Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians

A variety of field studies suggest that sex change in animalsmay be more complicated than originally depicted by the size-advantagehypothesis. A modification of the size-advantage hypothesis,the expected reproductive success threshold model, proposesthat sperm competition and size-fecundity skew can stronglyaffect reproductive pay-offs. Size-fecundity skew occurs ifa large female's fecundity is markedly higher than the aggregateof the other members of her social group and, together withpaternity dilution from sperm competition, can produce situationsin which large females benefit by deferring sex change to smallerfemales. Deferral by large females can create sex-size distributionscharacterized by the presence of large females and small sex-changedmales, and it is precisely these distributions that the traditionalsize-advantage model cannot explain. We tested the predictionsof the new model with the bucktooth parrotfish, Sparisoma radians,on coral reefs in St. Croix, U.S. Virgin Islands. Collectionsand spawning observations determined that the local environmentalregime of S. radians is characterized by pervasive sperm competition(accompanying 30% of spawns) and factors that can produce substantialsize-fecundity skew in social groups. Dominant male removalexperiments demonstrate that the largest females in social groupsoften do not change sex when provided an opportunity. Instead,smaller, lower-ranking females change sex when a harem vacancyarises. This pattern of sex change is in contrast to virtuallyall previous studies of social control of sex change in fishes,but provides strong support for the general predictions of theexpected reproductive success threshold model.     

Sperm competition and sex change: a comparative analysis across fishes

Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change.     

Sperm competition and the evolution of ejaculate composition

We present a model of sperm competition that incorporates both sperm and nonsperm parts of the ejaculate. Our primary focus is on determining how ejaculate composition and size evolves as a function of the effects of seminal fluid on male reproductive success and as a function of asymmetry in sperm usage by females. The model predicts that different patterns of investment in sperm and seminal products are expected to evolve as a function of the bias in sperm usage by females. It also predicts the evolution of distinct patterns in ejaculate composition depending on the function of seminal fluid. In the discussion, we highlight a number of potential approaches for testing the theory that we develop.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

Reproductive Competition Among Males in Multimale Groups of Primates: Modeling the Costs and Effectiveness of Conflict

Multimale groups of primates are characterized by strong reproductive competition among males, generally resulting in an uneven division of male reproductive success (reproductive skew). The observed patterns of conflict and reproductive skew have often been attributed to the so-called tug-of-war model. We show, however, that two important assumptions of this model are not met in male primates. First, the tug-of-war model assumes that reproductive conflict reduces overall group productivity, but in male primates (and most other vertebrates) conflict likely involves mortality rather than fecundity costs. Second, the tug-of-war model does not account for the possibility that male primates can achieve some reproductive success without engagement in open conflict, such as when a single male cannot guard several receptive females at the same time. We therefore develop a dynamic version of the tug-of-war model, in which reproductive competition causes mortality costs, and in which individuals can gain uncontested shares of reproduction dependent on the degree of female receptive overlap. This model differs substantially from the original tug-of-war model, and derives a new and rich set of comparative predictions. For instance, it predicts that the level of conflict among males declines as the queuing success of subordinate males increases (as survival increases), and also, as their uncontested share of reproduction increases, e.g., as female receptive overlap increases. Our model shows how male–male conflict and female receptive overlap collectively determine the level of reproductive skew among male primates, and illustrates that this relationship is more complex than previously thought.     

REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

Abstract I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex‐ratio theory predicts that workers in monogynous (single‐queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker‐controlled population sex ratio is too female‐biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less‐valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen‐worker conflict over sex allocation.     

Size, operational sex ratio, and mate-guarding success of the carrion beetle, Necrophila americana

When male insects guard females until oviposition, the benefitsfrom last-male sperm precedence must outweigh the costs of relinquishingadditional fertilizations. The profitability of guarding isincreased when males guard large, fecund females and when femalesare scarce because fewer fertilizations are sacrificed. However,the male reproductive success is not only determined by theprofitability of guarding but also by his ability to maintainguarding. In this study, we used male carrion beetles (Necrophilaamericana) to examine the effects of sex ratio, male relativesize, and female quality on the ability to guard. First, wepresent a model of mate guarding that explores factors, suchas sperm precedence, sex ratio, male size, and female quality,that influence the profitability of postcopulatory riding. Ourmodel predicts that large N. americana males should preferentiallyguard the largest female only when the sex ratio is male biasedand sperm precedence is above 80%. In contrast, small malesgain little from guarding because they are not likely to maintainit and be the last male to mate. Then, we tested these predictionsby manipulating sex ratio, relative male size, and female quality.All males in equal sex ratio and large males in male-biasedsex ratio guarded females significantly longer than did malesin female-biased sex ratio. In male-biased sex ratio, largemales guarded significantly longer and achieved more takeoversthan small males. Large females were guarded longer. The successof guarding males in this beetle depends on their size relativeto other males and the operational sex ratio.     

