Seminal fluid and accessory male investment in sperm competition.
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ABSTRACT:
SUBMITTER: Ramm SA
PROVIDER: S-EPMC7661439 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundEjaculates contain a diverse mixture of sperm and seminal fluid proteins, the combination of which is crucial to male reproductive success under competitive conditions. Males should therefore tailor the production of different ejaculate components according to their social environment, with particular sensitivity to cues of sperm competition risk (i.e. how likely it is that females will mate promiscuously). Here we test this hypothesis using an established vertebrate model system, the house mouse (Mus musculus domesticus), combining experimental data with a quantitative proteomics analysis of seminal fluid composition. Our study tests for the first time how both sperm and seminal fluid components of the ejaculate are tailored to the social environment.ResultsOur quantitative proteomics analysis reveals that the relative production of different proteins found in seminal fluid--i.e. seminal fluid proteome composition--differs significantly according to cues of sperm competition risk. Using a conservative analytical approach to identify differential expression of individual seminal fluid components, at least seven of 31 secreted seminal fluid proteins examined showed consistent differences in relative abundance under high versus low sperm competition conditions. Notably three important proteins with potential roles in sperm competition--SVS 6, SVS 5 and CEACAM 10--were more abundant in the high competition treatment groups. Total investment in both sperm and seminal fluid production also increased with cues of heightened sperm competition risk in the social environment. By contrast, relative investment in different ejaculate components was unaffected by cues of mating opportunities.ConclusionsOur study reveals significant plasticity in different ejaculate components, with the production of both sperm and non-sperm fractions of the ejaculate strongly influenced by the social environment. Sperm competition risk is thus shown to be a key factor in male ejaculate production decisions, including driving plasticity in seminal fluid composition.
| S-EPMC4624372 | biostudies-literature
Project description:In many species, males can make rapid adjustments to ejaculate performance in response to sperm competition risk; however, the mechanisms behind these changes are not understood. Here, we manipulate male social status in an externally fertilising fish, chinook salmon (Oncorhynchus tshawytscha), and find that in less than 48 hr, males can upregulate sperm velocity when faced with an increased risk of sperm competition. Using a series of in vitro sperm manipulation and competition experiments, we show that rapid changes in sperm velocity are mediated by seminal fluid and the effect of seminal fluid on sperm velocity directly impacts paternity share and therefore reproductive success. These combined findings, completely consistent with sperm competition theory, provide unequivocal evidence that sperm competition risk drives plastic adjustment of ejaculate quality, that seminal fluid harbours the mechanism for the rapid adjustment of sperm velocity and that fitness benefits accrue to males from such adjustment.
| S-EPMC5669631 | biostudies-literature
Project description:A considerable body of evidence supports the prediction that males should increase their expenditure on the ejaculate in response to sperm competition risk. The prediction that they should reduce their expenditure with increasing sperm competition intensity is less well supported. Moreover, most studies have documented plasticity in sperm numbers. Here we show that male crickets Teleogryllus oceanicus exhibit reduced seminal fluid gene expression and accessory gland mass in response to elevated sperm competition intensity. Together with previous research, our findings suggest that strategic adjustments in seminal fluid composition contribute to competitive fertilization success in this species.
| S-EPMC5803594 | biostudies-literature
Project description:There is considerable evidence that males will increase the number of sperm ejaculated in response to sperm competition risk. However, whether they have the capacity to adjust seminal fluid components of the ejaculate has received less attention. Male crickets (Teleogryllus oceanicus) have been shown to adjust the viability of sperm in their ejaculate in response to sperm competition risk. Here we show that socially mediated plasticity in sperm viability is probably due, at least in part, to male adjustments in the protein composition of the seminal fluid. Seven seminal fluid protein genes were found to have an increased expression in males exposed to rival calls. Increased expression of these genes was correlated with increased sperm viability in whole ejaculates, and gene knockdown confirmed that at least one of these proteins promotes sperm viability. Our results lend support for recent theoretical models that predict complex responses in male allocation to seminal fluid composition in response to sperm competition risk.
