Sneaker “jack” males outcompete dominant “hooknose” males under sperm competition in Chinook salmon (Oncorhynchus tshawytscha)

In a variety of taxa, males deploy alternative reproductive tactics to secure fertilizations. In many species, small “sneaker” males attempt to steal fertilizations while avoiding encounters with larger, more aggressive, dominant males. Sneaker males usually face a number of disadvantages, including reduced access to females and the higher likelihood that upon ejaculation, their sperm face competition from other males. Nevertheless, sneaker males represent an evolutionarily stable strategy under a wide range of conditions. Game theory suggests that sneaker males compensate for these disadvantages by investing disproportionately in spermatogenesis, by producing more sperm per unit body mass (the “fair raffle”) and/or by producing higher quality sperm (the “loaded raffle”). Here, we test these models by competing sperm from sneaker “jack” males against sperm from dominant “hooknose” males in Chinook salmon. Using two complementary approaches, we reject the fair raffle in favor of the loaded raffle and estimate that jack males were ~1.35 times as likely as hooknose males to fertilize eggs under controlled competitive conditions. Interestingly, the direction and magnitude of this skew in paternity shifted according to individual female egg donors, suggesting cryptic female choice could moderate the outcomes of sperm competition in this externally fertilizing species.     

Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism.

The outcome of sperm competition in species with alternative male reproductive strategies may be determined by fair or loaded raffle mechanisms. The sperm production and quality of male Atlantic salmon using alternative reproductive tactics were investigated in order to determine the relative importance of sperm quality for male reproductive success. Sexually mature resident parr males produced greater numbers of spermatozoa per millilitre of ejaculate and invested more in their gonads as a percentage of body mass than their anadromous counterparts. Parr males had greater proportions of motile spermatozoa and a greater sperm ATP content as compared with anadromous males. Parr males invested relatively more in sperm quality and sperm numbers after the effect of body size was accounted for. In fertilization experiments, parr males fertilized greater proportions of eggs than anadromous males. A polynomial model exhibited a trade-off between testes mass and ejaculate expenditure and explained 60% of the variation. These results establish that, in sperm competition with dominant males, parr males may compensate for behavioural subordinance by producing physiologically superior spermatozoa.     

Sperm competition games: a comparison of loaded raffle models and their biological implications

Our main aim is to compare the additive model, due to Mesterton-Gibbons, and the multiplicative model, due to Parker, of sperm allocation under sperm competition, when other influences are treated in the same way. We first review these (and other) models and their foundations, leading to a generalization of the multiplicative model. Sperm is assumed to cost energy, and this constraint is incorporated differently in the two models. These give the same results in the random-roles situation when the males occupy roles (of first and second to mate) randomly: the number of sperm ejaculated in the favoured role is greater than that in the disfavoured role by an amount that depends on the effect of sperm limitation (i.e. the probability that there is insufficient sperm to ensure full fertility). If the latter is negligible, or the fertilization raffle fair, this difference is zero, as Parker found originally. In the constant roles situation (where males of a particular type always occupy the same role) the predictions differ: the additive model has the same predictions as in the random roles case, but the multiplicative model predicts that males of the type occupying the favoured role ejaculate less than males of the type occupying the disfavoured role, in accord with Parker's original conclusion. The fitnesses of the two types of male can be calculated in the multiplicative model: the fitness of the favoured male is usually higher, even if he has to expend more energy in "finding" a female, e.g. through fighting, etc. These conclusions relate to inter-male behaviour (i.e. of different male types), as distinct from intra-male behaviour (i.e. of a given male when in different roles). We analyse situations in which one male type has some probability of acting in its less usual role: calculations with varying amounts of sperm limitation are presented. It is found that the presence of a male of a different type has an effect on intra-male ejaculate behaviour, which also depends critically on the role usually occupied. We conclude that the multiplicative model is the more accurate model and provides more information. Some experimental data on sperm numbers are used to find the effects of sperm limitation. For species which conform to the loaded raffle model, sperm limitation typically has small or negligible effects: in this case, we argue that empiricists should look for equal ejaculates in the two roles when studying random role situations; when roles are occupied non-randomly average sperm expenditure should be greater by male types typically occupying the disfavoured role, but within a male type, expenditure should be greater in the role it typically occupies.     

