Sexual selection favors female-biased sex ratios: the balance between the opposing forces of sex-ratio selection and sexual selection

In a verbal model, Trivers and Willard proposed that, whenever there is sexual selection among males, natural selection should favor mothers that produce sons when in good condition but daughters when in poor condition. The predictions of this model have been the subject of recent debate. We present an explicit population genetic model for the evolution of a maternal-effect gene that biases offspring sex ratio. We show that, like local mate competition, sexual selection favors female-biased sex ratios whenever maternal condition affects the reproductive competitive ability of sons. However, Fisherian sex-ratio selection, which favors a balanced sex ratio, is an opposing force. We show that the evolution of maternal sex-ratio biasing by these opposing selection forces requires a positive covariance across environments between the sex-ratio bias toward sons (b) and the mating success of sons (r). This covariance alone is not a sufficient condition for the evolution of maternal sex-ratio biasing; it must be sufficiently positive to outweigh the opposing sex-ratio selection. To identify the necessary and sufficient conditions, we partition total evolutionary change into three components: (1) maternal sex-ratio bias, (2) sexual selection on sons, and (3) sex-ratio selection. Because the magnitude of the first component asymmetrically affects the strength of the second, biasing broods toward females in a poor environment evolves faster than the same degree of bias toward males in a good environment. Consequently, female-biased sex ratios, rather than male-biased sex ratios, are more likely to evolve. We discuss our findings in the context of the primary sex-ratio biases observed in strongly sexually selected species and indicate how this perspective can assist the experimental study of sex ratio evolution.     

Sex ratios when helpers stay at the nest

This study investigates the evolution of the sex ratio (parental investment in sons) when breeding adults are supported by help provided by nonbreeding individuals of one sex. The study also assumes that the helping sex remains on its natal site to compete for the opportunity to breed, whereas the nonhelping sex disperses. Two kin-selection models are presented, both of which incorporate the age structure found in many natural populations where such helping occurs. The first model assumes that helpers increase the survival of their parents. The second model assumes that helpers are indiscriminant: a helper chooses to increase the survival of a random pair of adults breeding on its natal patch. In both models, sex ratios are not always biased toward the sex that provides the most help. When helpers do not discriminate (second model), the direction of sex-ratio bias is determined solely by the size of the benefit of helping behavior. When this benefit is small, sex-ratio evolution is primarily influenced by local resource competition and sex ratios are biased toward the nonhelping (dispersive) sex. If the benefit of help is large enough, the effect of local resource competition is reduced and sex-ratio bias favors the helpful sex. When helpers help only their parents, the same qualitative relationship exists between the direction of sex-ratio bias and the benefit of helping. In this case, however, the direction of sex-ratio bias is also influenced by the size of the social group, mortality, and which individual (mother or father) controls the sex ratio. This study also investigates a sex-ratio conflict that exists between mates. Helping behavior of nonbreeders can act to alleviate the disparities between the optimal sex ratio from the perspective of a mother and that from the perspective of a father. This consequence of helping has not been previously recognized.     

Do female parasitoid wasps recognize and adjust sex ratios to build cooperative relationships?

Sex allocation theories provide excellent opportunities to investigate not only the extent to which individuals' behaviour is adaptive, but also how they use relevant information for their decision-making. Here, we investigated whether female parasitoid wasps recognize the sex ratios of other females and adjust their laying sex ratios accordingly. Specifically, we tested the prediction of reciprocal cooperation over sex allocation. Theory predicts more female-biased (cooperative) sex ratios than in the interest of individual benefit, when a restricted number of ovipositing females interact for a long period and their offspring mate within the natal patch. This is because the female-biased sex ratio reduces competition for mates among the male offspring of the females and increases the overall reproductive productivity of the patch. In this case, females would be expected to respond to more even (noncooperative) sex ratios by others and to retaliate by also producing a less female-biased sex ratio to avoid exploitation by defectors. However, contrary to this prediction, our experiment using a sterile male technique showed that female Melittobia australica did not change their offspring sex ratios in response to the sex ratios produced by other females. This suggests that their extremely female-biased sex ratios cannot be explained by reciprocity. A meta-analysis of studies examining sex recognition ability in parasitoid wasps also did not support the predicted pattern of relevant sex ratio adjustment, suggesting that parasitoid females do not possess this ability. Here, we discuss the conditions necessary for the evolution of reciprocity linked to recognition ability.     

