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Journal Article•DOI•

Drosophila melanogaster seminal fluid can protect the sperm of other males

Luke Holman
01 Feb 2009-Functional Ecology (Blackwell Publishing Ltd)-Vol. 23, Iss: 1, pp 180-186
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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Journal Article•DOI•
Insect seminal fluid proteins: identification and function.

[...]

Frank W. Avila1, Laura K. Sirot1, Brooke A. LaFlamme1, C. Dustin Rubinstein1, Mariana F. Wolfner1 •
Cornell University1
01 Jan 2011-Annual Review of Entomology
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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Journal Article•DOI•
Resolving mechanisms of competitive fertilization success in Drosophila melanogaster.

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Mollie K. Manier1, John M. Belote1, Kirstin S. Berben1, David Novikov1, Will T. Stuart1, Scott Pitnick1 •
Syracuse University1
16 Apr 2010-Science
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

Journal Article•DOI•
Sperm wars and the evolution of male fertility

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Leigh W. Simmons1, John L. Fitzpatrick1•
University of Western Australia1
01 Nov 2012-Reproduction
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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Journal Article•DOI•
The seminal symphony: how to compose an ejaculate.

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Jennifer C. Perry1, Laura K. Sirot2, Stuart Wigby1•
University of Oxford1, College of Wooster2
01 Jul 2013-Trends in Ecology and Evolution
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

Journal Article•DOI•
Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster

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Laura K. Sirot1, Mariana F. Wolfner, Stuart Wigby•
Cornell University1
14 Jun 2011-Proceedings of the National Academy of Sciences of the United States of America
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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Journal Article•DOI•
Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila.

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Willie J. Swanson1, Andrew G. Clark, Heidi M. Waldrip-Dail, Mariana F. Wolfner, Charles F. Aquadro •
Cornell University1
19 Jun 2001-Proceedings of the National Academy of Sciences of the United States of America
TL;DR: Nineteen (∼11%) of 176 independent genes identified in the EST screen contain protein-coding regions with an excess of nonsynonymous over synonymous changes, suggesting that their divergence has been accelerated by positive Darwinian selection.
Abstract: Sequence comparisons of genomes or expressed sequence tags (ESTs) from related organisms provide insight into functional conservation and diversification. We compare the sequences of ESTs from the male accessory gland of Drosophila simulans to their orthologs in its close relative Drosophila melanogaster, and demonstrate rapid divergence of many of these reproductive genes. Nineteen (∼11%) of 176 independent genes identified in the EST screen contain protein-coding regions with an excess of nonsynonymous over synonymous changes, suggesting that their divergence has been accelerated by positive Darwinian selection. Genes that encode putative accessory gland-specific seminal fluid proteins had a significantly elevated level of nonsynonymous substitution relative to nonaccessory gland-specific genes. With the 57 new accessory gland genes reported here, we predict that ∼90% of the male accessory gland genes have been identified. The evolutionary EST approach applied here to identify putative targets of adaptive evolution is readily applicable to other tissues and organisms.

484 citations

"Drosophila melanogaster seminal flu..." refers background in this paper

  • ...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....

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Journal Article•DOI•
Sex Peptide Causes Mating Costs in Female Drosophila melanogaster

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Stuart Wigby1, Tracey Chapman1•
University College London1
22 Feb 2005-Current Biology
TL;DR: It is demonstrated here that a single Acp, the sex peptide (SP or Acp70A), which decreases female receptivity and stimulates egg production in the first matings of virgin females , is a major contributor to Acp-mediated mating costs in females.

452 citations

Additional excerpts

  • ...2002; Wigby & Chapman 2005)....

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Journal Article•DOI•
Seminal fluid‐mediated fitness traits in Drosophila

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Tracey Chapman1•
University College London1
10 Nov 2001-Heredity
TL;DR: Evidence is brought together for the function, evolution, diversification, and maintenance of variation in, seminal fluid-mediated traits in Drosophila by addressing the question of how and why the reproductive processes of females are influenced by males.
Abstract: The seminal fluid of male Drosophila contains a cocktail of proteins that have striking effects on male and female fitness. In D. melanogaster, seminal fluid proteins affect female receptivity, ovulation, oogenesis, sperm storage, sperm competition and mating plug formation. In addition, the seminal fluid contains antibacterial peptides and protease inhibitors. Some seminal fluid-encoding genes also show high rates of evolutionary change, exhibiting both significant between-species divergence and within-species polymorphism. Seminal fluid protein genes are expressed only in males, begging the question of how and why the reproductive processes of females are influenced by males. In this review I address these issues by bringing together evidence for the function, evolution, diversification, and maintenance of variation in, seminal fluid-mediated traits.

