Drosophila melanogaster seminal fluid can protect the sperm of other males
TL;DR: It is suggested that residual seminal fluid inside females could benefit the sperm of subsequent mates, affecting the outcome of sperm competition and influencing the evolution of ejaculates and mating systems.
Abstract: Summary
1Many internally-fertilizing animals produce seminal fluid which is transferred along with sperm during mating. Seminal fluid typically contains a diverse range of chemicals that coordinate sperm storage, moderate sperm motility, provide advantages in sexual selection and influence female physiology.
2Seminal fluid is well-studied in Drosophila melanogaster, a species in which it has been suggested to ‘incapacitate’ the sperm of rival males (e.g. by killing them) and thereby provide an advantage in sperm competition. This hypothesis has been tested several times over many years, but different studies have yielded conflicting conclusions. Here, I use fluorescent staining to directly measure the effects of D. melanogaster seminal fluid on the survival of sperm from the same male or from a rival. The results suggest that seminal fluid improves sperm survival, even if the sperm are from a different male. This study therefore provides strong evidence that seminal fluid does not kill rival sperm, and instead can actually protect them. This study also tested whether chemicals in the female reproductive tract harm sperm as in another Drosophila species, but found no evidence of this.
3These findings suggest that residual seminal fluid inside females could benefit the sperm of subsequent mates, affecting the outcome of sperm competition and influencing the evolution of ejaculates and mating systems.
Citations
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TL;DR: Recent identification of insect SFPs is reviewed and the multiple roles these proteins play in the postmating processes of female insects are discussed.
Abstract: Seminal fluid proteins (SFPs) produced in reproductive tract tissues of male insects and transferred to females during mating induce numerous physiological and behavioral postmating changes in females. These changes include decreasing receptivity to remating; affecting sperm storage parameters; increasing egg production; and modulating sperm competition, feeding behaviors, and mating plug formation. In addition, SFPs also have antimicrobial functions and induce expression of antimicrobial peptides in at least some insects. Here, we review recent identification of insect SFPs and discuss the multiple roles these proteins play in the postmating processes of female insects.
726 citations
Cites background from "Drosophila melanogaster seminal flu..."
...melanogaster seminal fluid has a protective function, improving the survival of even rival sperm (66)....
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TL;DR: Sperm showed more mobility within the female storage organs than expected, with those from the most recent copulation displacing sperm from previous males; however, sperm viability remained consistent over long-term storage and each male's sperm was equally competitive in fertilizing the female's eggs.
Abstract: Our understanding of postcopulatory sexual selection has been constrained by an inability to discriminate competing sperm of different males, coupled with challenges of directly observing live sperm inside the female reproductive tract. Real-time and spatiotemporal analyses of sperm movement, storage, and use within female Drosophila melanogaster inseminated by two transgenic males with, respectively, green and red sperm heads allowed us to unambiguously discriminate among hypothesized mechanisms underlying sperm precedence, including physical displacement and incapacitation of "resident" sperm by second males, female ejection of sperm, and biased use of competing sperm for fertilization. We find that competitive male fertilization success derives from a multivariate process involving ejaculate-female and ejaculate-ejaculate interactions, as well as complex sperm behavior in vivo.
333 citations
TL;DR: It is argued that future research must consider sperm and seminal fluid components of the ejaculate as a functional unity, and that research at the genomic level will identify the genes that ultimately control male fertility.
Abstract: Females frequently mate with several males, whose sperm then compete to fertilize available ova. Sperm competition represents a potent selective force that is expected to shape male expenditure on the ejaculate. Here, we review empirical data that illustrate the evolutionary consequences of sperm competition. Sperm competition favors the evolution of increased testes size and sperm production. In some species, males appear capable of adjusting the number of sperm ejaculated, depending on the perceived levels of sperm competition. Selection is also expected to act on sperm form and function, although the evidence for this remains equivocal. Comparative studies suggest that sperm length and swimming speed may increase in response to selection from sperm competition. However, the mechanisms driving this pattern remain unclear. Evidence that sperm length influences sperm swimming speed is mixed and fertilization trials performed across a broad range of species demonstrate inconsistent relationships between sperm form and function. This ambiguity may in part reflect the important role that seminal fluid proteins (sfps) play in affecting sperm function. There is good evidence that sfps are subject to selection from sperm competition, and recent work is pointing to an ability of males to adjust their seminal fluid chemistry in response to sperm competition from rival males. We argue that future research must consider sperm and seminal fluid components of the ejaculate as a functional unity. Research at the genomic level will identify the genes that ultimately control male fertility.