FEMALE-BIASED SEX RATIOS: INDIVIDUAL OR GROUP SELECTION?

The evolution of biased sex ratios in a randomly structured population stems from individual selection acting through local parental control (LPC) of the sex ratio and hence of the mating success of the sons and/or daughters. As a general rule, the sex ratio is biased away from the sex whose fitness is most affected by changes in the local sex ratio. This is the sex whose fitness is subject to the most effective parental control. The bias acts to increase the fitness of the rarer, controlled sex and to increase parental productivity. In the specific case of the evolution of the female-biased Hamiltonian ratios, LPC can affect the mating success of sons but has no effect on the success of daughters. It is argued here and elsewhere (Nunney, unpubl.) that group selection can only promote the spread of a genotype through the maintenance of a positive association of individuals of that genotype. The importance of positive association is well established in the special case of kin selection. Given such a definition, group selection plays no part in the evolution of the Hamiltonian sex ratios, although it is possible to conceive of circumstances under which group selection could favor an even more extreme sex ratio bias. In general, such circumstances involve kin selection. It is argued that the examination of differences in group productivity is not a useful way of looking at the process of natural selection, since (i) by dividing up almost any evolving population into random groups, some groups (those with the highest frequency of the fittest individuals) will be more productive than others; and (ii) in the specific case of the evolution of the Hamiltonian ratios, it is possible to develop models either with or without a group structure and get the same result. Hamilton (1967) originally suggested that a female-biased sex ratio arose in his model because of the advantage of reducing local mate competition (specifically, reducing competition between brothers for mates). This possibility was eliminated by developing a model in which competition between the brothers was prevented regardless of the sex ratio. It was found that the optimum sex-ratio strategy was unaffected. On the other hand, the idea of local parental control has, in each case examined, been able to account for the predicted optimum strategy.     

Adaptive colony sex ratios in primitively eusocial bees

Colony-level predictions about sex-ratio optimization in eusocial Hymenoptera are different from the ones that apply to the population level. A recent empirical study on the sweat bee Halictus rubicundus has revealed a distinct pattern in the colony sex ratio of the summer brood: eusocial colonies produced more female-biased sex ratios and non-eusocial colonies produce more male-biased sex ratios. These data are consistent with theoretical hypotheses as put forward by Trivers and Hare and several later authors. When interpreted in the light of these theoretical contentions, the sex-ratio variation in Halictus rubicundus appears to be adaptive for workers, replacement queens and - under reasonable additional assumptions - also for foundresses.     

Intersexual competition as an explanation for sex-ratio and dispersal biases in polygynous species

In polygynous mammals, it is commonly observed that both sex ratios at birth and dispersal are male biased. This has been interpreted as resulting from low female dispersal causing high female local resource competition, which would select for male-biased sex ratios. However, a female-biased sex ratio can be selected despite lower female than male-biased dispersal. This will occur if the low female dispersal is close to the optimal dispersal rate, while the male dispersal is not close to the optimal dispersal rate. The actual outcome depends on the joint evolution of sex-biased dispersal and sex ratio. Earlier analyses of joint evolution imply that there will be no sex-ratio nor dispersal biases at the joint evolutionarily stable strategy, thus they do not explain the data. However, these earlier analyses assume no intersexual competition for resources. Here, we show that when males and females compete with each other for access to resources, male-biased dispersal will be associated with male-biased birth sex ratio, as is commonly observed. A trend toward male-biased birth sex ratios is also expected if there is intersexual local resource competition and if birth sex ratio is constrained so that it cannot depart from balanced sex ratio.     

Can the extremely female‐biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?

Abstract.  1. Extremely female-biased sex ratios are known in the social spider mite species, Stigmaeopsis longus and S. miscanthi . Whether Hamilton's local mate competition (LMC) theory can explain such sex ratios was investigated.
2. Significant changes of the progeny sex ratios in the direction predicted by the LMC model were found in both species when the foundress number changed. Therefore, LMC can partly explain the skewed sex ratios in these species.
3. When the foundress number increased, the progeny sex ratio was still female biased and significantly different from the prediction of the LMC model for haplodiploidy. Relatedness between foundresses could not fully explain the female-biased sex ratios. Therefore, these results suggest that there are factors other than LMC skewing the sex ratios of these species toward female.     

