scholarly journals Divergent allocation of sperm and the seminal proteome along a competition gradient in Drosophila melanogaster

2019 ◽  
Vol 116 (36) ◽  
pp. 17925-17933 ◽  
Author(s):  
Ben R. Hopkins ◽  
Irem Sepil ◽  
Marie-Laëtitia Thézénas ◽  
James F. Craig ◽  
Thomas Miller ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Sperm Competition ◽  
Seminal Fluid ◽  
Sperm Transfer ◽  
Male Mating ◽  
Compositional Change ◽  
Seminal Fluid Proteins ◽  
Allocation Rules ◽  
Offspring Production ◽  
Component Allocation

Sperm competition favors large, costly ejaculates, and theory predicts the evolution of allocation strategies that enable males to plastically tailor ejaculate expenditure to sperm competition threat. While greater sperm transfer in response to a perceived increase in the risk of sperm competition is well-supported, we have a poor understanding of whether males (i) respond to changes in perceived intensity of sperm competition, (ii) use the same allocation rules for sperm and seminal fluid, and (iii) experience changes in current and future reproductive performance as a result of ejaculate compositional changes. Combining quantitative proteomics with fluorescent sperm labeling, we show that Drosophila melanogaster males exercise independent control over the transfer of sperm and seminal fluid proteins (SFPs) under different levels of male–male competition. While sperm transfer peaks at low competition, consistent with some theoretical predictions based on sperm competition intensity, the abundance of transferred SFPs generally increases at high competition levels. However, we find that clusters of SFPs vary in the directionality and sensitivity of their response to competition, promoting compositional change in seminal fluid. By tracking the degree of decline in male mating probability and offspring production across successive matings, we provide evidence that ejaculate compositional change represents an adaptive response to current sperm competition, but one that comes at a cost to future mating performance. Our work reveals a previously unknown divergence in ejaculate component allocation rules, exposes downstream costs of elevated ejaculate investment, and ultimately suggests a central role for ejaculate compositional plasticity in sexual selection.

scholarly journals Genetic coordination of sperm morphology and seminal fluid proteins promotes male reproductive success in Drosophila melanogaster

2021 ◽  
Author(s):  
Jake Galvin ◽  
Erica Larson ◽  
Sevan Yedigarian ◽  
Mohammad Rahman ◽  
Kirill Borziak ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Reproductive Success ◽  
Sperm Competition ◽  
Seminal Fluid ◽  
Fertilization Success ◽  
Male Reproductive Success ◽  
Sperm Length ◽  
Seminal Fluid Proteins ◽  
Female Remating ◽  
Paternity Success

Spermatozoal morphology is highly variable both among and within species and in ways that can significantly impact fertilization success. In Drosophila melanogaster, paternity success depends on sperm length of both competing males and length of the female's primary sperm storage organ. We found that genes upregulated in long sperm testes are enriched for lncRNAs and seminal fluid proteins (Sfps). Transferred in seminal fluid to the female during mating, Sfps are secreted by the male accessory glands (AG) and affect female remating rate, physiology, and behavior with concomitant advantages for male reproductive success. Despite being upregulated in long sperm testes, they have no known function in testis tissue. We found that Sex Peptide and ovulin (Acp26Aa) knockouts resulted in shorter sperm, suggesting that Sfps may regulate sperm length during spermatogenesis. However, knockout of AG function did not affect sperm length, suggesting that AG expression has no influence on spermatogenic processes. We also found that long sperm males are better able to delay female remating, suggesting higher Sfp expression in AG. These results might suggest that long sperm males have a double advantage in sperm competition by both delaying female remating, likely through transfer of more Sfps, and by resisting sperm displacement. However, we also found that this extra advantage does not necessarily translate to more progeny or higher paternity success. Thus, we found that multiple components of the ejaculate coordinate to promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain.

scholarly journals Conceptual developments in sperm competition: a very brief synopsis

2020 ◽  
Vol 375 (1813) ◽  
pp. 20200061 ◽  
Author(s):  
Geoff A. Parker
Keyword(s):  
Sexual Selection ◽  
Sperm Competition ◽  
Seminal Fluid ◽  
Female Reproduction ◽  
Internal Fertilization ◽  
Seminal Fluid Proteins ◽  
Competition Theory ◽  
Past Half Century ◽  
Mate Acquisition ◽  
Gamete Competition

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. This article is part of the theme issue ‘Fifty years of sperm competition'.

scholarly journals Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

2012 ◽  
Vol 279 (1746) ◽  
pp. 4423-4432 ◽  
Author(s):  
A. Gioti ◽  
S. Wigby ◽  
B. Wertheim ◽  
E. Schuster ◽  
P. Martinez ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Sexual Conflict ◽  
Seminal Fluid ◽  
Nutrient Sensing ◽  
Seminal Fluid Proteins ◽  
Sex Peptide ◽  
Efficient Induction ◽  
Transcriptional Changes ◽  
Female Behaviour ◽  
Reproductive Processes

