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.
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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 results suggest that costs associated with the production and maintenance of large accessory glands, although yet to be identified, are likely to be a major constraint on mating frequency in natural populations of C. dalmanni.
Abstract: Traditionally it was thought that fitness-related traits such as male mating frequency, with a history of strong directional selection, should have little additive genetic variance and thus respond asymmetrically to bidirectional artificial selection. However, recent findings and theory suggest that a balance between selection for increased male mating frequency and opposing selection pressures on physiologically linked traits will cause male mating frequency to have high additive genetic variation and hence respond symmetrically to selection. We tested these hypotheses in the stalk-eyed fly, Cyrtodiopsis dalmanni, in which males hold harems comprising many females and so have the opportunity to mate at extremely high frequencies. We subjected male stalk-eyed flies to artificial selection for increased ('high') and decreased ('low') mating frequency in the presence of ecologically realistic, high numbers of females. High line males mated significantly more often than control or low line males. The direct response to selection was approximately symmetric in the high and low lines, revealing high additive genetic variation for, and no significant genetic constraints on, increased male mating frequency in C. dalmanni. In order to investigate trade-offs that might constrain male mating frequency under natural conditions we examined correlated responses to artificial selection. We measured accessory gland length, testis length and eyespan after 7 and 14 generations of selection. High line males had significantly larger accessory glands than low line males. No consistent correlated responses to selection were found in testis length or eyespan. Our results suggest that costs associated with the production and maintenance of large accessory glands, although yet to be identified, are likely to be a major constraint on mating frequency in natural populations of C. dalmanni.
35 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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TL;DR: The present study showed that although the antigenic levels of PCI in two seminal plasma samples from patients with infertility were normal or slightly elevated, their inhibitory activities toward urokinase plasminogen activator (uPA) and tissue-type plAsminogen activateator (tPA) were absent.
Abstract: Protein C inhibitor (PCI) has been found in seminal plasma and is considered to protect intact surrounding cells and seminal plasma proteins from possible proteolytic damage. In the present study, we showed that although the antigenic levels of PCI in two seminal plasma samples from patients with infertility were normal or slightly elevated, their inhibitory activities toward urokinase plasminogen activator (uPA) and tissue-type plasminogen activator (tPA) were absent. In contrast, uPA and tPA proteolytic activities in these two samples were 20‐60-fold higher than that from normal volunteers. A time-course analysis of PCI‐uPA complex formation showed that >80% of the complex had been formed within 15 min in normal seminal plasma in the presence of heparin, compared with the total complex formed after 150 min incubation, whereas no response to heparin stimulation was observed in the assays with the two patient samples. Similarly, >90% of PCI‐tPA complex was formed after 30 min of heparin stimulation in normal seminal plasma but no response was observed in the two patient samples. Kinetic assays of PCI inhibitory function in the presence of activated protein C (APC) showed that PCI inhibitory activity in the two patient samples was absent and not stimulated by heparin. Western blotting also showed that most of the intact PCI molecules, in normal samples, formed complexes with either uPA or tPA but there was no complex formed in one of the two patient samples and very little complex was observed in the other, suggesting that PCI in the two patient samples is inactive. These results suggest that the presence of functionally inactive PCI in seminal plasma may be associated with infertility.
31 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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...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....
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TL;DR: The assumption that the four products of meiosis in the male Drosophila are equally functional has been made untenable by recent studies of abnormal progeny ratios, and gametic lethality has been implicated as a possible cause of anomalies.
Abstract: The assumption that the four products of meiosis in the male Drosophila are equally functional has been made untenable by recent studies of abnormal progeny ratios. The potential causes of anomalous ratios can be classified in three categories: (1) postfertilization selection; (2) aberrant meiotic segregations; and (3) gametic lethality or selection. Unusual ratios resulting from zygotic lethality are well known, and it is relatively easy to fix this as the cause of an abnormal ratio by comparing the number of eggs laid to the number of adults recovered. There are also deviations from expected ratios which have been attributed to phenomena occurring during meiosis which render some of the products of meiosis non-functional (Novitski and Sandler, 1957; Sandler, Hiraizumi, and Sandler, 1959). Gametic lethality has also been implicated as a possible cause of anomalous ratios (C. W. Metz, 1929; Gershenson, 1928; Novitski, 1947). However, in these studies where gametic lethality is suggested as a possible cause of abnormal progeny ratios, this has been as a result of eliminating other possibilities and no mechanism has been described to account for the phenomenon. In fact, it has been generally held that the DNA of the spermatozoon is wholly inert and that the functional ability of the spermatozoon is independent of its gene content (Muller and Settles, 1927). Recent studies of sperm DNA suggest, however, that there may be changes in the
25 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...2005; Adams & Wolfner, 2007), seminal fluid has been suggested to interfere with the ejaculates of other, ‘rival’, males that previously mated with the same female (e.g. Lefevre & Jonsson 1962; DeVries 1964; Harshman & Prout 1994; Price et al. 1999)....
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TL;DR: Frequency distributions of progeny production for control, remating and nonremating wildtype females indicated that lowered first male productivity was not due to either preferential remating by females that initially stored few first male sperm or excessive depletion of firstmale sperm before remating.
22 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...1999) and/or first male progeny production (Lefevre & Jonsson 1962; Scott & Williams 1993; Price et al ....
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21 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...Seminal fluid is thought to improve sperm survival after insemination by suppressing female immunity in humans and other mammals (Alexander & Anderson 1987; Aumuller & Riva 1992; Robertson 2007), which might also occur in insects (which possess innate immunity only)....
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