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
More filters
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)....
[...]
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)....
[...]
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)....
[...]
References
More filters
TL;DR: It is shown, using labelled sperm in doubly mated females, that males can both physically displace andcapacitate stored sperm from earlier-mating males.
Abstract: Females in almost all animal groups copulate with multiple males1,2. This behaviour allows different males to compete for fertilization3 and gives females the opportunity to mediate this competition4. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring1,5,6. In Drosophila melanogaster, this second-male sperm precedence has long been studied7,8,9,10,11,12,13,14,15 but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace andincapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not ‘stratified’ in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.
176 citations
"Drosophila melanogaster seminal flu..." refers background or methods or result 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)....
[...]
...A second experiment by Price et al. (1999) mated females to two males: one that transferred sperm that have GFPlabelled tails, and one with normal sperm....
[...]
...This experiment demonstrates very clearly that first male sperm are lost from storage following remating, and that this translates into a loss of progeny (Price et al. 1999)....
[...]
...Finally, the experiment of Price et al. (1999) was repeated using three D. melanogaster strains, but the results were only replicated in one strain (P. D. Mack, B. A. Hammock & D. Promislow; in prep)....
[...]
...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)....
[...]
TL;DR: A bimodal model of postmating gene expression initially correlated with mating and the final stages of female reproductive tract maturation and later with the declining presence of male reproductive molecules and with sperm maintenance and utilization is suggested.
Abstract: Male-derived accessory gland proteins that are transferred to females during mating have profound effects on female reproductive physiology including increased ovulation, mating inhibition, and effects on sperm utilization and storage. The extreme rates of evolution seen in accessory gland proteins may be driven by sperm competition and sexual conflict, processes that may ultimately drive complex interactions between female- and male-derived molecules and sperm. However, little is known of how gene expression in female reproductive tissues changes in response to the presence of male molecules and sperm. To characterize this response, we conducted parallel genomic and proteomic analyses of gene expression in the reproductive tract of 3-day-old unmated and mated female Drosophila melanogaster. Using DNA microarrays, we identified 539 transcripts that are differentially expressed in unmated vs. mated females and revealed a striking peak in differential expression at 6 h postmating and a marked shift from primarily down-regulated to primarily up-regulated transcripts within 3 h after mating. Combining two-dimensional gel electrophoresis and liquid chromatography mass spectrometry analyses, we identified 84 differentially expressed proteins at 3 h postmating, including proteins that appeared to undergo posttranslational modification. Together, our observations define transcriptional and translational response to mating within the female reproductive tract and suggest a bimodal model of postmating gene expression initially correlated with mating and the final stages of female reproductive tract maturation and later with the declining presence of male reproductive molecules and with sperm maintenance and utilization.
176 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...Additionally, there was no control for the stimulus of mating itself, and mating also causes contractions (Adams & Wolfner 2007) and affects gene expression (Begun & Lawniczak 2004; McGraw et al. 2004; Mack et al. 2006)....
[...]
TL;DR: The male fruitfly, Drosophila melanogaster, transfers to his mate proteins that increase his reproductive success by causing changes in her behavior and physiology, and it is shown that among the transferred proteins are ones with antibacterial activity.
163 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...…at least 112 accessory gland proteins (Acps) in the seminal fluid (Ram & Wolfner 2007), which are involved in sperm storage (Neubaum & Wolfner 1999; Tram & Wolfner 1999), anti-bacterial activity (Lung & Wolfner 2001a), formation of the mating plug (Lung & Wolfner 2001b) and many other processes....
[...]
TL;DR: It is shown that by causing females to delay remating, first males suffer very little reduction in reproductive success due to female remating.
