Spermicide by females: what should males do?

The female reproductive tract can be particularly aggressive towards ejaculates, often leading to the death of large numbers of sperm. It has been suggested that males can respond to these actions by investing more in sperm and donating larger ejaculates. Such counteractions may lead to arms races, which can have significant implications for the mating system. In a series of simple models we first show that arms races are not necessarily supported: in fact, sperm killing may even favour no change or reductions in sperm allocation. Second, we identify a simple mechanistic rule for sperm killing that determines whether an arms race or sperm reduction will be favoured. Which of these responses is favoured by selection depends on whether a certain number, or proportion, of sperm are killed. When a specific number is killed, larger investment in sperm is favoured and when a specific proportion is killed, no change or lower investment in sperm is favoured. Both of these mechanisms are biologically plausible.     

Flow cytometric sexing of spider sperm reveals an equal sperm production ratio in a female-biased species

Producing equal amounts of male and female offspring has long been considered an evolutionarily stable strategy. Nevertheless, exceptions to this general rule (i.e. male and female biases) are documented in many taxa, making sex allocation an important domain in current evolutionary biology research. Pinpointing the underlying mechanism of sex ratio bias is challenging owing to the multitude of potential sex ratio-biasing factors. In the dwarf spider, Oedothorax gibbosus, infection with the bacterial endosymbiont Wolbachia results in a female bias. However, pedigree analysis reveals that other factors influence sex ratio variation. In this paper, we investigate whether this additional variation can be explained by the unequal production of male- and female-determining sperm cells during sperm production. Using flow cytometry, we show that males produce equal amounts of male- and female-determining sperm cells; thus bias in sperm production does not contribute to the sex ratio bias observed in this species. This demonstrates that other factors such as parental genes suppressing endosymbiont effects and cryptic female choice might play a role in sex allocation in this species.     

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.     

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.     

A state-based model of sperm allocation in a group-breeding salamander

We developed a dynamic program of optimal sperm allocation for group-breeding species. Using the small-mouthed salamander,Ambystoma texanum, as a model organism, we considered how spermatophoredeposition is affected by sperm reserves, male and female numberin breeding aggregations, and time during the breeding season.Parameters for part of the model were based on field data ofbreeding-pond arrival times for both sexes and on laboratoryspermatophore deposition data. Our model included simulationsof three different seasonal patterns of female arrival rate: decreasing (as in A. texanum), increasing, and uniform. General predictions are (1) Increased male competitor numbers at breedingaggregations should cause a reduction in spermatophore allocation.(2) Increased female numbers at breeding aggregations shouldincrease spermatophore allocation. (3) The effect of currentsperm reserve levels on sperm allocation depends on the seasonaldistribution of the mean number of females per male during the breeding season: (3a) If relative female availability decreasesover time, males with low sperm reserves should limit allocationearly in the season but should deposit maximal sperm loadslate in the season; (3b) if female availability increases overtime, males with low sperm loads should limit allocation throughoutthe entire breeding season; and (3c) if female availabilityis constant, sperm reserves are predicted to have little effect on spermatophore allocation tactics. We discuss model predictionsin the context of current sperm allocation theory.     

Sperm as a paternal investment: a model of sex allocation in sperm-digesting hermaphrodites

Some simultaneously hermaphroditic animals are known to digest received sperm. To investigate the effect of sperm digestion on the sex allocation of simultaneous hermaphrodites, we constructed models about evolutionarily stable resource allocation between male and female functions. We assumed that resource obtained from sperm digestion is used for gametogenesis (sperm and/or egg production). As a result, we found that sperm digestion increases the evolutionarily stable allocation to male function under finite number of matings. This is because excess sperm function as nuptial gift or paternal investment when at least a fraction of digested sperm is translated into eggs. Therefore, some factors which affect the assurance of paternity for sperm donors, such as cryptic female choice and/or sperm displacement, may change the result. In addition, this result implies that sperm digestion does not necessarily make male role less preferred. Further studies on the usage of donated sperm are required to test the validity of our models.     

Cryptic male choice: sperm allocation strategies when female quality varies

We examined evolutionary stable sperm allocation and included stochastic variation in male mating frequency, not included in previous models examining sperm allocation strategies. We assumed sperm mixing and variation in female quality and used a genetic algorithm to analyse the evolution of male sperm allocation. Our results show that males should invest more sperm in initial copulations than in subsequent copulations as a male might fail to mate again. The inclusion of variation in female fecundity had no influence on the evolutionary stable sperm allocation strategy if males were unable to recognize female quality. If males were assumed to allocate sperm in response to female quality, the proportion of sperm allocated was positively correlated with female quality. Moreover, with increasing variance in female quality, males conserved more sperm for later copulations. Literature data on sperm allocation from diverse taxa show a good fit with the predictions given by our model.     

The evolution of sperm-allocation strategies and the degree of sperm competition

The prevailing viewpoint in the study of sperm competition is that male sperm-allocation strategies evolve in response to the degree of sperm competition an ejaculate can expect to experience within a given mating. If males cannot assess the degree of sperm competition their ejaculate will face and/or they are unable to facultatively adjust sperm investment in response to perceived levels of competition, high sperm allocation (per mating) is predicted to evolve in the context of high sperm competition. An implicit assumption of the framework used to derive this result is that the degree of sperm competition is unaffected by changes in sperm-allocation strategies. We present theory based on an alternative perspective, in which the degree of sperm competition and the sperm-allocation strategy are coupled traits that coevolve together. Our rationale is that the pattern of sperm allocation in the population will, in part, determine the level of sperm competition by affecting the number of ejaculates per female in the population. In this setting, evolution in sperm-allocation strategies is driven by changes in underlying environmental parameters that influence both the degree of sperm competition and sperm allocation. This change in perspective leads to predictions that are qualitatively different from those of previous theory.     

