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: In this paper, the authors provide an overview of the current knowledge on the inter-specific divergence of the SFP repertoire in Drosophila and compile the increasing amount of relevant genomic information from multiple species.
Abstract: While the striking effects of seminal fluid proteins (SFPs) on females are fairly conserved among Diptera, most SFPs lack detectable homologues among the SFP repertoires of phylogenetically distant species. How such a rapidly changing proteome conserves functions across taxa is a fascinating question. However, this and other pivotal aspects of SFPs' evolution remain elusive because discoveries on these proteins have been mainly restricted to the model Drosophila melanogaster. Here, we provide an overview of the current knowledge on the inter-specific divergence of the SFP repertoire in Drosophila and compile the increasing amount of relevant genomic information from multiple species. Capitalizing on the accumulated knowledge in D. melanogaster, we present novel sets of high-confidence SFP candidates and transcription factors presumptively involved in regulating the expression of SFPs. We also address open questions by performing comparative genomic analyses that failed to support the existence of many conserved SFPs shared by most dipterans and indicated that gene co-option is the most frequent mechanism accounting for the origin of Drosophila SFP-coding genes. We hope our update establishes a starting point to integrate further data and thus widen the understanding of the intricate evolution of these proteins.
5 citations
Dissertation•
14 Oct 2010
TL;DR: This paper aims to provide a chronology of the events leading up to and including the publication of this book and some of the key events that led to its publication.
Abstract: ........................................................................................................................... 2 Acknowledgements ......................................................................................................... 3
4 citations
TL;DR: In this article , the expression of 16 SFP encoding genes were manipulated using tissue-specific knockdown (KDs) to determine the effect of these genes' perturbation on three important post-mating phenotypes: female refractoriness to remating, defensive (P1), and offensive (P2) sperm competitive abilities in Drosophila melanogaster.
Abstract: The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role of SFPs in competition for fertilization phenotypes, like the ability to transfer and store sperm and the modulation of female receptivity and ovulation, the prevalence of selectively relaxed SFPs appears as a conundrum. One possible explanation is that selection on SFPs might be relaxed in terms of protein amino acid content, but adjustments of expression are essential for post-mating function. Interestingly, there is a general lack of systematic implementation of gene expression perturbation assays to monitor their effect on phenotypes related to sperm competition.We successfully manipulated the expression of 16 SFP encoding genes using tissue-specific knockdowns (KDs) and determined the effect of these genes' perturbation on three important post-mating phenotypes: female refractoriness to remating, defensive (P1), and offensive (P2) sperm competitive abilities in Drosophila melanogaster. Our analyses show that KDs of tested SFP genes do not affect female refractoriness to remating and P2, however, most gene KDs significantly decreased P1. Moreover, KDs of SFP genes that are selectively constrained in terms of protein-coding sequence evolution have lower P1 than KDs of genes evolving under relaxed selection.Our results suggest a more predominant role, than previously acknowledged, of variation in gene expression than coding sequence changes on sperm competitive ability in D. melanogaster.
4 citations
TL;DR: For example, this article found that the transcript levels of multiple seminal fluid proteins (SFPs) were significantly increased in the large sex comb (high) genetic lines in D. bipectinata.
3 citations
TL;DR: In this article, the authors used fluorescence lifetime imaging microscopy (FLIM) in combination with time-correlated single-photon counting (TCSPC) to quantify sperm metabolism based on the fluorescent properties of autofluorescent coenzymes.
Abstract: Sperm metabolism is fundamental to sperm motility and male fertility. Its measurement is still in its infancy, and recommendations do not exist as to whether or how to standardize laboratory procedures. Here, using the sperm of an insect, the common bedbug, Cimex lectularius, we demonstrate that standardization of sperm metabolism is required with respect to the artificial sperm storage medium and a natural medium, the seminal fluid. We used fluorescence lifetime imaging microscopy (FLIM) in combination with time-correlated single-photon counting (TCSPC) to quantify sperm metabolism based on the fluorescent properties of autofluorescent coenzymes, NAD(P)H and flavin adenine dinucleotide. Autofluorescence lifetimes (decay times) differ for the free and protein-bound state of the co-enzymes, and their relative contributions to the lifetime signal serve to characterize the metabolic state of cells. We found that artificial storage medium and seminal fluid separately, and additively, affected sperm metabolism. In a medium containing sugars and amino acids (Grace's Insect medium), sperm showed increased glycolysis compared with a commonly used storage medium, phosphate-buffered saline (PBS). Adding seminal fluid to the sperm additionally increased oxidative phosphorylation, likely reflecting increased energy production of sperm during activation. Our study provides a protocol to measure sperm metabolism independently from motility, stresses that protocol standardizations for sperm measurements should be implemented and, for the first time, demonstrates that seminal fluid alters sperm metabolism. Equivalent protocol standardizations should be imposed on metabolic investigations of human sperm samples.
2 citations
References
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TL;DR: This article extensively discusses two dimensionless (and thus standardised) classes of effect size statistics: d statistics (standardised mean difference) and r statistics (correlation coefficient), because these can be calculated from almost all study designs and also because their calculations are essential for meta‐analysis.