Sperm competition games between related males

Three sperm competition games against relatives are examined. In the first, a male has no information at the time of mating as to whether or not his ejaculate will face sperm competition from a related or unrelated male. Sperm expenditure increases with overall sperm competition risk q and declines with the probability rho that the competitor shares the same allele for sperm expenditure. In the second game, males have almost perfect information: they 'know' whether there will be sperm competition and, if so, whether this involves a related or unrelated male. Sperm expenditure is reduced by a factor rho when competing with a relative. In the third game, males 'know' when they compete with relatives, but have no information for other matings whether they will face sperm competition from unrelated males. A male without information expends less on his ejaculate than a male competing with a close relative if the overall risk of sperm competition is low, but more if the overall risk is high. The average relative ejaculate expenditure is the same in all three games so that, if this determines testis size, data is required only on the overall sperm competition risk, the probability of competing with a relative and the average rho in order to perform comparative analyses.     

Sperm storage and copulation duration in a sexually cannibalistic spider

Female St Andrew’s Cross spiders control copulation duration by timing sexual cannibalism and may thereby control paternity if cannibalism affects sperm transfer. We have investigated the effect of copulation duration on sperm transfer and documented sperm storage patterns when we experimentally reduced the ability of females to attack and cannibalise the male. Virgin males and females were paired and randomly allocated either to a control treatment, where females were allowed to attack and cannibalise the male during copulation, or to an experimental treatment, where females were unable to cannibalise the male. The latter was achieved by placing a paintbrush against her chelicerae during copulation. Our experimental manipulation did not affect copulation duration or sperm storage. However, the number of sperm stored by the female increased with copulation duration only if the male was cannibalised, suggesting that cannibalism increases relative paternity not only through prolonged copulation duration following a fair raffle model but also through the cannibalism act itself. Future studies should explore whether cannibalised males ejaculate more sperm or whether females selectively store the sperm of cannibalised males.     

Sperm transfer and paternity in the scorpionfly <Emphasis Type="Italic">Panorpa cognata</Emphasis>: large variance in traits favoured by post-copulatory episodes of sexual selection

Post-copulatory episodes of sexual selection can be a powerful selective force influencing the reproductive success of males. In order to understand variation in male fertilisation success, we first need to consider the pattern of sperm utilisation by females following matings with more than one male. Second, we need to study those traits responsible for male success in sperm competition. Here we study both male sperm transfer characteristics as well as offspring paternity of females mated to two males in the scorpionfly Panorpa cognata. By repeatedly mating males to virgin females and interrupting copulation at defined time points, we found for all males that sperm transfer set off after approximately 40 min. During the remaining copulation, sperm transfer of individual males was continuous and with constant rate. Yet the rate of sperm transfer differed between individual males from about one sperm per minute to more than eight sperm per minute for the most successful males. In addition, we measured the fertilisation success in sperm competition of males with known sperm transfer capability. The relative number of sperm transferred by males during copulation, estimated from copulation duration and the males’ individual sperm transfer rate, explained a large proportion of variation in offspring paternity. The mode of sperm competition in this species, thus, conforms largely to a fair raffle following complete mixing of sperm prior to fertilisation. Hence, male differences in both the ability to copulate for long and of rapid sperm transfer will translate directly into differences in reproductive success.     

SPERM COMPETITION GAMES: A GENERAL MODEL FOR PRECOPULATORY MALE–MALE COMPETITION

Reproductive males face a trade‐off between expenditure on precopulatory male–male competition—increasing the number of females that they secure as mates—and sperm competition—increasing their fertilization success with those females. Previous sperm allocation models have focused on scramble competition in which males compete by searching for mates and the number of matings rises linearly with precopulatory expenditure. However, recent studies have emphasized contest competition involving precopulatory expenditure on armaments, where winning contests may be highly dependent on marginal increases in relative armament level. Here, we develop a general model of sperm allocation that allows us to examine the effect of all forms of precopulatory competition on sperm allocation patterns. The model predicts that sperm allocation decreases if either the “mate‐competition loading,”a, or the number of males competing for each mating, M, increases. Other predictions remain unchanged from previous models: (i) expenditure per ejaculate should increase and then decrease, and (ii) total postcopulatory expenditure should increase, as the level of sperm competition increases. A negative correlation between a and M is biologically plausible, and may buffer deviations from the previous models. There is some support for our predictions from comparative analyses across dung beetle species and frog populations.     

