Sperm competition games: the risk model can generate higher sperm allocation to virgin females

We examine the risk model in sperm competition games for cases where female fertility increases significantly with sperm numbers (sperm limitation). Without sperm competition, sperm allocation increases with sperm limitation. We define 'average risk' as the probability q that females in the population mate twice, and 'perceived risk' as the information males gain about the sperm competition probability with individual females. If males obtain no information from individual females, sperm numbers increase with q unless sperm limitation is high and one of the two competing ejaculates is strongly disfavoured. If males can distinguish between virgin and mated females, greater sperm allocation to virgins is favoured by high sperm limitation, high q, and by the second male's ejaculate being disfavoured. With high sperm limitation, sperm allocation to virgins increases and to mated females decreases with q at high q levels. With perfect information about female mating pattern, sperm allocation (i) to virgins that will mate again exceeds that to mated females and to virgins that will mate only once, (ii) to virgins that mate only once exceeds that for mated females if q is high and there is high second male disadvantage and (iii) to each type of female can decrease with q if sperm limitation is high, although the average allocation increases at least across low q levels. In general, higher sperm allocation to virgins is favoured by: strong disadvantage to the second ejaculate, high sperm limitation, high average risk and increased information (perceived risk). These conditions may apply in a few species, especially spiders.     

Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory—broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal. Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae). We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size. Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.     

Sperm allocation strategies and female resistance: a unifying perspective

The classical viewpoint in sperm competition theory, which holds that males evolve sperm allocation strategies in response to a given degree of sperm competition, has recently been challenged by an alternative viewpoint, which holds that the degree of sperm competition is itself a consequence of these same strategies. Here, we present a game theory model that unites these alternative views as the endpoints of a continuum. Based on the recognition that female control over mating may limit the extent to which male strategies affect the degree of sperm competition, we investigate sperm allocation strategies in a setting where females can resist excessive matings more or less successfully. We discuss how conflicting predictions made by previous theory relate to implicit assumptions about female resistance behavior. Moreover, we show that female resistance, while being highly relevant to the predicted relationship between ejaculate size and the degree of sperm competition, has little effect on the predicted positive correlation between relative testis size and the degree of sperm competition. This result strengthens one of the central predictions of sperm competition theory and is in accordance with empirical findings from a wide range of taxa.     

Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics

Female remating rate dictates the level of sperm competition in a population, and extensive research has focused on how sperm competition generates selection on male ejaculate allocation. Yet the way ejaculate allocation strategies in turn generate selection on female remating rates, which ultimately influence levels of sperm competition, has received much less consideration despite increasing evidence that both mating itself and ejaculate traits affect multiple components of female fitness. Here, we develop theory to examine how the effects of mating on female fertility, fecundity and mortality interact to generate selection on female remating rate. When males produce more fertile ejaculates, females are selected to mate less frequently, thus decreasing levels of sperm competition. This could in turn favour decreased male ejaculate allocation, which could subsequently lead to higher female remating. When remating simultaneously increases female fecundity and mortality, females are selected to mate more frequently, thus exacerbating sperm competition and favouring male traits that convey a competitive advantage even when harmful to female survival. While intuitive when considered separately, these predictions demonstrate the potential for complex coevolutionary dynamics between male ejaculate expenditure and female remating rate, and the correlated evolution of multiple male and female reproductive traits affecting mating, fertility and fecundity.     

Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade‐offs in mating systems that have been overlooked in the past.     