EFFECTS OF FERTILIZATION DISTANCE ON MALE GAIN CURVES IN A FREE‐SPAWNING MARINE INVERTEBRATE: A COMBINED EMPIRICAL AND THEORETICAL APPROACH

Male gain curves describe the relationship between allocation to sperm production and male reproductive success and are central to models of sex allocation in hermaphrodites. Sperm competition is expected to result in more linear gains and select for increased allocation. We hypothesized that high sperm production in passively mating systems may also be the result of selection to enhance the ability to fertilize distant ova. Consequently, we explored the effect of distance on male gain curves in a free‐spawning colonial ascidian. The performance of focal males that varied in sperm production was assayed at three distances via microsatellite markers. An advection‐diffusion model was used to estimate sperm concentration gradients, to predict male reproductive gain integrated across multiple downstream females, and explore effects of hydrodynamic conditions. As distance increased, male reproductive success decreased and empirical gain curves became increasingly linear. Our model predicted that the expected net gain curve is relatively insensitive to variation in flow regime and will saturate much more slowly than if only a single, nearby distance is considered. Thus, high levels of sperm production may enhance fitness both in competitive situations and with increasing fertilization distance, highlighting the need to consider distance effects when evaluating gain curves.     

Optimal copula duration in yellow dung flies: effects of female size and egg content

We examine data on copula duration in dung flies, Scatophaga stercoraria, in relation to female phenotype. We use a marginal value theorem approach based on the plausible mechanisms of sperm competition to predict the effect of female variation on optimal copula duration, t *, from the male perspective. Future fertilizations are expected to have a trivial effect on t * with fully gravid females, but an increasing relative effect on t * towards completion of oviposition. t * is expected to be affected by female size because of variation in (1) a female's egg content, which increases the maximum egg gain available from a mating, and (2) the female reproductive tract, which affects the rate at which sperm are displaced. In fully gravid females, t * was not dependent on egg number variation, but showed a positive relation with egg content in females that had laid a varying proportion of their mature egg load at the time of mating, and were therefore not fully gravid. Our models predict that if a male can estimate egg content only by the distension of a female's abdomen, t * should increase in a similar way to that seen with 'take-over' females. We predict t * for fully gravid females by assuming that males can monitor female size. The data showed that sperm displacement rate decreased, and average egg content increased, with female size. Under two models for a sperm displacement mechanism, one (which assumes indirect displacement at a rate proportional to the increase in spermathecal volume) predicts the observed relation between t * and female size almost exactly. Small males copulated for longer than large males (as predicted and reported previously). Copyright 1999 The Association for the Study of Animal Behaviour.     

Mate-Guarding as a Male Reproductive Tactic in <Emphasis Type="Italic">Propithecus verreauxi</Emphasis>

Sexual selection theory predicts that in group-living mammals, male reproductive tactics can lead to high reproductive skew in favor of dominant individuals. In sifakas (Propithecus verreauxi), a group-living primate with extremely seasonal reproduction, male reproductive success is highly skewed because dominant males sire almost all offspring despite a tendency toward an even adult group sex ratio. To understand the underlying behavioral mechanism resulting in this rank-related reproductive skew in male sifakas, we studied mate-guarding as a potential reproductive tactic. Behavioral observations of dominant males and adult females in combination with hormonal determination of timing of female receptivity in 9 groups at Kirindy Forest revealed that dominant males spent more time in proximity to females when they were receptive and were responsible for the maintenance of this proximity. Results also indicated that monopolization of receptive females was facilitated by both estrous asynchrony within groups and by the ability of dominant males to obtain olfactory cues as to the timing of female receptivity. Although dominant males engaging in mate-guarding are expected to experience various costs, there was no evidence for decreased foraging behavior and only a trend toward increased aggression between dominant and subordinate non-natal males within groups. Our results are in accordance with the hypothesis that dominant males use mate-guarding to monopolize receptive females and that it is one proximate mechanism that contributes to the high reproductive skew observed within the population of male sifakas at Kirindy.     