Paternity analysis of wild‐caught females shows that sperm package size and placement influence fertilization success in the bushcricket Pholidoptera griseoaptera

In species where females store sperm, males may try to influence paternity by the strategic placement of sperm within the female's sperm storage organ. Sperm may be mixed or layered in storage organs, and this can influence sperm use beyond a ‘fair raffle’. In some insects, sperm from different matings is packaged into discrete packets (spermatodoses), which retain their integrity in the female's sperm storage organ (spermatheca), but little is known about how these may influence patterns of sperm use under natural mating conditions in wild populations. We examined the effect of the size and position of spermatodoses within the spermatheca and number of competing ejaculates on sperm use in female dark bushcrickets (Pholidoptera griseoaptera) that had mated under unmanipulated field conditions. Females were collected near the end of the mating season, and seven hypervariable microsatellite loci were used to assign paternity of eggs laid in the laboratory. Females contained a median of three spermatodoses (range 1–6), and only six of the 36 females contained more than one spermatodose of the same genotype. Both the size and relative placement of the spermatodoses within the spermatheca had a significant effect on paternity, with a bias against smaller spermatodoses and those further from the single entrance/exit of the spermatheca. A higher number of competing males reduced the chances of siring offspring for each male. Hence, both spermatodose size and relative placement in the spermatheca influence paternity success.     

Male meadow voles respond differently to risk and intensity of sperm competition

There are 2 models of male adjustment of sperm investment inthe ejaculate in relation to sperm competition. The "risk model"predicts that as "risk" of sperm competition increases, sperminvestment also increases. This prediction has been supportedin many species, including mammals. The "intensity model" involvesthe number of competing males copulating with the same femaleand predicts that males will allocate the highest sperm investmentat low sperm competition intensity (SCI) and then decreasingsperm investments as SCI increases. Two alternative outcomesare that sperm investment is unaffected by SCI and that sperminvestment increases as SCI increases. There are studies supportingall 3 possible outcomes in relation to SCI but no data on mammals.The present paper presents the first study of SCI in a mammalspecies, the meadow vole, Microtus pennsylvanicus. We used odorsof conspecific males to simulate low and high intensities ofsperm competition. We found that males allocate the highestsperm investment at low SCI and decrease significantly theirsperm investment at high SCI. We also found that males allocatethe lowest sperm investment at low sperm competition risk (SCR)and the highest sperm investment at high SCR. All these resultsagree with current theoretical models of sperm competition.     

Sperm competition games: optimal sperm allocation in response to the size of competing ejaculates

Sperm competition theory predicts that when males are certain of sperm competition, they should decrease sperm investment in matings with an increasing number of competing ejaculates. How males should allocate sperm when competing with differently sized ejaculates, however, has not yet been examined. Here, we report the outcomes of two models assuming variation in males' sperm reserves and males being faced with different amounts of competing sperm. In the first 'spawning model', two males compete instantaneously and both are able to assess the sperm competitive ability of each other. In the second 'sperm storage model', males are sequentially confronted with situations involving different levels of sperm competition, for instance different amounts of sperm already stored by the female mating partner. In both of the models, we found that optimal sperm allocation will strongly depend on the size of the male's sperm reserve. Males should always invest maximally in competition with other males that are equally strong competitors. That is, for males with small sperm reserves, our model predicts a negative correlation between sperm allocation and sperm competition intensity, whereas for males with large sperm reserves, this correlation is predicted to be positive.     

INDIVIDUAL VARIATION IN SPERM COMPETITION SUCCESS OF YELLOW DUNG FLIES,SCATOPHAGA STERCORARIA

Intraspecific variation in the proportion of offspring sired by the second male to mate with a female (P₂) is an aspect of sperm competition that has received little attention. We examined variation in the sperm competition success of individual male dung flies, Scatophaga stercoraria. In unmanipulated matings, copula duration was dependent on male size with smaller males copulating for longer. A principal component analysis was used to generate uncorrelated scores based on a male's size and copula duration. Using these scores demonstrated that P₂ values were dependent both on the relative size and copula durations of competing males. When copula duration was held constant, the success of an individual male increased as his body size, relative to the first male, increased. We interrupted copulations of “large” and “small” second males and fitted the resultant P₂ values to a linear model of sperm competition with unequal ejaculates. The data fit well to a model of sperm displacement in which sperm mix quickly on introduction to the sperm stores. Furthermore, they show that “large” males have a greater rate of sperm displacement than “small” males. The levels of prey availability during testis maturation may influence a male's success in sperm competition although his immediate mating history does not. We show why an understanding of variation in sperm competition success is important for understanding the mechanisms and evolutionary significance of sperm competition.     