Abstract: Null hypothesis significance testing (NHST) is the dominant statistical approach in biology, although it has many, frequently unappreciated, problems. Most importantly, NHST does not provide us with two crucial pieces of information: (1) the magnitude of an effect of interest, and (2) the precision of the estimate of the magnitude of that effect. All biologists should be ultimately interested in biological importance, which may be assessed using the magnitude of an effect, but not its statistical significance. Therefore, we advocate presentation of measures of the magnitude of effects (i.e. effect size statistics) and their confidence intervals (CIs) in all biological journals. Combined use of an effect size and its CIs enables one to assess the relationships within data more effectively than the use of p values, regardless of statistical significance. In addition, routine presentation of effect sizes will encourage researchers to view their results in the context of previous research and facilitate the incorporation of results into future meta-analysis, which has been increasingly used as the standard method of quantitative review in biology. In this article, we extensively discuss two dimensionless (and thus standardised) classes of effect size statistics: d statistics (standardised mean difference) and r statistics (correlation coefficient), because these can be calculated from almost all study designs and also because their calculations are essential for meta-analysis. However, our focus on these standardised effect size statistics does not mean unstandardised effect size statistics (e.g. mean difference and regression coefficient) are less important. We provide potential solutions for four main technical problems researchers may encounter when calculating effect size and CIs: (1) when covariates exist, (2) when bias in estimating effect size is possible, (3) when data have non-normal error structure and/or variances, and (4) when data are non-independent. Although interpretations of effect sizes are often difficult, we provide some pointers to help researchers. This paper serves both as a beginner’s instruction manual and a stimulus for changing statistical practice for the better in the biological sciences.
3,041 citations
"Drosophila melanogaster seminal flu..." refers methods in this paper
...I also present 95% confidence intervals for effect size, measured by Cohen’s r , to illustrate the range of statistically supported effect sizes (Nakagawa & Cuthill 2007; Stephens et al. 2007)....
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TL;DR: It is demonstrated here that seminal fluid products from the main cells of the male accessory gland are responsible for the cost of mating in females, and that increasing exposure to these products increases female death rate.
Abstract: Female Drosophila melanogaster with environmentally or genetically elevated rates of mating die younger than controls. This cost of mating is not attributable to receipt of sperm. We demonstrate here that seminal fluid products from the main cells of the male accessory gland are responsible for the cost of mating in females, and that increasing exposure to these products increases female death rate. Main-cell products are also involved in elevating the rate of female egg-laying, in reducing female receptivity to further matings and in removing or destroying sperm of previous mates. The cost of mating to females may therefore represent a side-effect of evolutionary conflict between males.
1,292 citations
TL;DR: The fine balance between ROS production and scavenging, as well as the right timing and site for ROS production are of paramount importance for acquisition of fertilizing ability.
Abstract: Although high concentrations of reactive oxygen species (ROS) cause sperm pathology (ATP depletion leading to insufficient axonemal phosphorylation, lipid peroxidation and loss of motility and viability), recent evidence demonstrates that low and controlled concentrations of these ROS play an important role in sperm physiology. Reactive oxygen species, such as the superoxide anion, hydrogen peroxide and nitric oxide, induce sperm hyperactivation, capacitation or the acrosome reaction in vitro. The ROS involved in these processes may vary depending on experimental conditions, but all the evidence converges to describe these events as ‘oxidative’ or ‘redox regulated’. Human sperm capacitation and acrosome reaction are associated with extracellular production of a superoxide anion that is thought to originate from a membrane ‘oxidase’. The enzymes responsible for tyrosine phosphorylation‐dephosphorylation of sperm proteins are possible targets for ROS since mild oxidative conditions cause increases in protein tyrosine phosphorylation and acrosome reaction. The lipid peroxidation resulting from low concentrations of ROS promotes binding to the zona pellucida and may trigger the release of unesterified fatty acids from the sperm plasma membrane. The fine balance between ROS production and scavenging, as well as the right timing and site for ROS production are of paramount importance for acquisition of fertilizing ability.
620 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....
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TL;DR: To understand how postcopulatory sexual selection influences sperm traits, future research should determine sex-specific interactions that influence paternity, identify genetic correlations between ejaculate characters, quantify the relative costs of producing different sperm trait, and test assumptions of models of sperm quality evolution.
Abstract: The outcome of sperm competition is mediated largely by the relative numbers of sperm from competing males. However, substantial variation in features of sperm morphology and behaviour, such as length, longevity and motility, exists and researchers have suggested that this variation functions in postcopulatory sexual selection. Recent studies have determined the effect of these sperm-quality traits on fertilization success and a synthesis of this literature reveals that they are important in both sperm competition and cryptic female choice. To understand how postcopulatory sexual selection influences sperm traits, future research should determine sex-specific interactions that influence paternity, identify genetic correlations between ejaculate characters, quantify the relative costs of producing different sperm traits, and test assumptions of models of sperm quality evolution. Such research will shed light on what evolutionary pressures are responsible for the diversity in sperm morphometry and behaviour.
591 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...Males are expected to possess adaptations that increase the number of live, functional sperm that reach storage or the site of fertilization (e.g. Snook 2005; Reinhardt 2007; Holman & Snook 2008) to maximize their reproductive success, especially when females mate multiply and there is an overlap…...
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TL;DR: These studies provide excellent models to address basic questions in cell biology such as the control of genes in response to sex-specific, mating-regulated and cell type-specific cues and the function and targeting of peptide hormones.
555 citations
"Drosophila melanogaster seminal flu..." refers background in this paper
...…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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