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.     

The role of sperm numbers in sperm competition and female remating in Drosophila melanogaster

Single mating productivities (used as estimates of the relative number of sperm transferred) are highly correlated with several parameters used to quantify sperm competition in D. melanogster. Matings that result in the transferal of large numbers of sperm are associated with longer delay of female remating than are matings that transfer fewer sperm. Males that transfer larger numbers of sperm also suffer a smaller proportional reduction in reproductive success (smaller COST) than males transferring fewer sperm. The number of sperm transferred by a female's second mate is not related to the COST to the first male. However, there is a high positive correlation between the number of sperm transferred by the second male and P₂ (the proportion of second male progeny following female remating). Thus, large sperm numbers apparently increase the reproductive success of males whether they mate with virgin or non-virgin females. Because female receptivity mediates these events, there is no need to invoke sperm displacement to explain the reproductive outcome of female remating.The timing of female remating is evaluated in terms of a receptivity-threshold model. This model suggests that female receptivity returns when some small, relatively constant, number of sperm remain in storage.     

Condition dependence of male and female reproductive success: insights from a simultaneous hermaphrodite

Sexually selected traits are predicted to show condition dependence by capturing the genetic quality of its bearer. In separate‐sexed organisms, this will ultimately translate into condition dependence of reproductive success of the sex that experiences sexual selection, which is typically the male. Such condition dependence of reproductive success is predicted to be higher in males than females under conditions promoting intense sexual selection. For simultaneous hermaphrodites, however, sex allocation theory predicts that individuals in poor condition channel relatively more resources into the male sex function at the expense of the female function. Thus, male reproductive success is expected to be less condition dependent than female reproductive success. We subjected individuals of the simultaneously hermaphroditic snail Physa acuta to two feeding treatments to test for condition dependence of male and female reproductive success under varying levels of male–male competition. Condition dependence was found for female, but not for male, reproductive success, meaning that selection on condition is relatively stronger through the female sex function. This effect was consistent over both male–male competition treatments. Decomposition of male and female reproductive performance revealed that individuals in poor condition copulated more in their male role, indicating an increased male allocation to mate acquisition. These findings suggest that sex‐specific condition dependence of reproductive success is at least partially driven by condition‐dependent sex allocation. We discuss the implications of condition‐dependent sex allocation for the evolution of sexually selected traits in simultaneous hermaphrodites.     

Why do chimpanzee males attack the females of neighboring communities?

Our closest nonhuman primate relatives, chimpanzees, engage in potentially lethal between‐group conflict; this collective aggressive behavior shows parallels with human warfare. In some communities, chimpanzee males also severely attack and even kill females of the neighboring groups. This is surprising given their system of resource defense polygyny, where males are expected to acquire potential mates. We develop a simple mathematical model based on reproductive skew among primate males to solve this puzzle. The model predicts that it is advantageous for high‐ranking males but not for low‐ranking males to attack females. It also predicts that more males gain a benefit from attacking females as the community's reproductive skew decreases, i.e., as mating success is more evenly distributed. Thus, fatal attacks on females should be concentrated in communities with low reproductive skew. These attacks should also concur with between‐community infanticide. A review of the chimpanzee literature provides enough preliminary support for this prediction to warrant more detailed testing. Am J Phys Anthropol 155:430–435, 2014. © 2014 Wiley Periodicals, Inc.     

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live‐bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male‐biased broods had greater mating success at maturity than sons in female‐biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male‐biased brood when the reproductive success of sons is expected to be high.     