Soay rams target reproductive activity towards promiscuous females' optimal insemination period

Female promiscuity is thought to have resulted in the evolution of male behaviours that confer advantages in the sperm competition that ensues. In mammalian species, males can gain a post-copulatory advantage in this sperm 'raffle' by inseminating females at the optimal time relative to ovulation, leading to the prediction that males should preferentially associate and copulate with females at these times. To the best of our knowledge, we provide the first high-resolution test of this prediction using feral Soay sheep, which have a mating system characterized by male competition for access to highly promiscuous females. We find that competitive males time their mate guarding (and hence copulations) to occur close to the optimal insemination period (OIP), when females are also increasingly likely to 'cooperate' with copulation attempts. Subordinate males practice an alternative mating tactic, where they break the integrity of the consort pair and force copulations on females. The timing of these forced copulations is also targeted towards the OIP. We thus provide quantitative evidence that female promiscuity has resulted in the evolution of reproductive strategies in which males 'load' the sperm raffle by targeting their mating activity towards female OIPs, when the probability of sperm-competition success is at its greatest.     

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.     

Sperm competition games played by dimorphic male beetles: fertilization gains with equal mating access

Alternative mating tactics can generate asymmetry in the sperm competition risk between males within species. Theory predicts that adaptations to sperm competition should arise in males facing the greater risk. This prediction is met in the dung beetle Onthophagus binodis where minor males which sneak copulations have a greater expenditure on the ejaculate. In its congener Onthophagus taurus there is a reduced asymmetry in sperm competition risk such that both tactics have equal ejaculate expenditure. We used the irradiated male technique to test whether adaptations to sperm competition in minor males result in higher paternity. We found that for both species, on average, each of two males gained equal numbers of fertilizations, confirming the assumption that sperm compete in a raffle. There were no differences in the sperm competition success of major and minor males in O. taurus as predicted from their equal expenditure on their ejaculate. Contrary to expectations, there were also no differences in fertilization success between the male tactics in O. binodis. Thus, in O. binodis minor males must expend more on their ejaculate in order to obtain the same fertilization gains as major males.     

On sperm competition games: raffles and roles revisited

 In principle there are two approaches to modelling a trade-off between the positive and negative outcomes of a behavior: after suitably defining a value for the behavior in the absence of any trade-off, one can either multiply that value by an appropriate discount or subtract an appropriate cost. In a prospective analysis of sperm competition, Parker (Proc. Roy. Soc. Lond. B (1990) 242, 120–126) adopted the multiplicative approach to model the trade-off between the value of a mating and the cost of its acquisition. He obtained two paradoxical results. First, if two males ‘know’ whether they are first or second to mate, but these roles are assigned randomly, then sperm numbers should be the same for both males whether the ‘raffle’ for fertilization is fair or unfair. Second, if mating order is constant, then a favored male should expend less on sperm. His results are puzzling not only in terms of intuition about nature, but also in terms of his model’s consistency. In other words, they present both an external and an internal paradox. Parker assumed the fairness of the raffle to a disfavored male to be independent of how much sperm a favored male deposits. This article both generalizes Parker’s analysis by allowing fairness to decrease with sperm expenditure by the favored male and compares Parker’s results to those obtained by the additive approach. In many respects, results are similar. Nevertheless, if the costs of mating are assumed to increase with sperm expenditure but not to depend on the role in which sperm is expended, as Parker assumed, then the additive approach is more fundamentally correct. In particular, Parker’s constant-role paradox is an artifact of his approach. His random-role paradox is internally rationalized in terms of standard microeconomic theory. When fairness decreases, however slightly, with sperm expenditure by the favored male, both models demonstrate that the evolutionarily stable strategy is for more sperm to be deposited during a favored mating than during a disfavored mating. The lower the costs, the greater the divergence. Thus a possible resolution of the external paradox is that fairness is not constant in nature. Received: 7 December 1998     

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 selection and genetic incompatibility: does relatedness of mates affect male success in sperm competition?