The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies

Mutual policing is thought to be important in conflict suppression at all levels of biological organization. In hymenopteran societies (bees, ants, and wasps), multiple mating by queens favors mutual policing of male production among workers (worker policing). However, worker policing of male production is proving to be more widespread than predicted by relatedness patterns, occurring in societies headed by single-mated queens in which, paradoxically, workers are more related to the workers' sons that they kill than the queen's sons that they spare. Here we develop an inclusive-fitness model to show that a second reproductive conflict, the conflict over sex allocation, can explain the evolution of worker policing contrary to relatedness predictions. Among ants, and probably other social Hymenoptera, workers kill males to favor their more related sisters. Importantly, males are killed at the larval stage, presumably because workers cannot determine the sex of queen-laid eggs. Sex-allocation biasing favors worker policing because policing removes some males (the workers' sons) at low cost at the egg stage rather than at higher cost at the larval stage. Our model reveals an important interaction between two reproductive conflicts in which the presence of one conflict (sex allocation) favors the suppression of the other (male production by workers).     

Factors influencing the optimum sex ratio in a structured population

W. D. Hamilton (1967, Science 156, 477-488) calculated the optimum sex-ratio strategy for a population subdivided into local mating groups. He made three important assumptions: that the females founding each group responded precisely to the number of them initiating the group; that ail broods within a group matured synchronously; and that males were incapable of dispersing between groups. We have examined the effects of relaxing each of these assumptions and obtained the following results: (1) When broods mature asynchronously the optimum sex ratio is considerably more female biased than the Hamiltonian prediction. (2) Increasing male dispersal always decreases the optimum female bias to the sex ratio, but it is of particular interest that when moderate levels of dispersal are coupled with asynchrony of brood maturation then the optimum strategy is relatively insensitive to changes in foundress number. (3) When females cannot precisely determine the number of other foundresses initiating the group then the optimum strategy is almost exactly the strategy appropriate to a group of average size. These effects can be most easily understood in terms of local parental control (LPC) of the sex ratio. Through LPC a founding female can alter the mating success of her sons by altering the sex ratio of her brood. Asynchrony in the maturation of broods within a group increases the control that a founding female has over the mating success of her sons, whereas male dispersal reduces it. We have shown that the role of LPC and the role of inbreeding, which favors a female-biased sex ratio in haploidiploid species, are independent and that their effects can be combined into a single general formula r = (1-(r2/z2) E(alpha z/alpha r]/(1 + I). The concept of LPC can also be used to interpret two factors which have been proposed to select for the Hamiltonian sex ratios: local mate competition is LPC acting through sons; and sib mating is LPC acting through daughters.     

Pollination intensity influences sex ratios in dioecious Rumex nivalis, a wind-pollinated plant

Determining the mechanisms governing sex-ratio variation in dioecious organisms represents a central problem in evolutionary biology. It has been proposed that in plants with sex chromosomes competition between pollen tubes of female- versus male-determining microgametophytes (certation) causes female-biased primary sex ratios. Experimental support for this hypothesis is limited and recent workers have cast doubt on whether pollen-tube competition can modify sex ratios in dioecious plants. Here we investigate the influence of variation in pollination intensity on sex ratios in Rumex nivalis, a wind-pollinated alpine herb with strongly female-biased sex ratios. In a garden experiment, we experimentally manipulated pollination intensity using three concentric rings of female recipient plants at different distances from a central group of male pollen donors. This design enabled us to test the hypothesis that increasing pollen load size, by intensifying gametophyte competition, promotes female-biased sex ratios in R. nivalis. We detected a significant decline in pollen load at successive distance classes with concomitant reductions in seed set. Sex ratios of progeny were always female biased, but plants at the closest distance to male donors exhibited significantly greater female bias than more distant plants. The amount of female bias was positively correlated with the seed set of inflorescences. Hand pollination of stigmas resulted in approximately 100-fold higher stigmatic pollen loads than wind-pollinated stigmas and produced exceptionally female-biased progenies (female frequency = 0.96). Our results are the first to demonstrate a functional relation between stigmatic pollen capture, seed set, and sex ratio and suggest that certation can contribute towards female-biased sex ratios in dioecious plants.     

