Strategic Sperm Allocation Research Articles

Female novelty and male status dynamically modulate ejaculate expenditure and seminal fluid proteome over successive matings in red junglefowl

Theory predicts that males will strategically invest in ejaculates according to the value of mating opportunities. While strategic sperm allocation has been studied extensively, little is known about concomitant changes in seminal fluid (SF) and its molecular composition, despite increasing evidence that SF proteins (SFPs) are fundamental in fertility and sperm competition. Here, we show that in male red junglefowl, Gallus gallus, along with changes in sperm numbers and SF investment, SF composition changed dynamically over successive matings with a first female, immediately followed by mating with a second, sexually novel female. The SF proteome exhibited a pattern of both protein depletion and enrichment over successive matings, including progressive increases in immunity and plasma proteins. Ejaculates allocated to the second female had distinct proteomic profiles, where depletion of many SFPs was compensated by increased investment in others. This response was partly modulated by male social status: when mating with the second, novel female, subdominants (but not dominants) preferentially invested in SFPs associated with sperm composition, which may reflect status-specific differences in mating rates, sperm maturation and sperm competition. Global proteomic SF analysis thus reveals that successive matings trigger rapid, dynamic SFP changes driven by a combination of depletion and strategic allocation.

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.

Strategic sperm allocation in response to perceived sperm competition risk in a lekking insect

Sperm competition has been demonstrated to be a strong selective force shaping male mating behaviours and ejaculate traits, particularly in highly polyandrous species. Its effect, however, is expected to be limited in lek mating systems, where female mating decisions appear relatively unconstrained and thus female remating rate is generally low. Hence, testing for male adaptations to sperm competition in lek mating species is of particular importance in order to understand whether and how sperm competition, as a selective force, may also have shaped male phenotype in such systems. Here, we investigated copulation behaviour and strategic sperm allocation in the lekking lesser wax moth, Achroia grisella, a well-established model for studying precopulatory sexual selection as males produce elaborate ultrasonic courtship songs targeted by female choice. Recent evidence suggests that females do sometimes remate, thus creating a selective potential for sperm competition. To test the hypothesis that sperm competition also selects for male adaptations in ejaculate traits in lek mating systems, we staged experimental matings after males had experienced either a competitive (one competitor present) or a noncompetitive (no competitor present) social environment during early adulthood. Males increased sperm transfer rate and thereby allocated higher proportions of available sperm reserves during virgin copulations when experiencing the elevated sperm competition risk environment. Our study provides the first evidence of strategic sperm allocation in relation to sperm competition risk in a lekking insect, demonstrating that sperm competition might represent an important selective force in such mating systems.

Sequential male mate choice under sperm competition risk.

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.

Strategic sperm allocation and a Coolidge effect in an externally fertilizing species

Because sperm is costly and limiting, males are predicted to allocate sperm differentially across matings, according to the level of sperm competition, female reproductive quality, and female novelty. We investigated sperm allocation in the European bitterling (Rhodeus amarus), an externally fertilizing species of fish that spawns and incubates its eggs in the gills of freshwater mussels. We predicted that males would allocate sperm differentially according to the quality and novelty of mussels. Dominant males responded to rivals by increasing both sperm investment and aggression, whereas subordinates responded chiefly through sperm investment. Dominant males invested more sperm in novel mussels in accordance with predictions for a Coolidge effect, the mussel representing a new fertilization opportunity. However, subordinate males were not influenced by mussel novelty but were responsive to order of mating. Males did not allocate sperm according to mussel quality, suggesting that certainty of paternity is a more important variable than offspring survival in shaping bitterling sperm allocation strategies. This study demonstrates strategic ejaculate expenditure in an externally fertilizing species, analogous to that in internal fertilizers, but with sperm investment operating on the level of the site of fertilization rather than the female. Key wor ds: ejaculate, mate choice, mating system, mussel, oviposition, sexual selection, sperm depletion. [Behav Ecol]

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.

Level of sperm competition promotes evolution of male ejaculate allocation patterns in a moth

The risk and intensity of sperm competition can influence male adaptations that ultimately affect male fertilization success, for example investment in sperm production and strategic sperm allocation patterns. Previous studies have examined male behavioural responses to variation in immediate levels of sperm competition. Here we quantified the evolutionary responses of male adaptations resulting from long-term manipulation of the level of sperm competition. By varying the adult sex ratio of populations of the Indian meal moth, Plodia interpunctella, we successfully altered the frequency of male and female copulations, and thus the level of sperm competition experienced by males. As predicted by theory, males evolving under higher levels of sperm competition increased investment in sperm production and differed in their sperm allocation patterns across matings, compared to males evolving under intermediate and low levels of sperm competition. However, we found no evidence for trade-offs between ejaculate components, or between total sperm production and male body size in this species.

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.

Reversed Sexual Conflict in a Promiscuous Antelope

A general tenet of sexual conflict theory is that males have higher optimum mating rates than do females and therefore should be more persistent when it comes to mating. However, in promiscuous species, females might benefit from high mating rates as a result of increased conception probability with favored males, whereas favored males benefit from mating selectively because of sperm depletion. When this results in higher optimum mating rates for females than for males, there is potential for reversed sexual conflicts between persistent females and resistant males. Here I report evidence of such a reversed sexual conflict in a promiscuous antelope, the African topi. Rather than mating randomly, favored males prefer to balance mating investment equally between females as predicted by strategic sperm allocation theory. Females, however, enhance their probability of mating with favored males through aggression toward mating pairs. Supporting the idea that aggressive females thereby harass males to mate at a rate that is suboptimal from the males' perspective, males become increasingly likely to counterattack aggressive females with whom they have already mated disproportionately, and such male counterattacks are associated with refusal to mate with the aggressive females. This study points to reversed sexual conflict as a more significant evolutionary force in promiscuous mammals than previously thought; however, such conflicts probably often go unnoticed because males, in contrast to females, can avoid mating without conspicuous resistance.

No evidence for strategic male mating effort in response to female weight in a bushcricket

AbstractTheoretical models predict that males should allocate sperm in response to female quality and empirical studies have shown that fecundity traits including age, mass and mating status can influence male sperm allocation strategies. We tested whether female size has an influence on sperm allocation in the bushcricket Poecilimon jonicus jonicus (Orthoptera: Phaneropterinae). Contrary to other studies, we found neither evidence of strategic sperm allocation in response to female size nor an effect of female size on spermatophore size. Male age and mating history was positively related to sperm number during sequential matings, but had no effect on spermatophylax or ampulla weight. Spermatophore weight, but not sperm number, was positively correlated with male body weight. Ampulla weight was positively correlated with spermatophylax weight.

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.