, and these proteins influence the outcome of sperm competition. Because Acps function within the female, male proteins can directly interact with female molecules in a manner that affects reproductive fitness. Here we begin to dissect the genetic architecture of male 3 female interactions underlying reproductive phenotypes important to sperm competition. By utilizing chromosome extraction lines, we demonstrate that the third and X chromosomes each have large effects on fertility phenotypes, female remating rate, and the sperm competition parameter, P1. Strikingly, the third and X chromosomes harbor genetic variation that gives rise to strong male 3 female interactions that modulate female remating rate and P1. Encoded on these chromosomes are, respectively, sex peptide (SP) and sex peptide receptor (SPR), the only pair of physically interacting male Acp and female receptor known. We identified several intriguing allelic interactions between SP and SPR. The results of this study begin to elucidate the complex genetic architecture of reproductive and sperm competition phenotypes and have significant implications for the evolution of male and female characters.

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“…Frozen females were stored at 280°for ,2 weeks before counting. Reproductive tracts were dissected and then stained with orcein (Neubaum and Wolfner 1999;Mueller et al 2008;Avila et al 2010). A transillumination microscope was used at 10003 magnification to visualize sperm.…”

Section: Sperm Countsmentioning

confidence: 99%

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

et al. 2014

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Members of the M13 class of metalloproteases have been implicated in diseases and in reproductive fitness. Nevertheless, their physiological role remains poorly understood. To obtain a tractable model with which to analyze this protein family's function, we characterized the gene family in Drosophila melanogaster and focused on reproductive phenotypes. The D. melanogaster genome contains 24 M13 class protease homologs, some of which are orthologs of human proteases, including neprilysin. Many are expressed in the reproductive tracts of either sex. Using RNAi we individually targeted the five Nep genes most closely related to vertebrate neprilysin, Nep1-5, to investigate their roles in reproduction. A reduction in Nep1, Nep2, or Nep4 expression in females reduced egg laying. Nep1 and Nep2 are required in the CNS and the spermathecae for wild-type fecundity. Females that are null for Nep2 also show defects as hosts of sperm competition as well as an increased rate of depletion for stored sperm. Furthermore, eggs laid by Nep2 mutant females are fertilized normally, but arrest early in embryonic development. In the male, only Nep1 was required to induce normal patterns of female egg laying. Reduction in the expression of Nep2-5 in the male did not cause any dramatic effects on reproductive fitness, which suggests that these genes are either nonessential for male fertility or perform redundant functions. Our results suggest that, consistent with the functions of neprilysins in mammals, these proteins are also required for reproduction in Drosophila, opening up this model system for further functional analysis of this protein class and their substrates. P ROTEASES play key roles in diverse physiological systems. One such family of metalloproteases, the M13 class of neutral endopeptidases, consists mainly of membranebound zinc proteases that are involved in the processing of neuropeptides and peptide hormones (reviewed in Turner et al. 2000;Turner et al. 2001;Bland et al. 2008). In mammals, seven members of this family have been identified, of which neprilysin (NEP) and endothelin converting enzyme (ECE) are the best studied. These proteins have been implicated in various diseases including cardiovascular disease (Segura and Ruilope 2011;Wick et al. 2011), Alzheimer's disease (Mulder et al. 2012;Klein et al. 2013), inflammation and inflammatory disorders (Wong et al. 2011), and cancer (Smollich et al. 2007;Maguer-Satta et al. 2011).In addition to their role in disease, NEPs are essential for development and reproduction in mammals. The mammalian Neprilysin-2, called NL1 in mice, is highly expressed in the testis. NL1-deficient males sire fewer pups, even though spermatogenesis appears to be unaffected (Carpentier et al. 2004). In females, NEP expression in the uterus is modulated by estrogen treatment in rats (Pinto et al. 1999) and during the estrogen/progesterone cycle in humans (Head et al. 1993). In female rats and mice, controlled degradation of tachykinins, particularly substance-P, by NEP in the uterus ...

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Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

Cited by 136 publications

References 46 publications

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

The Genetic Basis for Male × Female Interactions Underlying Variation in Reproductive Phenotypes of Drosophila

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

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