Female-biased sex allocation in wild populations of the eriosomatine aphid Prociphilus oriens: local mate competition or transgenerational effects of maternal investment?

Several aphid species exhibit female-biased sex allocation. Local mate competition (LMC) has been postulated to be the evolutionary factor of the female-biased sex allocation. We estimated individual sex allocation in the eriosomatine aphid Prociphilus oriens and explained the observed pattern of sex allocation based on a hypothesis other than LMC. On the basis of the relationship between maternal body size and brood size, we estimated the cost of producing a female to be 1.85 times the cost of producing a male. The population-wide allocation to males was 22–24 %. Winged mothers exhibited a large variation in the number of male and female embryos they had, including 23–30 % of winged mothers producing only female embryos. There was polymorphism in the sex-ratio expression. Thus, the constant male hypothesis assuming LMC was not supported. Winged mothers that produced an all-female brood contained larger female embryos than did mothers that produced a bisexual brood. Previous studies have indicated that a large sexual female produces a single large egg, which hatches into a first-instar larva containing a larger amount of gonads. Thus, in eriosomatine aphids, maternal investment in daughters directly affects the potential fecundity of granddaughters, whereas investment in sons does not. We propose a hypothesis that higher fitness returns from maternal investment in daughters than in sons may have primarily led to the evolution of highly female-biased sex allocation in P. oriens.     

UNEXPLAINED SPLIT SEX RATIOS IN THE NEOTROPICAL PLANT-ANT, ALLOMERUS OCTOARTICULATUS VAR. DEMERARAE (MYRMICINAE): A TEST OF HYPOTHESES

We investigated sex allocation in the Neotropical ant Allomerus octoarticulatus var. demerarae . Because Allomerus is a plant symbiont, we could make geographically extensive collections of complete colonies and of foundresses in saplings, allowing us to estimate not only population- and colony-level sex allocation but also colony resource levels and the relatednesses of competing ant foundresses. This species exhibits a strongly split sex ratio, with 80% of mature colonies producing ≥90% of one sex or the other. Our genetic analyses (DNA microsatellites) reveal that Allomerus has a breeding system characterized by almost complete monogyny and a low frequency of polyandry. Contrary to theoretical explanations, we find no difference in worker relatedness asymmetries between female- and male-specialist colonies. Furthermore, no clear link was found between colony sex allocation and life history traits such as the number of mates per queen, or colony size, resource level, or fecundity. We also failed to find significant support for male production by workers, infection by Wolbachia , local resource competition, or local mate competition. We are left with the possibility that Allomerus exhibits split sex ratios because of the evolution of alternative biasing strategies in queens or workers, as recently proposed in the literature.     

CAN A PATCHY POPULATION STRUCTURE AFFECT THE EVOLUTION OF COMPETITION STRATEGIES?

Simulation models are described that examine the effect of a patchy population structure on the evolution of competition strategies. The results of the models suggest that a patchy population structure will make the evolution of scramble competition strategies more likely than in a single undivided population. The outcome of the models depends on the details of the population structure, in particular the number of individuals that found patches, the number of generations of competition within a patch, and the point at which founding females mate can all affect the evolutionary outcome. The results of the models are compared to those of previous models examining the effects of a structured population on the evolution of female-biased sex ratios, and altruistic behavior. The results of the model may help to explain the patterns of larval competition strategies observed in bruchid beetles.     

Local Competition, Inbreeding, and the Evolution of Sex-Biased Dispersal

Using game theory, we developed a kin-selection model to investigate the consequences of local competition and inbreeding depression on the evolution of natal dispersal. Mating systems have the potential to favor strong sex biases in dispersal because sex differences in potential reproductive success affect the balance between local resource competition and local mate competition. No bias is expected when local competition equally affects males and females, as happens in monogamous systems and also in polygynous or promiscuous ones as long as female fitness is limited by extrinsic factors (breeding resources). In contrast, a male-biased dispersal is predicted when local mate competition exceeds local resource competition, as happens under polygyny/promiscuity when female fitness is limited by intrinsic factors (maximal rate of processing resources rather than resources themselves). This bias is reinforced by among-sex interactions: female philopatry enhances breeding opportunities for related males, while male dispersal decreases the chances that related females will inbreed. These results meet empirical patterns in mammals: polygynous/promiscuous species usually display a male-biased dispersal, while both sexes disperse in monogamous species. A parallel is drawn with sex-ratio theory, which also predicts biases toward the sex that suffers less from local competition. Optimal sex ratios and optimal sex-specific dispersal show mutual dependence, which argues for the development of coevolution models.     