| S-EPMC5577498 | biostudies-literature
Project description:Seminal fluid often makes up a large part of an ejaculate, yet most empirical and theoretical studies on sperm competition have focused on how sperm characteristics (number and quality) affect fertilization success. However, seminal fluid influences own sperm performance and may potentially influence the outcome of sperm competition, by also affecting that of rivals. As a consequence males may be expected to allocate their investment in both sperm and seminal fluid in relation to the potential level of competition. Grass goby (Zosterisessor ophiocephalus) is an external fertilizer with guard-sneaker mating tactics, where sperm competition risk varies according to the tactic adopted. Here, we experimentally manipulated grass goby ejaculates by separately combining sperm and seminal fluid from territorial and sneaker males. While sperm of sneaker and territorial males did not differ in their performance when they interacted with their own seminal fluid only, sperm of sneakers increased their velocity and fertilization rate in the presence of territorial males' seminal fluid. By contrast, sneaker males' seminal fluid had a detrimental effect on the performance of territorial males' sperm. Sperm velocity was unaffected by the seminal fluid of males employing the same tactic, suggesting that seminal fluid's effect on rival-tactic sperm is not based on a self/non-self recognition mechanism. Our findings show that cross interactions of sperm and seminal fluid may influence the fertilization success of competing ejaculates with males investing in both sperm and seminal fluid in response to sperm competition risk.
| S-EPMC3574395 | biostudies-literature
Project description:Postcopulatory sexual selection can select for sperm allocation strategies in males [1, 2], but males should also strategically allocate nonsperm components of the ejaculate [3, 4], such as seminal fluid proteins (Sfps). Sfps can influence the extent of postcopulatory sexual selection [5-7], but little is known of the causes or consequences of quantitative variation in Sfp production and transfer. Using Drosophila melanogaster, we demonstrate that Sfps are strategically allocated to females in response to the potential level of sperm competition. We also show that males who can produce and transfer larger quantities of specific Sfps have a significant competitive advantage. When males were exposed to a competitor male, matings were longer and more of two key Sfps, sex peptide [8] and ovulin [9], were transferred, indicating strategic allocation of Sfps. Males selected for large accessory glands (a major site of Sfp synthesis) produced and transferred significantly more sex peptide, but not more ovulin. Males with large accessory glands also had significantly increased competitive reproductive success. Our results show that quantitative variation in specific Sfps is likely to play an important role in postcopulatory sexual selection and that investment in Sfp production is essential for male fitness in a competitive environment.
| S-EPMC2737339 | biostudies-literature
Project description:Males of many species fine-tune their ejaculates in response to sperm competition risk. Resource availability and the number of competitors during development can also strongly influence sperm production. However, despite the key role of seminal proteins in mediating reproductive processes, it is unclear whether seminal protein investment is dependent on the developmental environment.We manipulated the developmental environment of Drosophila melanogaster by rearing flies at low and high density. As expected, this resulted in large and small (i.e. high and low condition) adult phenotypes, respectively.As predicted, large males produced more of two key seminal proteins, sex peptide (SP) and ovulin, and were more successful at obtaining matings with both virgin and previously mated females. However, there was only a weak and non-significant trend for large males to transfer more absolute quantities of SP at mating, and thus, small males ejaculated proportionally more of their stored accessory gland SP resources.Males transferred more receptivity-inhibiting SP to large females. Despite this, large females remated more quickly than small females and thus responded to their developmental environment over and above the quantity of SP they received.The results are consistent with two non-mutually exclusive hypotheses. First, flies might respond to condition-dependent reproductive opportunities, with (i) small males investing heavily in ejaculates when mating opportunities arise and large males strategically partitioning SP resources and (ii) small females remating at reduced rates because they have higher mating costs or need to replenish sperm less often.Second, flies may be primed by their larval environment to deal with similar adult population densities, with (i) males perceiving high density as signalling increased competition, leading small males to invest proportionally more SP resources at mating and (ii) females perceiving high density as signalling abundant potential mates, leading to a higher sexual receptivity threshold.Thus, by influencing the mating frequencies of both sexes, as well as the quantity of seminal proteins produced by males and received by females, the developmental environment is likely to have far-reaching and sex-specific consequences for sexual selection and sexual conflict.