Sperm competition and ejaculate economics

Sperm competition was identified in 1970 as a pervasive selective force in post‐copulatory sexual selection that occurs when the ejaculates of different males compete to fertilise a given set of ova. Since then, sperm competition has been much studied both empirically and theoretically. Because sperm competition often favours large ejaculates, an important challenge has been to understand the evolution of strategies through which males invest in sperm production and economise sperm allocation to maximise reproductive success under competitive conditions. Sperm competition mechanisms vary greatly, depending on many factors including the level of sperm competition, space constraints in the sperm competition arena, male mating roles, and female influences on sperm utilisation. Consequently, theoretical models of ejaculate economics are complex and varied, often with apparently conflicting predictions. The goal of this review is to synthesise the theoretical basis of ejaculate economics under sperm competition, aiming to provide empiricists with categorised model assumptions and predictions. We show that apparent contradictions between older and newer models can often be reconciled and there is considerable consensus in the predictions generated by different models. We also discuss qualitative empirical support for some of these predictions, and detail quantitative matches between predictions and observations that exist in the yellow dung fly. We argue that ejaculate economic theory represents a powerful heuristic to explain the diversity in ejaculate traits at multiple levels: across species, across males and within individual males. Future progress requires greater understanding of sperm competition mechanisms, quantification of trade‐offs between ejaculate allocation and numbers of matings gained, further knowledge of mechanisms of female sperm selection and their associated costs, further investigation of non‐sperm ejaculate effects, and theoretical integration of pre‐ and post‐copulatory episodes of sexual selection.     

Strategic ejaculation in the egg parasitoid Trichogramma turkestanica (Hymenoptera: Trichogrammatidae)

Abstract.  1. Several parameters influence sperm allocation by males, including their size and sperm stock, intra-specific variability, quality of females', as well as the risk and intensity of sperm competition.
2. Models predict that males should invest the maximum ejaculate size when sperm competition intensity is low. As sperm competition intensity increases, males should decrease the number of sperm transferred during mating.
3. This decrease in sperm transfer to females occurs because the benefits gained by males with each extra unit of expenditure on sperm decrease. When sperm supply is not unlimited, males could expect a better return by keeping some or all sperm for mating under lower competition intensity.
4. In this study, the ejaculate size of males that were kept in groups of one, five or 10 males prior to mating, has been investigated in the haplodiploid egg parasitoid Trichogramma turkestanica Meyer (Hymenoptera: Trichogrammatidae).
5. As predicted by theory, the number of sperm transferred decreased significantly with an increase in the number of rivals.
6. This is the first study showing strategic sperm allocation depending on sperm competition intensity in a parasitoid.     

Larger testes are associated with a higher level of polyandry, but a smaller ejaculate volume, across bushcricket species (Tettigoniidae)

While early models of ejaculate allocation predicted that both relative testes and ejaculate size should increase with sperm competition intensity across species, recent models predict that ejaculate size may actually decrease as testes size and sperm competition intensity increase, owing to the confounding effect of potential male mating rate. A recent study demonstrated that ejaculate volume decreased in relation to increased polyandry across bushcricket species, but testes mass was not measured. Here, we recorded testis mass for 21 bushcricket species, while ejaculate (ampulla) mass, nuptial gift mass, sperm number and polyandry data were largely obtained from the literature. Using phylogenetic-comparative analyses, we found that testis mass increased with the degree of polyandry, but decreased with increasing ejaculate mass. We found no significant relationship between testis mass and either sperm number or nuptial gift mass. While these results are consistent with recent models of ejaculate allocation, they could alternatively be driven by substances in the ejaculate that affect the degree of polyandry and/or by a trade-off between resources spent on testes mass versus non-sperm components of the ejaculate.     

Ejaculate allocation under varying sperm competition risk in the house mouse, Mus musculus domesticus

A common mechanism through which males can enhance their successin postcopulatory contests over paternity is to inseminate moresperm than their rivals. However, ejaculate production is costlyand the evolution of prudent sperm allocation strategies sensitiveto variation in local levels of sperm competition has now beendemonstrated in diverse taxa, including mammals. Theory predictsan increased sperm allocation in response to an elevated riskof sperm competition, but here we show that male house mice(Mus musculus domesticus) instead ejaculate fewer sperm perejaculate when mating in the presence of a rival male. Thissurprising sperm allocation pattern may be a necessary consequenceof adaptive changes in copulatory behavior, enabling males toachieve more rapid sperm transfer and/or to ejaculate repeatedlyunder risk of sexual competition. The size of a second ejaculatecomponent, the copulatory plug, is unaffected by sperm competitionrisk. Our results highlight how the often complex interplaybetween different reproductive traits can affect the evolutionof sperm competition phenotypes.     