Sex-ratio distortion driven by migration loads

The significance of migration load in driving the evolution of recipient populations has long been documented in population genetics, but its effects have not been linked to the formation of biased sex ratios in natural populations. In this study, we develop a single-locus model to demonstrate how the migration load can shape the primary and secondary sex ratios in dioecious plants where sexual dimorphism is determined by the sex chromosomes (the XX-XY or similar systems). Our results show that migration load can generate an array of sex ratios (from the female- to male-biased primary/secondary sex ratios), depending on the selection systems at the gametophyte and sporophyte stages and on the sex ratio in the migrating seeds. Ovule abortion and the purging of maladaptive genes from the immigrating pollen at the gametophyte stage can alter the primary sex ratio and indirectly alter the secondary sex ratio. The presence of maladaptive sex-linked genes from the migrating pollen and seeds of males facilitates the outcome of the female-biased secondary sex ratios, while the presence of maladaptive sex-linked genes from the migrating seeds of females can lead to the male-biased secondary sex ratios. The detrimental effects of the Y-chromosome from the migrating pollen and seeds can enhance the formation of female-biased primary and secondary sex ratios. These theoretical predictions highlight an alternative approach to the existing sex-ratio theories for interpreting the formation of biased sex ratios in the populations that are subject to the impacts of maladaptive genes from immigrants.     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

Local mate competition with lethal male combat: effects of competitive asymmetry and information availability on a sex ratio game

We constructed a sex allocation model for local mate competition considering the asymmetry of competitive abilities among sons. This model assumes two females of a parasitoid wasp oviposit on the same host in sequential order. The evolutionarily stable strategy will be in either Stackelberg or Nash equilibrium, depending on whether the females can recognize their opponent's sex ratio or not, respectively. The Nash equilibrium predicts the second female produce more males than the first. If the second female is able to know and respond to the strategy of the first (a Stackelberg equilibrium), the first will decide an optimal sex ratio assuming that the second reply to it. Under such an assumption, our model predicts that not producing sons is adaptive for the second female when the sons she produces have low competitive ability. Males of parasitoid wasps Melittobia spp. are engaged in lethal male-male combat, indicating large asymmetry in mating success among sons. If females have the ability to recognize their opponent's sex ratio, our model suggests that the severe lethal male-male combat may be one factor explaining their extremely female-biased sex ratio that is unexplainable by pre-existent models.     

Sex-ratio distortion driven by migration loads

The significance of migration load in driving the evolution of recipient populations has long been documented in population genetics, but its effects have not been linked to the formation of biased sex ratios in natural populations. In this study, we develop a single-locus model to demonstrate how the migration load can shape the primary and secondary sex ratios in dioecious plants where sexual dimorphism is determined by the sex chromosomes (the XX–XY or similar systems). Our results show that migration load can generate an array of sex ratios (from the female- to male-biased primary/secondary sex ratios), depending on the selection systems at the gametophyte and sporophyte stages and on the sex ratio in the migrating seeds. Ovule abortion and the purging of maladaptive genes from the immigrating pollen at the gametophyte stage can alter the primary sex ratio and indirectly alter the secondary sex ratio. The presence of maladaptive sex-linked genes from the migrating pollen and seeds of males facilitates the outcome of the female-biased secondary sex ratios, while the presence of maladaptive sex-linked genes from the migrating seeds of females can lead to the male-biased secondary sex ratios. The detrimental effects of the Y-chromosome from the migrating pollen and seeds can enhance the formation of female-biased primary and secondary sex ratios. These theoretical predictions highlight an alternative approach to the existing sex-ratio theories for interpreting the formation of biased sex ratios in the populations that are subject to the impacts of maladaptive genes from immigrants.