288 citations
Cites background from "Drosophila melanogaster seminal flu..."
...…functionality is largely dependent on post-translational modifications to their protein compliment that are brought about by sfps. Sfps are known to influence the viability of sperm (den Boer et al. 2008, Holman 2009, Simmons & Beveridge 2011) and their motility (Lindholmer 1974, Poiani 2006)....
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TL;DR: Assessment of the increasing evidence that considering ejaculate composition as a whole (and potential trade-offs among ejaculate components) has important consequences for predictions about male reproductive investment and female responses to ejaculates details how social and environmental effects on ejaculates have potentially far-reaching fitness consequences for both sexes.
Abstract: Ejaculates are fundamental to fitness in sexually reproducing animals: males gain all their direct fitness via the ejaculate and females require ejaculates to reproduce. Both sperm and non-sperm components of the ejaculate (including parasperm, seminal proteins, water, and macromolecules) play vital roles in postcopulatory sexual selection and conflict, processes that can potentially drive rapid evolutionary change and reproductive isolation. Here, we assess the increasing evidence that considering ejaculate composition as a whole (and potential trade-offs among ejaculate components) has important consequences for predictions about male reproductive investment and female responses to ejaculates. We review current theory and empirical work, and detail how social and environmental effects on ejaculate composition have potentially far-reaching fitness consequences for both sexes.
253 citations
TL;DR: The hypothesis that males can adaptively tailor the composition of proteins in the ejaculate, allowing a male to take advantage of the fecundity-stimulating effects of the previous male's ovulin, yet maintaining investment in sex peptide is supported.
Abstract: Female promiscuity can generate postcopulatory competition among males, but it also provides the opportunity for exploitation of rival male ejaculates. For example, in many insect species, male seminal fluid proteins (Sfps) transferred in a female's first mating stimulate increased fecundity and decreased receptivity to remating. Subsequent mates of females could potentially take advantage of the effects of the first male's Sfps and strategically reduce investment in their own ejaculate. We compared postmating responses (fecundity and sexual receptivity) of Drosophila melanogaster females after their first (virgin) matings (V), to the responses of females remating (M) 24 h after their first mating. The results show that M matings fail to boost fecundity and, thus, males are unlikely to gain fitness from transferring Sfps whose sole function—in V matings—is fecundity-stimulation. However, males can protect their likelihood of paternity in M matings through the transfer of receptivity-inhibiting Sfps. The levels of a fecundity-stimulating Sfp (ovulin) were significantly lower in M females relative to V females, at the same time point shortly after the end of mating. In contrast, the levels of a key receptivity-inhibiting Sfp (sex peptide) were the same in M and V females. These results support the hypothesis that males can adaptively tailor the composition of proteins in the ejaculate, allowing a male to take advantage of the fecundity-stimulating effects of the previous male's ovulin, yet maintaining investment in sex peptide. Furthermore, our results demonstrate sophisticated protein-specific ejaculate manipulation.
153 citations
Cites background from "Drosophila melanogaster seminal flu..."
...melanogaster male is higher upon in vitro exposure to seminal fluid from another male than it is in the absence of exposure to seminal fluid (12)....
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References
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TL;DR: The findings indicate that the female reproductive tract is a multi-organ system whose regions are modulated separately by mating and mating components, which could create an environment conducive to increased reproductive capacity.
Abstract: Mating induces changes in female insects, including in egg production, ovulation and laying, sperm storage, and behavior. Several molecules and effects that induce these changes have been identified, but their proximate effects on females remain unexplored. We examined whether vesicle release occurs as a consequence of mating; we used transgenic Drosophila that allow monitoring of secretory granule release at nerve termini. Changes in release occur at specific times postmating in different regions of the female reproductive tract: soon after mating in the lower reproductive tract, and later in the upper reproductive tract. Some changes are triggered by receipt of sperm, others by male seminal proteins, and still others by the act of mating itself (or other unidentified effectors). Our findings indicate that the female reproductive tract is a multi-organ system whose regions are modulated separately by mating and mating components. This modulation could create an environment conducive to increased reproductive capacity.
95 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...…groups on sperm viability is due to the presence/absence of seminal fluid rather than whether or not the female mated (mating alters gene expression and stimulates secretions in the reproductive tract of female D. melanogaster ; Begun & Lawniczak 2004; Heifetz & Wolfner 2004; McGraw et al ....
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...As well as transforming female gene expression and physiology (e.g. Heifetz & Wolfner 2004; McGraw et al ....