Sexual selection and sperm quantity: meta‐analyses of strategic ejaculation

Multiple mating or group spawning leads to post‐copulatory sexual selection, which generally favours ejaculates that are more competitive under sperm competition. In four meta‐analyses we quantify the evidence that sperm competition (SC) favours greater sperm number using data from studies of strategic ejaculation. Differential investment into each ejaculate emerges at the individual level if males exhibit phenotypic plasticity in ejaculate properties in response to the likely risk and/or intensity of sperm competition after a given mating. Over the last twenty years, a series of theoretical models have been developed that predict how ejaculate size will be strategically adjusted in relation to: (a) the number of immediate rival males, with a distinction made between 0 versus 1 rival (‘risk’ of SC) and 1 versus several rivals (‘intensity’ of SC); (b) female mating status (virgin or previously mated); and (c) female phenotypic quality (e.g. female size or condition). Some well‐known studies have reported large adjustments in ejaculate size depending on the relevant social context and this has led to widespread acceptance of the claim that strategic sperm allocation occurs in response to each of these factors. It is necessary, however, to test each claim separately because it is easy to overlook studies with weak or negative findings. Compiling information on the variation in outcomes among species is potentially informative about the relevance of these assumptions in different taxa or mating systems. We found strong evidence that, on average, males transfer larger ejaculates to higher quality females. The effect of female mating status was less straightforward and depended on how ejaculate size was measured (i.e. use of proxy or direct measure). There is strong evidence that ejaculate size increased when males were exposed to a single rival, which is often described as a response to the risk of SC. There is, however, no evidence for the general prediction that ejaculate size decreases as the number of rivals increases from one to several males (i.e. in response to a higher intensity of SC which lowers the rate of return per sperm released). Our results highlight how meta‐analysis can reveal unintentional biases in narrative literature reviews. We note that several assumptions of theoretical models can alter an outcome's predicted direction in a given species (e.g. the effect of female mating status depends on whether there is first‐ or last‐male sperm priority). Many studies do not provide this background information and fail to make strong a priori predictions about the expected response of ejaculate size to manipulation of the mating context. Researchers should be explicit about which model they are testing to ensure that future meta‐analyses can better partition studies into different categories, or control for continuous moderator variables.     

Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets

Female sexual promiscuity can have significant effects on male mating decisions because it increases the intensity of competition between ejaculates for fertilization. Because sperm production is costly, males that can detect multiple matings by females and allocate sperm strategically will have an obvious fitness advantage. The presence of rival males is widely recognized as a cue used by males to assess sperm competition. However, for species in which males neither congregate around nor guard females, other more cryptic cues might be involved. Here, we demonstrate unprecedented levels of sperm competition assessment by males, which is mediated via the use of chemical cues. Using the cricket Teleogryllus oceanicus, we manipulated male perception of sperm competition by experimentally coating live unmated females with cuticular compounds extracted from males. We found that males adjusted their ejaculate allocation in response to these compounds: the viability of sperm contained within a male's ejaculate decreased as the number of male extracts applied to his virgin female partner was increased. We further show that males do not respond to the relative concentration of male compounds present on females, but rather to the number of distinct signature odours of individual males. Our results conform to sperm competition theory, and show for the first time, to our knowledge, that males can detect different intensities of sperm competition by using distinct chemical cues of individual males present on females.     

Ejaculate expenditures of male crickets in response to varying risk and intensity of sperm competition: not all species play games

Costs incurred in the manufacture of ejaculates may constrainthe number of sperm that males can produce, so males shouldshow some economy in their allocation of sperm across multiplematings. In species in which females mate with multiple malesand are capable of storing sperm for extended periods, spermallocation of males should be tailored to the risk of spermcompetition. Recent game theory predicts that males shouldtransfer the least sperm when there are no other rivals, andthe most sperm when only one other rival is likely to inseminatethe female. However, as the numbers of competitors increasesbeyond two, the models predict a corresponding decrease in ejaculate expenditure. We tested these predictions in three cricket species, Gryllodes sigillatus, Gryllus veletis, and Gryllus texensis, assessing the sperm allocation of males held under three levelsof apparent interrival competition: no rivals, one rival andsix rivals. Sperm allocation of G. veletis varied accordingto theory: males increased their sperm allocation with an increasedrisk of sperm competition (no rivals vs. one), but decreasedtheir allocation with an increased intensity of sperm competition(one rival vs. six). Sperm allocation of male G. texensis showedno significant response to the density of rivals, and spermallocation in G. sigillatus was influenced by an unexpectedinteraction between treatment density and the order in whichmales experienced the three treatments. The observed interspecificvariation in facultative sperm allocation may be due to interspecificdifferences in population density, rearing environment, orfemale mating behavior.     