Sperm selection may be said to occur if females influence the relative success of ejaculates competing to fertilize their ova. Most evidence that female animals or their ova are capable of sperm selection relates to male genetic incompatibility, although relatively few studies focus on competition between conspecific males. Here I look for evidence of sperm selection with respect to relatedness of mates. Reduced fitness or inbreeding effects in offspring resulting from copulations between close relatives are well documented. If females are capable of sperm selection, they might therefore be expected to discriminate against the sperm of sibling males during sperm competition. I describe an experimental protocol designed to test for evidence of sperm selection while controlling for inbreeding effects. Using decorated field crickets (Gryllodes supplicans), I found that sibling males achieved lower fertilization success in competition with a male unrelated to the female than in competition with another sibling more frequently than expected by chance, although the mean paternity values did not differ significantly between treatments. The tendancy for sibling males to achieve relatively lower fertilization success in competition with males unrelated to the female could not be explained by the effects of increased ejaculate allocation, female control of sperm transfer or inbreeding. This study therefore provides some evidence in support of the idea that female insects (or their ova) may be capable of selection against sperm on the basis of genetic similarity of conspecific males.     

On sperm competition games: incomplete fertilization risk and the equity paradox

Evolutionary game theory has been used to predict the effect on sperm expenditure of a trade-off between the value of a mating and the cost of its acquisition. In particular, G. A. Parker has predicted that if two males ''know'' whether they are first or second to mate, but these roles are assigned randomly, then sperm numbers should be the same for both males whether the ''raffle'' for fertilization is fair or unfair. This prediction relies on the assumption that, in the absence of sperm competition, ejaculates would always contain enough sperm to ensure complete fertilization after mating. The slightest risk of incomplete fertilization, however, is enough to ensure that favoured males expend more than disfavoured males in the presence of sperm competition, unless the competition is perfectly fair. Divergence of expenditures increases with unfairness until unfairness reaches a critical value, beyond which a disfavoured male should no longer compete. The higher the fertilization risk, the lower the critical unfairness. All predictions are independent of the probability of mating first or second. Implications are discussed for the mechanisms that underlie sperm competition.     

Sperm competition affects male behaviour and sperm output in the rainbow darter

Rainbow darters, Etheostoma caeruleum, are promiscuous fish with moderate rates of group spawning (between one and five males may simultaneously mate with one female). In this study, I examined male sperm output and male willingness to spawn under different levels of sperm competition intensity. One male and one female were allowed to spawn in an aquarium where they had visual and olfactory access to one of four treatments: four males, one male, zero males, or one female. Theory predicts that males should reduce sperm output when there are more than the average number of males at a group spawning (four-male treatment) and should increase sperm output when there are fewer than average males at a group spawning (one-male treatment). Mean sperm output did not differ among treatments. However, males released more sperm when spawning in the presence of competing males (four-male and one-male treatments pooled) than when spawning in the absence of competing males (zero-male and one-female treatments pooled). Males were also most likely to forego spawning opportunities when sperm competition intensity was high. Furthermore, male willingness to spawn was size dependent. Large males were more likely to forego spawning opportunities under high sperm competition intensity. Large males may be better off waiting for future spawning opportunities when there is a lower potential for sperm competition intensity.     

Conditions for the evolution of soldier sperm classes

Abstract.— There has been wide disagreement as to whether sperm competition among animals can produce a soldier class of sperm to fight against other males. Utilizing mathematical models, we analyze the appropriate conditions for the evolution and maintenance of a soldier sperm class. We conclude that: (1) soldier sperm evolve even if one soldier sperm can kill or block less than one competing sperm; (2) soldier sperm evolve faster when there is a large variance in the number of competing sperm; (3) soldier ratio increases until reproductive sperm are too scarce to fertilize all ova or a sperm intensely refuses to become a soldier; and (4) soldier sperm are more likely to be smaller than reproductive sperm. Our models suggest that the conditions for the evolution of a soldier sperm class are not stringent.