Abstract: As a consequence of copulation, males of Drosophila melanogaster induce a variety of physiological and behavioral effects in the female. Egg production and oviposition are stimulated by products of the male's accessory glands (Kummer, 1960; Garcia-Bellido, 1964; Merle, 1968; Bumet et al., 1973), and female attractiveness and receptivity are both reduced following copulation. Changes in female attractiveness are mediated pheromonally. A change in pheromonal profile from courtship-eliciting to courtship-discouraging pheromones is induced during the first 3 min of copulation (Tompkins et al., 1980; Tompkins and Hall, 1981; Venard and Jallon, 1980). The seminal fluid enzyme esterase-6 metabolizes the seminal fluid component cis-vaccenyl acetate to produce the antiaphrodisiac cis-vaccenyl alcohol (Mane et al., 1983). Behavioral effects of this metabolite on female attractiveness have been demonstrated and have been shown to be short-lived. There is a close correspondence between the time course of these behavioral effects and those first identified by Manning (1967) as the "copulation effect." Manning (1962, 1967) also identified a "sperm effect" on female receptivity which is longer lasting and causes females to remain unreceptive to male courtship. The strength of the sperm effect seems to be proportional to the number of sperm in storage (Gromko and Pyle, 1978; Gromko et al., 1984). The sperm effect is characterized behaviorally by the use of ovipositor extrusion to reject males, a behavior used only in very low frequency by virgin females (Connolly and Cook, 1973; Tompkins and Hall, 1981). The "sperm effect" -or the sperm dependence of the return of female receptivity-is not evident when mated females are confined with second males continuously for 24 h (Newport and Gromko, 1984). In this paper we investigate the details of the sperm dependence of female receptivity within the context of an experimental design which allows females periodic interactions with second males. We also quantify the impact of sperm-dependent female receptivity on the reproductive outcome of double matings. We show that by causing females to delay remating, first males suffer very little reduction in reproductive success due to female remating.
161 citations
"Drosophila melanogaster seminal flu..." refers result in this paper
...Consistent with this conclusion, three other published studies of D. melanogaster with the capacity to find evidence of sperm incapacitation did not find any (Lefevre & Jonsson 1962; Gromko et al. 1984; Snook & Hosken 2004)....
[...]
...Two studies remated females to males that transfer seminal fluid only but detected no decline in progeny production relative to singly-mated controls, suggesting that the seminal fluid did not harm the resident sperm (Lefevre & Jonsson 1962; Gromko et al. 1984)....
[...]
TL;DR: This comprehensive set of Acp genes allows us to dissect the patterns of evolutionary change in a suite of proteins from a single male-specific reproductive tissue and shows that there are separate classes undergoing distinctly dissimilar evolutionary dynamics.
Abstract: Drosophila melanogaster males transfer seminal fluid proteins along with sperm during mating. Among these proteins, ACPs ( Ac cessory gland p roteins) from the male9s accessory gland induce behavioral, physiological, and life span reduction in mated females and mediate sperm storage and utilization. A previous evolutionary EST screen in D. simulans identified partial cDNAs for 57 new candidate ACPs. Here we report the annotation and confirmation of the corresponding Acp genes in D. melanogaster . Of 57 new candidate Acp genes previously reported in D. melanogaster , 34 conform to our more stringent criteria for encoding putative male accessory gland extracellular proteins, thus bringing the total number of ACPs identified to 52 (34 plus 18 previously identified). This comprehensive set of Acp genes allows us to dissect the patterns of evolutionary change in a suite of proteins from a single male-specific reproductive tissue. We used sequence-based analysis to examine codon bias, gene duplications, and levels of divergence (via d N / d S values and ortholog detection) of the 52 D. melanogaster ACPs in D. simulans , D. yakuba , and D. pseudoobscura . We show that 58% of the 52 D. melanogaster Acp genes are detectable in D. pseudoobscura . Sequence comparisons of ACPs shared and not shared between D. melanogaster and D. pseudoobscura show that there are separate classes undergoing distinctly dissimilar evolutionary dynamics.
156 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...Seminal fluid also contains anti-oxidants in D. melanogaster (Mueller et al. 2005), Apis mellifera (Collins et al. 2004), mammals (de Lamirande et al. 1997) and birds (Breque et al. 2003), which could protect sperm from damage by reactive oxygen species....
[...]
...For example, seminal fluid could regulate proteolysis; multiple seminal anti-proteases have been identified in D. melanogaster (Swanson et al. 2001; Lung et al. 2002; Mueller et al. 2005; 184 L. Holman © 2008 The Author....
[...]