424 citations

"Drosophila melanogaster seminal flu..." refers background in this paper

  • ...The seminal fluid of Drosophila melanogaster contains a diverse array of molecules that serve a multitude of functions (e.g. Wolfner 1997; Chapman 2001; Chapman & Davies 2004; Ram & Wolfner 2007)....

    [...]

  • ...…sperm competition, spermicide, viability staining Functional Ecology (2008) xx , 000–000 Introduction The seminal fluid of Drosophila melanogaster contains a diverse array of molecules that serve a multitude of functions (e.g. Wolfner 1997; Chapman 2001; Chapman & Davies 2004; Ram & Wolfner 2007)....

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Journal Article•DOI•
Sperm Transfer, Storage, Displacement, and Utilization in Drosophila Melanogaster

[...]

G. Lefevre1, Ulla-Britt Jonsson1•
Harvard University1
01 Dec 1962-Genetics

354 citations

"Drosophila melanogaster seminal flu..." refers background 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)....

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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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  • ...…incapacitation (followed by disintegration, in those studies that observed sperm directly), physical displacement by the second males’ sperm (‘sperm displacement’; Lefevre & Jonsson 1962), sperm dumping (Snook & Hosken 2004), changes in the females’ rate of sperm use, or a combination of these....

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  • ...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)....

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  • ...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)....

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Journal Article•DOI•
Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction

[...]

K. Ravi Ram1, Mariana F. Wolfner1•
Cornell University1
01 Sep 2007-Integrative and Comparative Biology
TL;DR: Understanding how Acps elicit particular female responses will provide insights into reproductive biology and chemical communication, tools for analyzing models of sexual cooperation and/or sexual conflict, and information potentially useful for strategies for managing insect pests.
Abstract: Successful reproduction requires contributions from both the male and the female. In Drosophila, contributions from the male include accessory gland proteins (Acps) that are components of the seminal fluid. Upon their transfer to the female, Acps affect the female's physiology and behavior. Although primary sequences of Acp genes exhibit variation among species and genera, the conservation of protein biochemical classes in the seminal fluid suggests a conservation of functions. Bioinformatics coupled with molecular and genetic tools available for Drosophila melanogaster has expanded the functional analysis of Acps in recent years to the genomic/proteomic scale. Molecular interplay between Acps and the female enhances her egg production, reduces her receptivity to remating, alters her immune response and feeding behavior, facilitates storage and utilization of sperm in the female and affects her longevity. Here, we provide an overview of the D. melanogaster Acps and integrate the results from several studies that bring the current number of known D. melanogaster Acps to 112. We then discuss several examples of how the female's physiological processes and behaviors are mediated by interactions between Acps and the female. Understanding how Acps elicit particular female responses will provide insights into reproductive biology and chemical communication, tools for analyzing models of sexual cooperation and/or sexual conflict, and information potentially useful for strategies for managing insect pests.

337 citations

"Drosophila melanogaster seminal flu..." refers background or methods in this paper

  • ...Seminal fluid also influences a number of female traits important to male reproductive success, such as oviposition rate and remating behaviour (Ram & Wolfner 2007), and some Acps contribute to the cost of mating in females (Chapman et al ....

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  • ...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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  • ...When adding seminal fluid, both accessory glands, the ejaculatory duct and the ejaculatory bulb (all of which contribute to the seminal fluid; Ram & Wolfner 2007) were placed in the drop of saline with the sperm, punctured to the release the contents of the lumen and then lightly mixed with a pin....

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  • ...…sperm competition, spermicide, viability staining Functional Ecology (2008) xx , 000–000 Introduction The seminal fluid of Drosophila melanogaster contains a diverse array of molecules that serve a multitude of functions (e.g. Wolfner 1997; Chapman 2001; Chapman & Davies 2004; Ram & Wolfner 2007)....

    [...]

  • ...There are 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…...

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Trending Questions (2)
Does Preseed help keep sperm alive?

This study therefore provides strong evidence that seminal fluid does not kill rival sperm, and instead can actually protect them.

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The results suggest that seminal fluid improves sperm survival, even if the sperm are from a different male.

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