Seminal fluid proteins (Sfps) alter female behaviour and physiology and can mediate sexual conflict. In Drosophila melanogaster , a single Sfp, the sex peptide (SP), triggers remarkable post-mating responses in females, including altered fecundity, feeding, immunity and sexual receptivity. These effects can favour the evolutionary interests of males while generating costs in females. We tested the hypothesis that SP is an upstream master-regulator able to induce diverse phenotypes through efficient induction of widespread transcriptional changes in females. We profiled mRNA responses to SP in adult female abdomen (Abd) and head+thorax (HT) tissues using microarrays at 3 and 6 h following mating. SP elicited a rich, subtle signature of temporally and spatially controlled mRNAs. There were significant alterations to genes linked to egg development, early embryogenesis, immunity, nutrient sensing, behaviour and, unexpectedly, phototransduction. There was substantially more variation in the direction of differential expression across time points in the HT versus Abd. The results support the idea that SP is an important regulator of gene expression in females. The expression of many genes in one sex can therefore be under the influence of a regulator expressed in the other. This could influence the extent of sexual conflict both within and between loci.

scholarly journals Interactions between the microbiome and mating influence the female’s transcriptional profile in Drosophila melanogaster

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Sofie Y. N. Delbare ◽  
Yasir H. Ahmed-Braimah ◽  
Mariana F. Wolfner ◽  
Andrew G. Clark
Keyword(s):  
Drosophila Melanogaster ◽  
Egg Production ◽  
Seminal Fluid ◽  
Transcript Abundance ◽  
Vital Role ◽  
Transcriptional Profile ◽  
Seminal Fluid Proteins ◽  
Two Factors ◽  
Immunity Genes ◽  
Neuronal Functions

Abstract Drosophila melanogaster females undergo a variety of post-mating changes that influence their activity, feeding behavior, metabolism, egg production and gene expression. These changes are induced either by mating itself or by sperm or seminal fluid proteins. In addition, studies have shown that axenic females—those lacking a microbiome—have altered fecundity compared to females with a microbiome, and that the microbiome of the female’s mate can influence reproductive success. However, the extent to which post-mating changes in transcript abundance are affected by microbiome state is not well-characterized. Here we investigated fecundity and the post-mating transcript abundance profile of axenic or control females after mating with either axenic or control males. We observed interactions between the female’s microbiome and her mating status: transcripts of genes involved in reproduction and genes with neuronal functions were differentially abundant depending on the females’ microbiome status, but only in mated females. In addition, immunity genes showed varied responses to either the microbiome, mating, or a combination of those two factors. We further observed that the male’s microbiome status influences the fecundity of both control and axenic females, while only influencing the transcriptional profile of axenic females. Our results indicate that the microbiome plays a vital role in the post-mating switch of the female’s transcriptome.

A genome-wide analysis of courting and mating responses in Drosophila melanogaster females

Genome ◽  
2004 ◽  
Vol 47 (5) ◽  
pp. 900-910 ◽  
Author(s):  
Mara KN Lawniczak ◽  
David J Begun
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Seminal Fluid ◽  
Differentially Expressed ◽  
Male Reproductive Success ◽  
Female Side ◽  
Accessory Gland Proteins ◽  
Seminal Fluid Proteins ◽  
A Genome ◽  
Immune Related Genes

In Drosophila melanogaster, seminal fluid proteins influence several components of female physiology and behavior, including re-mating rates, ovulation and oviposition, and sperm use. It is well-known that female flies are not simply passive vessels and that female-mediated interactions with male products are important to female (and thus male) reproductive success. While the population genetics, molecular evolution and physiological effects of seminal fluid proteins have been examined, the genetics and evolution of the female side of these post-mating interactions is unexplored in spite of work showing that female genotype and female-by-male genotype interactions are important determinants of sperm competition outcomes. Here we use microarrays to identify candidate genes involved in the female side of post-mating sexual interactions. We report the results of a whole-genome oligonucleotide chip experiment that reveals 23 genes differentially expressed between virgin females exposed and unexposed to courting males, and 38 genes differentially expressed between virgin and recently mated females. Immune related genes are overrepresented among the mating-influenced candidates. We use quantitative reverse-transcriptase PCR to independently assess gene expression changes for roughly half of the mating-affected candidate genes.Key words: reproduction, gene expression, Drosophila immune related genes, serine proteases, accessory gland proteins.

scholarly journals Divergence in sex peptide-mediated female post-mating responses in Drosophila melanogaster

2018 ◽  
Vol 285 (1886) ◽  
pp. 20181563 ◽  
Author(s):  
Kristina U. Wensing ◽  
Claudia Fricke
Keyword(s):  
Drosophila Melanogaster ◽  
Seminal Fluid ◽  
Lifetime Reproductive Success ◽  
Fitness Costs ◽  
Seminal Fluid Proteins ◽  
Sex Peptide ◽  
Fitness Measures ◽  
Different Populations ◽  
Reproductive Processes ◽  
Sexually Antagonistic Coevolution