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.     

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.     

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.     

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.     

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.     

Male reproductive strategy in Trichogramma evanescens: sperm production and allocation to females

Abstract.  The production and allocation of sperm among successive mates during a male's life largely determine its fitness. The sperm production pattern and sperm allocation to females is studied in Trichogramma evanescens , a short-lived egg parasitoid of several lepidopteran species. At emergence, virgin males have an average of 1607 ± 249 sperm stored in the seminal vesicles and no further production occurs during adult life. These males are able to mate with at least 20 females in rapid succession. During the first 10 matings, the males transfer approximately 100 sperm each time and then transfer fewer and fewer sperm per mating. The number of sperm stored in spermathecae of successively mated females remains relatively constant for the first 10 females, and decreases slowly for the subsequent females. The relationship between male reproductive strategy and some life-history traits are discussed.     

Modeling strategic sperm allocation: Tailoring the predictions to the species

Two major challenges exist when empirically testing the predictions of sperm allocation theory. First, the study species must adhere to the assumptions of the model being tested. Unfortunately, the common assumption of sperm allocation models that females mate a maximum of once or twice does not hold for many, if not most, multiply and sequentially mating animals. Second, a model's parameters, which dictate its predictions, must be measured in the study species. Common examples of such parameters, female mating frequency and sperm precedence patterns, are unknown for many species used in empirical tests. Here, we present a broadly applicable model, appropriate for multiply, sequentially mating animals, and test it in three species for which data on all the relevant parameter values are available. The model predicts that relative allocation to virgin females, compared to nonvirgins, depends on the interaction between female mating rate and the sperm precedence pattern: relative allocation to virgins increases with female mating rate under first‐male precedence, while the opposite is true under later‐male precedence. Our model is moderately successful in predicting actual allocation patterns in the three species, including a cricket in which we measured the parameter values and performed an empirical test of allocation.     

Social status and availability of females determine patterns of sperm allocation in the fowl

Where sperm competition occurs, the number and quality of sperm males inseminate relative to rival males influences fertilization success. The number of sperm males produce, however, is limited, and theoretically males should allocate sperm according to the probability of gaining future reproductive opportunities and the reproductive benefits associated with copulations. However, the reproductive opportunities and value of copulations males obtain can change over their lifetime, but whether individuals respond to such changes by adjusting the way they allocate sperm is unclear. Here we show that, in the fowl, Gallus gallus, dominant males, which have preferential access to females, modulate the number of sperm they ejaculate according to the availability of females. When presented with two females, dominant males allocated more sperm to higher quality females, whereas when females were on their own, only copulation order had an affect on their sperm numbers. In contrast, subordinate males, whose mating activity is restricted by dominant males, allocated high numbers of sperm to initial copulations, irrespective of female availability. We further show, by manipulating male social status, that sperm allocation is both phenotypically plastic, with males adjusting their patterns of sperm allocation according to their dominance rank, and intrinsic, with males being consistently different in the way they allocate sperm, once the effects of social status are taken into account. This study suggests that males have evolved sophisticated patterns of sperm allocation to respond to frequent fluctuations in the value and frequency of reproductive opportunities.     

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.     

Strategic sperm allocation under parasitic sex-ratio distortion

Parasitic sex-ratio distorters are a major selective force in the evolution of host mating behaviour and mate choice. Here, we investigate sperm limitation in the amphipod Gammarus duebeni and the impact of the microsporidian sex-ratio distorter Nosema granulosis on sperm allocation strategies. We show that males become sperm limited after three consecutive matings and provide uninfected, high fecundity, females with more sperm than infected females. We show that sperm limitation leads to a decrease in female productivity. The outcome of sex-ratio distortion has been shown theoretically to be sensitive to the mating limits of males. Our results indicate that strategic sperm allocation under male rarity will have a greater impact on infected females and has the potential to regulate spread of parasitic feminisers in host populations.     

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.     

INTRASPECIFIC VARIATION IN SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE: THE EFFECT OF INDIVIDUAL SIZE

Within a population of simultaneous hermaphrodites, individuals may vary in both their current reproductive investment (biomass invested in gonads) and in how they allocate that investment between male and female function. In the chalk bass, Serranus tortugarum, estimates of both reproductive allocation and reproductive success as a male and a female can be made for individuals of different sizes. As individuals increase in size, their investment in gamete production increases, and there is a shift in allocation to a stronger female bias. Spawning frequency as a female in pair spawnings and as a male in both pair spawning and streaking (an alternative mating tactic) does not vary with individual size. As a result, larger individuals should release more sperm or eggs per spawn. Size-assortative pair spawning in this species leads to larger individuals having higher potential returns in total male reproductive success than smaller individuals, which should lead to increases in absolute levels of sperm production in larger individuals when individuals compete for fertilizations through sperm competition. However, smaller individuals contribute a smaller proportion of the sperm released in spawns with multiple spawners and thus are under more intense sperm competition than larger individuals, which should select for increases in male allocation in smaller individuals, all else equal. A local-mate-competition (LMC) model predicts that these factors select for increasing absolute male and female investment with individual size but a relative shift to more female-biased allocation as individual size increases. These predictions are supported by gonadal data. The predictions of average male allocation from the quantitative LMC model were 21.6% and 25.7%, whereas the collections averaged 21.3%. This close agreement of both the mean male allocation and its relative shift with individual size between model and data support the hypothesis that size-specific shifts in sex allocation in this species represent an adaptive response to patterns of mating success and sperm competition.