scholarly journals Drosophila Sex Peptide Controls the Assembly of Lipid Microcarriers in Seminal Fluid

2020 ◽  
Author(s):  
S. Mark Wainwright ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
Josephine E.E.U. Hellberg ◽  
...  
Keyword(s):  
Reproductive Success ◽  
Neutral Lipid ◽  
Seminal Fluid ◽  
Critical Role ◽  
Fruit Fly ◽  
Male Reproductive Success ◽  
Sex Peptide ◽  
Accessory Glands ◽  
Assembly Factor ◽  
Female Physiology

AbstractSeminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behaviour. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterised protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term post-mating responses including ovulation, elevated feeding and reduced receptivity to remating, primarily signalling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating, where they rapidly disassemble. Remarkably, SP is a key assembly factor for microcarriers and is also required for the female disassembly process to occur normally. Males expressing non-functional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread defects in ejaculate function. Our data therefore reveal a novel role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species, which lack the signalling functions seen in D. melanogaster.Significance StatementSeminal fluid plays a critical role in reprogramming female physiology and behaviour to promote male reproductive success. We show in the fruit fly that specific seminal proteins, including the archetypal ‘female-reprogramming’ molecule Sex Peptide, are stored in male seminal secretions in association with large neutral lipid-containing microcarriers, which rapidly disperse in females. Related structures are also observed in other Sex Peptide-expressing Drosophila species. Males lacking Sex Peptide have structurally defective microcarriers, leading to abnormal cargo loading and transfer to females. Our data reveal that this key signalling molecule in Drosophila seminal fluid is also a microcarrier assembly factor that controls transfer of other seminal factors, and that this may be a more evolutionarily ancient role of this protein.

scholarly journals Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid

2021 ◽  
Vol 118 (5) ◽  
pp. e2019622118
Author(s):  
S. Mark Wainwright ◽  
Ben R. Hopkins ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Fruit Fly ◽  
Male Reproductive Success ◽  
Mutant Proteins ◽  
Macromolecular Assemblies ◽  
Sex Peptide ◽  
Accessory Glands ◽  
Storage Organs ◽  
Paired Male ◽  
Male Specific

Seminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behavior. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterized protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term postmating responses, including increased ovulation, elevated feeding, and reduced receptivity to remating, primarily signaling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating where they rapidly disassemble. Remarkably, SP is a key microcarrier assembly and disassembly factor. Its absence leads to major changes in the seminal proteome transferred to females upon mating. Males expressing nonfunctional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread abnormalities in ejaculate function. Our data therefore reveal a role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species that lack the signaling functions seen in D. melanogaster.

scholarly journals Male reproductive ageing: a tale of the whole ejaculate

Reproduction ◽  
2019 ◽  
Vol 158 (6) ◽  
pp. R219-R229 ◽  
Author(s):  
Claudia Fricke ◽  
Mareike Koppik
Keyword(s):  
Reproductive Success ◽  
Conformational Changes ◽  
Seminal Fluid ◽  
Reproductive Capacity ◽  
Male Reproductive Success ◽  
Seminal Fluid Proteins ◽  
Area Of Interest ◽  
General Decline ◽  
Age Dependent ◽  
The Impact

Ageing is nearly ubiquitous and encompasses all biological functions. We here focus on age-dependent changes in male reproductive capacity across a broad range of animal taxa. While there has been a long-standing focus on mating ability and overall reproductive success, we here highlight the underlying mechanisms that explain loss in fertilisation capacity in ageing males. Fertilisation is mediated by not only the presence of sperm, but also the cocktail of seminal fluid proteins that ensure sperm survival, capacitation and interaction with female physiology. Sperm ageing has received much attention in studies of male reproductive senescence; however, post-mating processes include a number of interlocked steps that together cumulate in successful fertilisation. As such we consider male ability to elicit female post mating responses such as uterine conformational changes, sperm storage and ovulation and the components within the ejaculate that mediate these post-mating processes. For the latter seminal fluid proteins are key and hence we reflect on age-dependent changes in quality of the entire ejaculate and its consequences for male reproductive capacity. While first studies accrue and highlight that changes in the non-sperm fraction can explain substantial variation in senescent male reproductive success and male ability to induce post-mating responses necessary for fertilisation many open questions still remain that warrant further investigations. One being what the potential age-dependent changes in composition are or whether there is a general decline and how this interacts with sperm to affect fertilisation success. Further, the impact females might have to ameliorate these changes will be an area of interest.

scholarly journals Regulation of Mating-Induced Increase in Female Germline Stem Cells in the Fruit Fly Drosophila melanogaster