Ejaculate size varies with socio-sexual situation in an insect

Abstract.

• 1 Males operate within a finite energy budget and cannot produce limitless supplies of sperm. On the other hand, when a female mates with a second male while still containing fertile sperm from a rival male, selection should favour the male that inseminates more sperm. Optimal strategy should thus be for males to exercise discretion in the allocation of sperm to individual females. Assuming the outcome of sperm competition to be based on either the raffle or kamikaze principles, the sperm competition hypothesis predicts a positive association between the probability that the sperm will find themselves in competition with sperm from rival males and the number of sperm inseminated.
• 2 The beetle, Tenebrio molitor L., behaves in accordance with this hypothesis. Males accompanied by a rival male before and during mating inseminate more sperm per ejaculate than unaccompanied males. Accompanied males are also faster to initiate mating and more likely to show post-copulatory guarding. Adjustment of number of sperm inseminated was shown by males subjected to both long-term (5 days) and short-term (5 min) exposure to potential intrasexual competitors. Individual males exposed to both levels also demonstrated the ability to adjust their ejaculate according to socio-sexual situation.
• 3 We conclude that male T.molitor adjust the number of sperm they inseminate according to some perception of the risk of sperm competition.

     

Sperm competition within a dominance hierarchy: investment in social status vs. investment in ejaculates

There is increasing recognition that male-male competition can take many forms, but as yet the form is not predictable a priori. Many recent studies have focused attention on how males in disadvantaged mating roles compensate through sperm competition. However, mating systems in which subordinate males are reproductively suppressed, particularly through the stress of social interactions, may limit the ability of males to respond by increasing investment in sperm quality. We examined the interaction between social status and ejaculate tactics in Nauphoeta cinerea, a cockroach that has a mating system with well-characterized dominance hierarchies. Both social experience with other males and social status influenced aspects of ejaculates. The stress of social interactions reduced the size of the ejaculate and number of sperm inseminated. In ejaculates formed prior to social experience, however, males that go on to become dominant inseminated more sperm than males that go on to become subordinate, suggesting innate differences among males. Our results show that though selection for increased success in sperm competition for subordinate males in a hierarchy can occur, both the traits and the way in which the balance between pre- and post-copulatory strategies is negotiated will depend on specific details of the mating system. These details will include how the physiological effects of social interactions may limit selection through male-male competition.     

EXPERIMENTAL EVOLUTION OF SPERM QUALITY VIA POSTCOPULATORY SEXUAL SELECTION IN HOUSE MICE

Individuals of many species copulate with multiple mates (polygamy). Multiple mating by females (polyandry) promotes sperm competition, which has broad implications for the evolution of the ejaculate. Multigenerational studies of polygamous insects have shown that the removal of sexual selection has profound fitness consequences for females, and can lead to an evolutionary divergence in ejaculate traits. However, the evolutionary implications of polygamous mating across successive generations have not before been demonstrated in a vertebrate. By manipulating the mating system we were able to reinstate postcopulatory sexual selection in a house mouse population that had a long history of enforced monogamy. Following eight generations of selection, we performed sperm quality assays on males from both the polygamous and monogamous selection lines. We applied a principal component analysis to summarize the variation among 12 correlated sperm traits, and found that males evolving under sperm competition had significantly larger scores on the first axis of variation, reflecting greater numbers of epididymal sperm and increased sperm motility, compared to males from lines under relaxed selection. Moreover, we found a correlated response in the size of litters born to females in lines subject to sperm competition. Thus, we present significant evidence that sperm competition has profound fitness consequences for both male and female house mice.     

