The life history of
            <i>Drosophila</i>
            sperm involves molecular continuity between male and female reproductive tracts

McCullough, Erin L.; Whittington, Emma; Singh, Akanksha; Pitnick, Scott; Wolfner, Mariana F.; Dorus, Steve

doi:10.1073/pnas.2119899119

Cited by 40 publications

(73 citation statements)

References 87 publications

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“…We considered those proteins as predicted to be transferred by the male during mating (figure 2). Of these 141 proteins, only one was an orthologue to a known D. melanogaster Sfps (FBgn0023529, with unknown function, and that is also a canonical D. melanogaster sperm protein [23]) and 48 were orthologues to known D. melanogaster sperm proteins (electronic supplementary material, tables S1 and S2) [23,24]. Since only supernatant samples were analysed, it is likely that most of the identified proteins were Sfps rather than sperm proteins, which would have pelleted out of the samples.…”

Section: Resultsmentioning

confidence: 99%

Characterization of reproductive proteins in the Mexican fruit fly points towards the evolution of novel functions

et al. 2022

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Seminal fluid proteins (Sfps) modify female phenotypes and have wide-ranging evolutionary implications on fitness in many insects. However, in the Mexican fruit fly, Anastrepha ludens , a highly destructive agricultural pest, the functions of Sfps are still largely unknown. To gain insights into female phenotypes regulated by Sfps, we used nano-liquid chromatography mass spectrometry to conduct a proteomic analysis of the soluble proteins from reproductive organs of A. ludens . The proteins predicted to be transferred from males to females during copulation were 100 proteins from the accessory glands, 69 from the testes and 20 from the ejaculatory bulb, resulting in 141 unique proteins after accounting for redundancies from multiple tissues. These 141 included orthologues to Drosophila melanogaster proteins involved mainly in oogenesis, spermatogenesis, immune response, lifespan and fecundity. In particular, we found one protein associated with female olfactory response to repellent stimuli (Scribble), and two related to memory formation (aPKC and Shibire). Together, these results raise the possibility that A. ludens Sfps could play a role in regulating female olfactory responses and memory formation and could be indicative of novel evolutionary functions in this important agricultural pest.

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Section: Resultsmentioning

confidence: 99%

Characterization of reproductive proteins in the Mexican fruit fly points towards the evolution of novel functions

et al. 2022

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“…2014), and may affect how it interacts with sperm and other ejaculate components. 2) A recent study demonstrates that during sperm storage, sperm progressively lose Sfps and gain female-derived proteins: whereas uniquely female-derived proteins only constitute 1.2% of the sperm proteome at 30 min after mating, this proportion increases to 19.1% by 4 days after mating (McCullough et al 2022). The relatively more male-like proteome of second-male sperm may allow the female to distinguish those from first-male sperm, or even offer them an advantage to reach the fertilization site or to fertilize the egg.…”

Section: Discussionmentioning

confidence: 99%

Octopaminergic/tyraminergicTdc2neurons regulate biased sperm usage in femaleDrosophila melanogaster

Chen

Clark

Wolfner

2022

Preprint

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In polyandrous internally fertilizing species, a multiply-mated female can use stored sperm from different males in a biased manner to fertilize her eggs. The female’s ability to assess sperm quality and compatibility is essential for her reproductive success, and represents an important aspect of postcopulatory sexual selection. In Drosophila melanogaster, previous studies demonstrated that the female nervous system plays an active role in influencing progeny paternity proportion, and suggested a role for octopaminergic/tyraminergic Tdc2 neurons in this process. Here, we report that inhibiting Tdc2 neuronal activity causes females to produce a higher-than-normal proportion of first-male progeny. This difference is not due to differences in sperm storage or release, but instead is attributable to the suppression of second-male sperm usage bias that normally occurs in control females. We further show that a subset of Tdc2 neurons innervating the female reproductive tract is largely responsible for the progeny proportion phenotype that is observed when Tdc2 neurons are inhibited globally. On the contrary, overactivation of Tdc2 neurons does not further affect sperm storage and release or progeny proportion. These results suggest that octopaminergic/tyraminergic signaling allows a multiply-mated female to bias sperm usage, and identify a new role for the female nervous system in postcopulatory sexual selection.

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“…Third, recent results [32] show that as sperm transit through and remain in the FRT, female-derived proteins become associated with them. It is possible that some of these female proteins facilitate the binding of particular SFPs to sperm, and that the kinetics of each SFP’s association reflects the association of particular female proteins with sperm.…”

Section: Discussionmentioning

confidence: 99%

“…It was unknown whether the female also contributes to the binding of SP to sperm, but several recent findings suggest the importance of testing this possibility. First, the molecular composition of sperm changes within the mated female, by the association of multiple female-derived proteins with sperm ([29–32]); such female proteins would be in a position to affect SP’s binding to sperm. Second, female molecules play roles in modification (cleavage) of some SFPs in D. melanogaster [33], and in the proteolytic dissolution of the mating plug in cabbage-white butterflies [34], again indicating that FRT proteins can have direct effects on SFPs and their molecular milieu.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Female factors are important for the seminal Sex Peptide’s association with sperm in mated D. melanogaster

Misra

Singh

Wolfner

2022

Preprint

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BackgroundMale-derived seminal fluid proteins (SFPs) enter and induce a myriad of physiological and behavioral changes in mated female flies optimizing fertility. Many post-mating changes in female Drosophila melanogaster persist for ∼10-14 days, because the seminal protein that induces them, 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” sperm to bind SP. 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 this reproductive process 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, and 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. Thus, female contributions are needed for maximal and appropriate binding of SP, and other SFPs, to sperm. Towards understanding the molecular roles of the female, we found no dramatic change in pH of the female reproductive tract after mating and that initial binding of SP to sperm is normal in females with ablated or defective spermathecal secretory cells and/or parovaria, but that higher levels of SP (and sperm) are retained in the latter females.ConclusionThis study reveals that the SP pathway is not entirely male-biased and that females also contribute to regulating it.

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The life history of Drosophila sperm involves molecular continuity between male and female reproductive tracts

Cited by 40 publications

References 87 publications

Characterization of reproductive proteins in the Mexican fruit fly points towards the evolution of novel functions

Characterization of reproductive proteins in the Mexican fruit fly points towards the evolution of novel functions

Octopaminergic/tyraminergicTdc2neurons regulate biased sperm usage in femaleDrosophila melanogaster

Female factors are important for the seminal Sex Peptide’s association with sperm in mated D. melanogaster

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