2021 ◽  
Vol 12 ◽  
Author(s):  
Ryo Hoshino ◽  
Ryusuke Niwa
Keyword(s):  
Stem Cells ◽  
Drosophila Melanogaster ◽  
Energy Demand ◽  
Seminal Fluid ◽  
Fruit Fly ◽  
Egg Laying ◽  
Germline Stem Cells ◽  
Humoral Factors ◽  
Mating Response ◽  
Sex Peptide

In many insect species, mating stimuli can lead to changes in various behavioral and physiological responses, including feeding, mating refusal, egg-laying behavior, energy demand, and organ remodeling, which are collectively known as the post-mating response. Recently, an increase in germline stem cells (GSCs) has been identified as a new post-mating response in both males and females of the fruit fly, Drosophila melanogaster. We have extensively studied mating-induced increase in female GSCs of D. melanogaster at the molecular, cellular, and systemic levels. After mating, the male seminal fluid peptide [e.g. sex peptide (SP)] is transferred to the female uterus. This is followed by binding to the sex peptide receptor (SPR), which evokes post-mating responses, including increase in number of female GSCs. Downstream of SP-SPR signaling, the following three hormones and neurotransmitters have been found to act on female GSC niche cells to regulate mating-induced increase in female GSCs: (1) neuropeptide F, a peptide hormone produced in enteroendocrine cells; (2) octopamine, a monoaminergic neurotransmitter synthesized in ovary-projecting neurons; and (3) ecdysone, a steroid hormone produced in ovarian follicular cells. These humoral factors are secreted from each organ and are received by ovarian somatic cells and regulate the strength of niche signaling in female GSCs. This review provides an overview of the latest findings on the inter-organ relationship to regulate mating-induced female GSC increase in D. melanogaster as a model. We also discuss the remaining issues that should be addressed in the future.

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 Morphological and Developmental Traits of the Binucleation of Male Accessory Gland Cells in the Benthic Water Bug, Aphelocheirus vittatus (Hemiptera: Aphelochiridae)

2020 ◽  
Vol 20 (4) ◽  
Author(s):  
Koji Takeda ◽  
Jun Yamauchi ◽  
Takashi Adachi-Yamada
Keyword(s):  
Epithelial Cells ◽  
Cell Fusion ◽  
Seminal Fluid ◽  
Physiological Role ◽  
Reproductive Organs ◽  
Accessory Gland ◽  
Male Reproductive Success ◽  
Reproductive Behaviors ◽  
Accessory Glands ◽  
Close Relationship

Abstract The male accessory glands (MAGs) in insects are pair(s) of internal reproductive organs that produce and secrete the plasma component of seminal fluid. In various insects, MAG size is important for male reproductive success because the fluid provides physiologically active substances and/or nutrients to females to control sperm as well as female reproductive behaviors. Although the MAG epithelial cells in most insect species are standard mononucleate cells, those in some insect taxa are binucleate due to incomplete cytokinesis (e.g., Drosophila [Fallén] [Diptera: Drosophilidae]) or cell fusion (e.g., Cimex [Linnaeus] [Hemiptera: Cimicidae]). In the case of Drosophila, the apicobasal position of the two nuclei relative to the epithelial plane changes from vertical to horizontal after nutrient intake, which allows the volume of the MAG cavity to expand effectively. On the other hand, in the case of Cimex, the positions of the two nuclei do not change apicobasally in response to feeding, but their position relative to the proximodistal axis varies depending on the tubular/spherical organ morphology. Here, we report that the MAG of the benthic water bug Aphelocheirus vittatus (Matsumura) (Hemiptera: Aphelochiridae) shows binucleation in all epithelial cells. Despite the phylogenetically close relationship between Aphelocheirus and Cimex, the MAG cells in Aphelocheirus showed a Drosophila-like apicobasal change in the position of the two nuclei in response to feeding. Furthermore, the cytological processes during binucleation are more similar to those in Drosophila (incomplete cytokinesis) than to those in Cimex (cell fusion). These results indicate that the physiological role and mechanism of binucleation in MAG cells changed during the evolution of Hemiptera.

scholarly journals Seminal Fluid Protein Allocation and Male Reproductive Success

2009 ◽  
Vol 19 (9) ◽  
pp. 751-757 ◽  
Author(s):  
Stuart Wigby ◽  
Laura K. Sirot ◽  
Jon R. Linklater ◽  
Norene Buehner ◽  
Federico C.F. Calboli ◽  
...  
Keyword(s):  
Reproductive Success ◽  
Seminal Fluid ◽  
Male Reproductive Success ◽  
Seminal Fluid Protein

scholarly journals Post-Insemination Selection Dominates Pre-Insemination Selection in Driving Rapid Evolution of Male Competitive Ability

2021 ◽  
Author(s):  
Katja R Kasimatis ◽  
Megan J Moerdyk-Schauwecker ◽  
Ruben Lancaster ◽  
Alexander Smith ◽  
John H Willis ◽  
...  
Keyword(s):  
Sexual Selection ◽  
Reproductive Success ◽  
Critical Role ◽  
Rapid Evolution ◽  
Genetic System ◽  
Fertilization Success ◽  
Male Reproductive Success ◽  
Complex Process ◽  
Explicit Consideration ◽  
Genome Level

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male's perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.