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TL;DR: It is shown here that the processing of Acp26Aa involves sequential proteolytic cleavages, and the position of these Cleavages is mapped and could restrict its activity to the mated female.
95 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...This delay was likely to be enough time for the proteins to be completely processed and fully capable of their natural functions (for comparison, the pre-processed forms of Acp26Aa become undetectable 30 min after mating; Park & Wolfner 1995)....
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...…of this experiment is that the seminal fluid had been naturally transferred to a female; some seminal fluid proteins are known to be processed soon after insemination, for example, by proteolytic cleavage and glycosylation, which can affect their function (Park & Wolfner 1995; Heifetz et al ....
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TL;DR: It is shown that systemic ectopic expression of ovulin is sufficient to stimulate ovulation in unmated females and that ovulin's cleavage in mated females is not destructive and may liberate additional functional products with potential to modulate ovulation independently.
Abstract: Proteins and peptides in Drosophila melanogaster seminal fluid induce mated females to increase their rates of egg deposition. One seminal-fluid protein, ovulin (Acp26Aa), stimulates an early step in the egg-laying process, the release of oocytes by the ovary. Ovulin, upon transfer to females, is cleaved sequentially within the mated female's reproductive tract. Here, we show that systemic ectopic expression of ovulin is sufficient to stimulate ovulation in unmated females. By using this assay to assess the functionality of ovulin's cleavage products, we find that two of the four cleavage products of ovulin can stimulate ovulation independently. Thus, ovulin's cleavage in mated females is not destructive and instead may liberate additional functional products with potential to modulate ovulation independently.
94 citations
TL;DR: It is found that male mice deficient for the gene encoding the protease inhibitor protease nexin-1 (PN-1) show a marked impairment in fertility from the onset of sexual maturity and the level of extracellular proteolytic activity is a critical element in controlling male fertility.
Abstract: Understanding infertility and sterility requires knowledge of the molecular mechanisms underlying sexual reproduction. We have found that male mice deficient for the gene encoding the protease inhibitor protease nexin-1 (PN-1) show a marked impairment in fertility from the onset of sexual maturity. Absence of PN-1 results in altered semen protein composition, which leads to inadequate semen coagulation and deficient vaginal plug formation upon copulation. Progressive morphological changes of the seminal vesicles also are observed. Consistent with these findings, abnormal PN-1 expression was found in the semen of men displaying seminal dysfunction. The data demonstrate that the level of extracellular proteolytic activity is a critical element in controlling male fertility.
93 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...Journal compilation © 2008 British Ecological Society, Functional Ecology, 23, 180–186 Mueller et al. 2007; Ram & Wolfner 2007), and deficiency in seminal anti-proteases has been linked to infertility in humans (He et al. 1999) and mice (Murer et al. 2001)....
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TL;DR: It is concluded that accessory gland size is a critical determinant of sexual maturity and male mating frequency in this species and is more closely associated with the time taken to reach sexual maturity than is testis growth.
Abstract: Age at first reproduction is an extremely important life-history trait. Several factors such as nutritional state and age-specific fecundity have been shown to influence time to sexual maturity; however, little work has been done in insects. We addressed this in a stalk-eyed fly (Cyrtodiopsis dalmanni), by testing the hypothesis that time to sexual maturity is associated with the development of male internal reproductive structures. We found that sexual maturity was attained after an increased rate of growth in the accessory glands, several days after mature sperm bundles, and motile sperm were observed in the testes. Although testis development is essential, the results suggest that accessory gland growth is more closely associated with the time taken to reach sexual maturity than is testis growth. When we manipulated the growth of testes and accessory glands via a dietary manipulation, we found that delayed growth rates increased the time taken to reach sexual maturity. Among the delayed individuals, sexually mature males had larger accessory glands, but not testes, than did immature males. In adult males, mating frequency was significantly positively correlated with accessory gland size, but not with testis length or body size. We conclude that accessory gland size is a critical determinant of sexual maturity and male mating frequency in this species.
81 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...The authors speculated that this ‘buffering’ effect may contribute to phenomena such as last-male sperm precedence and could select for novel traits in males, such as prudent seminal fluid allocation (male reproductive potential can be constrained by finite seminal fluid reserves in insects; (Lefevre & Jonsson 1962; Baker et al. 2003; Rogers et al. 2005; Linklater et al. 2007)....
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...…as last-male sperm precedence and could select for novel traits in males, such as prudent seminal fluid allocation (male reproductive potential can be constrained by finite seminal fluid reserves in insects; (Lefevre & Jonsson 1962; Baker et al. 2003; Rogers et al. 2005; Linklater et al. 2007)....
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