THE COSTS OF CHANGING SEX AND THE ONTOGENY OF MALES UNDER CONTEST COMPETITION FOR MATES

In its simplest form, the size-advantage hypothesis predicts that individuals should change sex in order to increase their reproductive success. In terms of lifetime expectations, this must be true for the hypothesis to hold. However, as we review here, some loss of reproductive success may occur immediately after sex change. Unavoidable costs (e.g., those resulting from a restructuring of the gonad) have not been adequately distinguished from adaptive allocations of resources which diminish current reproduction in favor of large increases in future mating success. This strategy can become particularly important for species in which a few males monopolize matings. To illustrate this idea, we describe the changes in mating frequency as mature females become sexually active males in three species of protogynous wrasses. In one species, a male defends a permanent, all-purpose territory composed of up to 12 females. When he is removed, a single female changes sex and successfully completes mating sequences with all females in the territory within an average of 5.6 days. This duration roughly corresponds to the time required for functional transformation of gonads; thus, individuals in this species suffer few reproductive losses as a result of changing sex. The largest males in two other species mate with an average of 25 to 50 females per day, but only by successfully defending reproductive territories. In one of those species, individuals that changed sex mated infrequently over a two-year period after sexual transformation and, by the end of the study, were still well below the average size of males that consistently obtained territories. Sex-changed individuals in the other species had very low reproductive success for up to 45% of the maximum lifespan as a male. It is improbable that the substantial cost of changing sex in the latter two species results from gonad restructuring or from mistakes due to imprecise cues for sex change. Instead, the cost appears to represent an investment in growth rather than current reproduction as a means of rapidly attaining a size advantage when individuals face intense competition for extraordinarily successful mating territories.     

Influence of female reproductive anatomy on the outcome of sperm competition in Drosophila melanogaster

Females as well as males can influence the outcome of sperm competition, and may do so through the anatomy of their reproductive tracts. Female Drosophila melanogaster store sperm in two morphologically distinct organs: a single seminal receptacle and, normally, two spermathecae. These organs have different temporal roles in sperm storage. To examine the association between sperm storage organ morphology and sperm competition, we used a mutant type of female with three spermathecae. Although the common measure of sperm competition, P(2), did not differ between females with two and three spermathecae, the pattern of sperm use over time indicated that female morphology did affect male reproductive success. The rate of offspring production by females with three spermathecae rose and fell more rapidly than by females with two spermathecae. If females remate or die before using up second male sperm, then second male reproductive success will be higher when they mate with females with three spermathecae. The results indicate that temporal patterns of sperm use as well as P(2) should be taken into account when measuring the outcome of sperm competition.     

Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

An integrative view of sexual selection in Tribolium flour beetles

Sexual selection is a major force driving the evolution of diverse reproductive traits. This evolutionary process is based on individual reproductive advantages that arise either through intrasexual competition or through intersexual choice and conflict. While classical studies of sexual selection focused mainly on differences in male mating success, more recent work has focused on the differences in paternity share that may arise through sperm competition or cryptic female choice whenever females mate with multiple males. Thus, an integrative view of sexual selection needs to encompass processes that occur not only before copulation (pre-mating), but also during copulation (peri-mating), as well as after copulation (post-mating), all of which can generate differences in reproductive success. By encompassing mechanisms of sexual selection across all of these sequential reproductive stages this review takes an integrative approach to sexual selection in Tribolium flour beetles (Coleoptera: Tenebrionidae), a particularly well-studied and economically important model organism. Tribolium flour beetles colonize patchily distributed grain stores, and juvenile and adult stages share the same food resources. Adults are highly promiscuous and female reproduction is distributed across an adult lifespan lasting approximately 1 year. While Tribolium males produce an aggregation pheromone that attracts both sexes, there appears to be little pre-mating discrimination among potential mates by either sex. However, recent work has revealed several peri-mating and post-mating mechanisms that determine how offspring paternity is apportioned among a female's mates. During mating, Tribolium females reject spermatophore transfer and limit sperm numbers transferred by males with low phenotypic quality. Although there is some conflicting evidence, male copulatory leg-rubbing appears to be associated with overcoming female resistance to insemination and does not influence a male's subsequent paternity share. Evidence suggests that Tribolium beetles have several possible post-mating mechanisms that they may use to bias paternity. Male sperm precedence has been extensively studied in Tribolium spp. and the related Tenebrio molitor, and several factors influencing male paternity share among a female's progeny have been identified. These include oviposition time, inter-mating interval, male strain/genotype, the mating regimen of a male's mother, male starvation, and tapeworm infection. Females exert muscular control over sperm storage, although there is no evidence to date that females use this to differentiate among mates. Females could also influence offspring paternity by re-mating with additional males, and T. castaneum females more readily accept spermatophores when they are re-mating with more attractive males. Additional work is needed to examine the possible roles played by both male and female accessory gland products in determining male paternity share. Sexual selection during pre-mating episodes may be reinforced or counteracted by peri- and post-copulatory selection, and antagonistic coevolution between the sexes may be played out across reproductive stages. In Tribolium, males' olfactory attractiveness is positively correlated with both insemination success and paternity share, suggesting consistent selection across different reproductive stages. Similar studies across sequential reproductive stages are needed in other taxa to provide a more integrative view of sexual selection.     

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.