Current Sperm Competition Determines Sperm Allocation in a Tephritid Fruit Fly

Sperm competition (SC) occurs when the sperm of two or more males compete for the same set of ova. Theoretical models and experimental observations indicate that the presence of rival males causes focal males to adjust sperm allocation in a given copulation. Males allocate more sperm when they perceive the presence of one rival male (SC risk), either before or during mating, or when they perceive the presence of multiple rival males before mating (previous SC intensity). Conversely, males are expected to allocate fewer sperm when they perceive the presence of rival males during mating (current SC intensity). Here, we varied male perception of SC by manipulating the number of rival males, both before mating (from emergence to mating) and during mating (at the time of mating) to examine their effects on mating latency, copulation duration, and sperm allocation in the South American fruit fly Anastrepha fraterculus. We showed that exposure to rival males at the time of mating decreased mating latency. However, in contrast to the theory, exposure to multiple rivals at the time of mating increased sperm allocation. Female and male size were significant predictors of mating latency, copulation duration, and sperm allocation. Our results showed that there is a plastic response of males to the level of perceived SC through the number of rival males. Current levels of SC intensity are important in shaping male responses to SC, although the patterns in this species are opposite to predictions from the existing theory. We propose that female preference for males forming leks could explain lower sperm counts when encountering only one or two males.     

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.     

No Plastic Responses to Experimental Manipulation of Sperm Competition per se in a Free‐Living Flatworm

In the absence of sperm competition evolutionary theory predicts low mating rates and low ejaculate expenditure per mating, and sex allocation theory for simultaneous hermaphrodites predicts a strongly female‐biased sex allocation. In the presence of sperm competition a shift towards a more male‐biased sex allocation and a higher ejaculate expenditure are predicted. The free‐living flatworm Macrostomum lignano has been shown to respond plastically in mating rate, testis size, and sperm transfer to manipulation of the social group size, a proxy of the strength of sperm competition. However, manipulation of social group size may manipulate not only sperm competition, but also other factors, such as food supply and metabolite concentration. In this study we therefore manipulated sperm competition per se by repeatedly exposing individuals to partners that have either mated with rivals or not, while keeping the social group size constant. Our results suggest that M. lignano does not have the ability to detect sperm competition per se, as worms experimentally exposed to the presence or absence of sperm competition did not differ in sex allocation, sperm transfer or mating behavior. A response to our manipulation would have required individual recognition, the ability to detect self‐referencing tags, or tags or traces left by rivals on or in the mating partners. We first discuss the possibility that highly efficient sperm displacement may have decreased the difference between the treatment groups and then propose three alternative cues that may allow M. lignano to respond plastically to the social group size manipulation used in earlier studies: assessment of the mating rate, chemical cues, or tactile cues.     

Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners

In many animals in which females store sperm, males may detect female mating status and, in order to outcompete rival sperm, increase ejaculate size when copulating with non-virgin females. Although most studies have been restricted to organisms with separate sexes, theoretical models suggest that sperm competition should also be an important selective agent shaping life-history traits in simultaneous hermaphrodites. Nevertheless, the empirical support for ejaculate adjustment in a mating opportunity is scarce in hermaphrodites. In the present study, we performed a double-mating experiment to determine whether earthworms (Eisenia andrei) detect the mating status of their partners and whether they respond by adjusting their ejaculate. We found that earthworms triplicated the donated sperm when mating with a non-virgin mate. Moreover, such increases were greater when the worms were mated with larger (more fecund) partners, indicating that earthworms perform a fine-tune control of ejaculate volume. The results of the present study suggest that, under high intensity of sperm competition, partner evaluation is subject to intense selection in hermaphrodite animals, and donors are selective about to whom they donate how much sperm.     

Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis

Sperm competition theory predicts that under high risk of sperm competition, males will increase the number of sperm that they allocate to a female. This prediction has been supported by some experimental studies but not by others. Here, I conducted a meta-analysis to determine whether the increase in sperm allocation under high risk of sperm competition is a generalized response across taxa. I collected data from 39 studies and 37 species. Across taxa, males under a high risk of sperm competition respond by increasing their sperm allocation (mean effect size=0.32). Number of offspring did not explain a significant portion of the variation in effect sizes. A traditional meta-analysis (i.e. without phylogenetic information) described the variation among effect sizes better than a meta-analysis that incorporates the phylogenetic relationships among species, suggesting that the increase in sperm allocation under high risk of sperm competition is similarly prevalent across taxa.