| S-EPMC4974917 | biostudies-literature
Project description:BackgroundPromiscuous mating and sperm competition often induce arms races between the sexes with detrimental outcomes for females. However, ants with multiply-inseminated queens have only a single time-window for sperm competition and queens are predicted to gain control over the outcome of sperm storage quickly. The seminal fluid of Acromyrmex leaf-cutting ants reduces the viability of rival sperm, but how confrontations between unrelated ejaculates affect sperm storage remains unknown.ResultsWe investigated the effects of ejaculate admixture on sperm motility in A. echinatior and found that the proportion of motile spermatozoa, sperm swimming speed, and linearity of sperm movement increased when rival ejaculates were mixed in vitro. Major effects induced by the seminal fluid of rival males were of similar magnitude to those generated by queen reproductive tract secretions, whereas own seminal fluid induced lower sperm activation levels.ConclusionsOur results suggest that ant sperm respond via a self-non-self recognition mechanism to similar or shared molecules expressed in the reproductive secretions of both sexes. Lower sperm motility in the presence of own seminal fluid indicates that enhanced motility is costly and may trade-off with sperm viability during sperm storage, consistent with studies in vertebrates. Our results imply that ant spermatozoa have evolved to adjust their energetic expenditure during insemination depending on the perceived level of sperm competition.
| S-EPMC5865361 | biostudies-literature
Project description:Male eagerness to mate is a central paradigm of sexual selection theory. However, limited sperm supplies mean that male sexual restraint might sometimes be favored under promiscuous mating. Here, we demonstrate dynamic plasticity in male mating effort when females are encountered sequentially under varying sperm competition risk. Rather than showing consistent eagerness to mate, male house mice (Mus musculus domesticus) instead tailor their mating effort according to likely reproductive payoffs. They are significantly less likely to mate when sperm competition is certain and potential reproductive payoffs low, but dramatically increase investment if they do choose to mate under such circumstances. By contrast, male mice are significantly more likely to mate in situations simulating extra-territorial copulations, where future risk of competition is high but so too are potential reproductive rewards. Differential mating propensity appears to be the primary mechanism by which male house mice allocate sperm adaptively under sperm competition risk because we find no evidence for facultative adjustment of sperm numbers per ejaculate or ejaculation frequency in response to female-related cues. We conclude that sequential male mate choice under sperm competition risk could be a widespread but often unappreciated mechanism of strategic sperm allocation.
| S-EPMC4014308 | biostudies-literature
Project description:The role of non-gametic components of the ejaculate (seminal fluid) in fertility and sperm competitiveness is now well established. Surprisingly, however, we know far less about female reproductive fluid (FRF) in the context of sexual selection, and insights into male-FRF interactions in the context of sperm competition have only recently emerged. Despite this limited knowledge, evidence from taxonomically diverse species has revealed insights into the effects of FRF on sperm traits that have previously been implicated in studies of sperm competition. Specifically, through the differential effects of FRF on a range of sperm traits, including chemoattraction and alterations in sperm velocity, FRF has been shown to exert positive phenotypic effects on the sperm of males that are preferred as mating partners, or those from the most compatible or genetically diverse males. Despite these tantalizing insights into the putative sexually selected functions of FRF, we largely lack a mechanistic understanding of these processes. Taken together, the evidence presented here highlights the likely ubiquity of FRF-regulated biases in fertilization success across a diverse range of taxa, thus potentially elevating the importance of FRF to other non-gametic components that have so far been studied largely in males. This article is part of the theme issue 'Fifty years of sperm competition'.
| S-EPMC7661459 | biostudies-literature