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

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.

2021 ◽  
Author(s):  
Jake Galvin ◽  
Erica Larson ◽  
Sevan Yedigarian ◽  
Mohammad Rahman ◽  
Kirill Borziak ◽  
...  

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.


2018 ◽  
Vol 103 ◽  
pp. 1-10 ◽  
Author(s):  
Hanna Ruhmann ◽  
Mareike Koppik ◽  
Mariana F. Wolfner ◽  
Claudia Fricke

Genome ◽  
2004 ◽  
Vol 47 (5) ◽  
pp. 900-910 ◽  
Author(s):  
Mara KN Lawniczak ◽  
David J Begun

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.


2020 ◽  
Author(s):  
S. Mark Wainwright ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
Josephine E.E.U. Hellberg ◽  
...  

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.


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

2019 ◽  
Author(s):  
Michael Weber ◽  
Bahar Patlar ◽  
Steven A. Ramm

AbstractAlong with sperm, in many taxa male ejaculates also contain a complex mixture of proteins, peptides and other substances found in seminal fluid. Once seminal fluid proteins (SFPs) are transferred to the mating partner, they play crucial roles in mediating post-mating sexual selection, since they can modulate the partner’s behavior and physiology in ways that influence the reproductive success of both partners. One way in which sperm donors can maximize their own reproductive success is by changing the partners’ (sperm recipient’s) postcopulatory behavior to prevent or delay re-mating, thereby decreasing the likelihood or intensity of sperm competition. We therefore adopted a quantitative genetic approach combining gene expression and behavioral data to identify candidates that could mediate such a response in the simultaneously hermaphroditic flatwormMacrostomum lignano. We identified two putative SFPs - Mlig-pro46 and Mlig-pro63 - that exhibit a negative genetic correlation between transcript expression and mating frequency. Importantly, however, in one of the two different group sizes, differing in their sperm competition level, in which we measured genetic correlations, these same two transcripts are also linked to a second post-mating behavior inM. lignano, namely the ‘suck’ behavior of recipients in which, upon ejaculate receipt, the worm places its pharynx over its female genital opening and appears to attempt to remove ejaculate components. To therefore investigate directly whether these two candidates manipulate partner behavior, and test whether this impacts on competitive fertilization success, we performed a manipulative experiment using RNA interference-induced knockdown to ask how loss of Mlig-pro46 and Mlig-pro63 expression, singly and in combination, affects mating frequency, partner suck propensity and both defensive and offensive sperm competitive ability (P1andP2, respectively). None of the knock-down treatments impacted strongly on mating frequency or sperm competitive ability, but the knock-down of Mlig-pro63 resulted in a significantly decreased ‘suck’ propensity of mating partners. This suggests that Mlig-pro63 may normally act as a cue in the ejaculate to trigger recipient suck behavior, though the functional and adaptive significance of these two seminal proteins from a donor perspective remains enigmatic.


1997 ◽  
Vol 200 (22) ◽  
pp. 2833-2840
Author(s):  
W Zheng ◽  
C Strobeck ◽  
N Stacey

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.


Behaviour ◽  
2015 ◽  
Vol 152 (7-8) ◽  
pp. 917-940 ◽  
Author(s):  
Devaleena S. Pradhan ◽  
Madelyne C. Willis ◽  
Tessa K. Solomon-Lane ◽  
Kevin Thonkulpitak ◽  
Matthew S. Grober

While males typically compete for females, species with female biased sex ratios and/or large male investment in offspring care often exhibit reversed sex roles. Here we investigated, in a haremic fish species, the bluebanded goby,Lythrypnus dalli, the impact of male and female courtship behaviour on male reproductive success, measured as the total number of eggs in the nest and total number of developed eggs. Reproductive success was not associated with rates of male behaviour, such as parenting, approaching and courtship, but was associated with rates of female courtship. Consistent with predictions for a role-reversed reproductive strategy, only males demonstrated nest care and females exhibited high rates of courtship and intrasexual competition, such that alpha females interrupted courtship solicitations by beta females. Overall, these data are consistent with sex role reversal inL. dalliand show that the expression of male courtship behaviour does not interfere with paternal care.


2013 ◽  
Vol 103 (5) ◽  
pp. 570-577 ◽  
Author(s):  
J.P. Michaud ◽  
Mahadev Bista ◽  
Geetanjali Mishra ◽  
Omkar Singh

AbstractMale contributions, both chemical and behavioural, can influence female sperm usage and reproductive success. To determine whether such male factors are subject to depletion inCoccinella septempunctataandCoccinella transversalis, we tested the effects of male mating history on male virility, as estimated by measures of mating behaviour, female reproductive success and progeny fitness, with parental age held constant. Overt measures of male mating effort (wriggling duration, number of shaking bouts and total copula duration) all diminished from virgin to 5 × mated males and were mirrored by concurrent declines in female fecundity and fertility (measured over 20 days). Paternal effects were also observed which diminished as a function of mating history, suggesting that transgenerational signals of male origin are also subject to depletion. Progeny of virgin fathers had higher rates of survival (C. transversalis) and faster development (both species) than progeny of 5 × mated fathers. Seminal fluid proteins are known to have allohormonal properties and can stimulate female fecundity and fertility in a number of insects, making them strong candidates for depletion as a function of mating activity. However, it is also possible that sperm limitation and/or reduced tactile stimulation of females by multiple-mated males may have contributed to some of the observed effects.


2015 ◽  
Vol 27 (6) ◽  
pp. 934 ◽  
Author(s):  
Heide Schatten ◽  
Qing-Yuan Sun

The effects of oocyte aging on meiotic spindle dynamics have been well recognised, but the mechanisms underlying the effects are not well understood. In this paper we review the role of centrosomes and the microtubule cytoskeleton in meiotic spindle formation and maintenance, and the impact of oocyte aging on spindle integrity resulting in centrosome and microtubule dysfunctions that are associated with aneuploidy. Loss of spindle integrity includes dispersion of proteins from the centrosome core structure and loss of attachment of microtubules to centrosomes and kinetochores, which will result in abnormal chromosome separation. The inability of centrosomal proteins to accurately associate with the centrosome structure may be the result of destabilisation of the core structure itself or of microtubule destabilisation at the centrosome-facing microtubule areas that are acetylated in fresh oocytes but may not be acetylated in aging oocytes. Microtubule destabilisation prevents accurate motor-driven transport of centrosomal proteins along microtubules to form and maintain a functional centrosome. Other factors to form and maintain the MII spindle include signal transductions that affect microtubule dynamics and stability. Understanding the mechanisms underlying centrosome and microtubule dysfunctions during oocyte aging will allow diagnosis and analysis of oocyte quality and abnormalities as important aspects for targeted treatment of aging oocytes to extend or restore viability and developmental capacity. New therapeutic approaches will allow improvements in reproductive success rates in IVF clinics, as well as improvements in reproductive success rates in farm animals. This review is focused on: (1) centrosome and microtubule dynamics in fresh and aging oocytes; (2) regulation of centrosome and/or microtubule dynamics and function; and (3) possible treatments to extend the oocyte’s reproductive capacity and viability span.


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