The steroid pheromone 4-pregnen-17,20ss-diol-3-one increases fertility and paternity in goldfish.

1997 ◽  
Vol 200 (22) ◽  
pp. 2833-2840
Author(s):  
W Zheng ◽  
C Strobeck ◽  
N Stacey
Keyword(s):  
Reproductive Success ◽  
Seminal Fluid ◽  
Sperm Quality ◽  
Paternity Analysis ◽  
Male Reproductive Success ◽  
Spawning Activity ◽  
Control Male ◽  
Goldfish Carassius Auratus ◽  
Serum Gonadotropin

Previous studies in goldfish (Carassius auratus) showed that the oocyte maturation-inducing steroid 4-pregnen-17,20ss-diol-3-one (17,20ssP) functions after release as a pheromone that increases male serum gonadotropin II (GtH II) concentration, milt (sperm and seminal fluid) volume and sexual activity, effects hypothesized to increase male reproductive success in the sperm competition of multi-male spawnings. The present study tested this hypothesis by determining whether overnight exposure to 17,20ssP increases fertility. In pair spawnings, 17,20ssP-exposed males fertilized a greater percentage of eggs than did control males, apparently because 17,20ssP-exposed males had more releasable sperm at the onset of spawning. Microsatellite DNA paternity analysis showed that 17,20ssP-exposed males also fertilized more eggs in competitive spawnings involving one control male and one 17,20ssP-exposed male. This effect of 17,20ssP on competitive fertility could be due to demonstrated increases in spawning activity, milt volume, duration of sperm motility and proportion of motile sperm. However, it appears that a change in sperm quality is a major component of the pheromonal effect because, in competitive in vitro fertilizations, sperm from 17,20ssP-exposed males fertilized more eggs than did sperm from control males. The results indicate that the response to pheromonal 17,20ssP is a major determinant of reproductive success in male goldfish.

scholarly journals Postweaning maternal care increases male chimpanzee reproductive success

2020 ◽  
Vol 6 (38) ◽  
pp. eaaz5746
Author(s):  
Catherine Crockford ◽  
Liran Samuni ◽  
Linda Vigilant ◽  
Roman M. Wittig
Keyword(s):  
Reproductive Success ◽  
Parental Investment ◽  
Maternal Care ◽  
Parental Loss ◽  
Male Reproductive Success ◽  
Complex Societies ◽  
Successful Reproduction ◽  
Using Data

Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This “prolonged dependency” is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.

scholarly journals Sperm modulate uterine immune parameters relevant to embryo implantation and reproductive success in mice

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
John E. Schjenken ◽  
David J. Sharkey ◽  
Ella S. Green ◽  
Hon Yeung Chan ◽  
Ricky A. Matias ◽  
...  
Keyword(s):  
Reproductive Success ◽  
Seminal Fluid ◽  
Embryo Implantation ◽  
Reproductive Investment ◽  
Global Gene Expression ◽  
Wild Type ◽  
Mouse Uterus ◽  
Immune Parameters ◽  
Oocyte Fertilization

AbstractSeminal fluid factors modulate the female immune response at conception to facilitate embryo implantation and reproductive success. Whether sperm affect this response has not been clear. We evaluated global gene expression by microarray in the mouse uterus after mating with intact or vasectomized males. Intact males induced greater changes in gene transcription, prominently affecting pro-inflammatory cytokine and immune regulatory genes, with TLR4 signaling identified as a top-ranked upstream driver. Recruitment of neutrophils and expansion of peripheral regulatory T cells were elevated by seminal fluid of intact males. In vitro, epididymal sperm induced IL6, CXCL2, and CSF3 in uterine epithelial cells of wild-type, but not Tlr4 null females. Collectively these experiments show that sperm assist in promoting female immune tolerance by eliciting uterine cytokine expression through TLR4-dependent signaling. The findings indicate a biological role for sperm beyond oocyte fertilization, in modulating immune mechanisms involved in female control of reproductive investment.

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