Transfer and receipt of seminal fluid proteins crucially affect reproductive processes in animals. Evolution in these male ejaculatory proteins is explained with post-mating sexual selection, but we lack a good understanding of the evolution of female post-mating responses (PMRs) to these proteins. Some of these proteins are expected to mediate sexually antagonistic coevolution generating the expectation that females evolve resistance. One candidate in Drosophila melanogaster is the sex peptide (SP) which confers cost of mating in females. In this paper, we compared female SP-induced PMRs across three D. melanogaster wild-type populations after mating with SP-lacking versus control males including fitness measures. Surprisingly, we did not find any evidence for SP-mediated fitness costs in any of the populations. However, female lifetime reproductive success and lifespan were differently affected by SP receipt indicating that female PMRs diverged among populations. Injection of synthetic SP into virgin females further supported these findings and suggests that females from different populations require different amounts of SP to effectively initiate PMRs. Molecular analyses of the SP receptor suggest that genetic differences might explain the observed phenotypical divergence. We discuss the evolutionary processes that might have caused this divergence in female PMRs.

scholarly journals Male Seminal Fluid Proteins Are Essential for Sperm Storage in Drosophila melanogaster

Genetics ◽  
1999 ◽  
Vol 153 (2) ◽  
pp. 837-844 ◽  
Author(s):  
Uyen Tram ◽  
Mariana F Wolfner
Keyword(s):  
Drosophila Melanogaster ◽  
Seminal Fluid ◽  
Accessory Gland ◽  
Sperm Storage ◽  
Competitive Pcr ◽  
Seminal Fluid Proteins ◽  
Pcr Assays ◽  
Transgenic Drosophila ◽  
Direct Counts

AbstractThe seminal fluid that is transferred along with sperm during mating acts in many ways to maximize a male’s reproductive success. Here, we use transgenic Drosophila melanogaster males deficient in the seminal fluid proteins derived from the accessory gland (Acps) to investigate the role of these proteins in the fate of sperm transferred to females during mating. Competitive PCR assays were used to show that while Acps contribute to the efficiency of sperm transfer, they are not essential for the transfer of sperm to the female. In contrast, we found that Acps are essential for storage of sperm by females. Direct counts of stored sperm showed that 10% of normal levels are stored by females whose mates transfer little or no Acps along with sperm.

scholarly journals Sperm wars and the evolution of male fertility

Reproduction ◽  
2012 ◽  
Vol 144 (5) ◽  
pp. 519-534 ◽  
Author(s):  
Leigh W Simmons ◽  
John L Fitzpatrick
Keyword(s):  
Sperm Competition ◽  
Swimming Speed ◽  
Male Fertility ◽  
Seminal Fluid ◽  
Future Research ◽  
Sperm Length ◽  
Seminal Fluid Proteins ◽  
Control Male ◽  
Form And Function ◽  
And Function

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.

scholarly journals Female Genetic Contributions to Sperm Competition in Drosophila melanogaster

Genetics ◽  
2019 ◽  
Vol 212 (3) ◽  
pp. 789-800 ◽  
Author(s):  
Dawn S. Chen ◽  
Sofie Y. N. Delbare ◽  
Simone L. White ◽  
Jessica Sitnik ◽  
Martik Chatterjee ◽  
...  
Keyword(s):  
Nervous System ◽  
Drosophila Melanogaster ◽  
Sperm Competition ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
Association Studies ◽  
Genome Wide Association Studies ◽  
Link Type ◽  
Female Genotype ◽  
Mechanistic Basis

In many species, sperm can remain viable in the reproductive tract of a female well beyond the typical interval to remating. This creates an opportunity for sperm from different males to compete for oocyte fertilization inside the female’s reproductive tract. In Drosophila melanogaster, sperm characteristics and seminal fluid content affect male success in sperm competition. On the other hand, although genome-wide association studies (GWAS) have demonstrated that female genotype plays a role in sperm competition outcome as well, the biochemical, sensory, and physiological processes by which females detect and selectively use sperm from different males remain elusive. Here, we functionally tested 26 candidate genes implicated via a GWAS for their contribution to the female’s role in sperm competition, measured as changes in the relative success of the first male to mate (P1). Of these 26 candidates, we identified eight genes that affect P1 when knocked down in females, and showed that five of them do so when knocked down in the female nervous system. In particular, Rim knockdown in sensory pickpocket (ppk)+ neurons lowered P1, confirming previously published results, and a novel candidate, caup, lowered P1 when knocked down in octopaminergic Tdc2+ neurons. These results demonstrate that specific neurons in the female’s nervous system play a functional role in sperm competition and expand our understanding of the genetic, neuronal, and mechanistic basis of female responses to multiple matings. We propose that these neurons in females are used to sense, and integrate, signals from courtship or ejaculates, to modulate sperm competition outcome accordingly.

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