Evolution of extraordinary female-biased sex ratios: the optimal schedule of sex ratio in local mate competition

Female-biased sex ratio in local mate competition has been well studied both theoretically and experimentally. However, some experimental data show more female-biased sex ratios than the theoretical predictions by Hamilton [1967. Science 156, 477-488] and its descendants. Here we consider the following two effects: (1) lethal male-male combat and (2) time-dependent control (or schedule) of sex ratio. The former is denoted by a male mortality being an increasing function of the number of males. The optimal schedule is analytically obtained as an evolutionarily stable strategy (ESS) by using Pontrjagin's maximum principle. As a result, an ESS is a schedule where only males are produced first, then the proportion of females are gradually increased, and finally only females are produced. Total sex ratio (sex ratio averaged over the whole reproduction period) is more female-biased than the Hamilton's result if and only if the two effects work together. The bias is stronger when lethal male combat is severer or a reproduction period is longer. When male-male combat is very severe, the sex ratio can be extraordinary female-biased (less than 5%). The model assumptions and the results generally agree with experimental data on Melittobia wasps in which extraordinary female-biased sex ratio is observed. Our study might provide a new basis for the evolution of female-biased sex ratios in local mate competition.     

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.     

Sex allocation in black-capped chickadees Poecile atricapilla

Optimal sex allocation for individuals can be predicted from a number of different hypotheses. Fisherian models of sex allocation predict equal investment in males and females up to the end of parental care and predict brood compositions based on the relative costs of producing males and females. The Trivers-Willard hypothesis predicts that individual females should alter the sex ratio of their broods based on their own condition if it has a differential impact on the lifetime reproductive success of their sons and daughters. The Charnov model of sex allocation predicts that females should alter sex allocation based on paternal attributes that may differentially benefit sons versus daughters. Because females are the heterogametic sex in birds, many recent studies have focussed on primary sex ratio biases. In black-capped chickadees Poecile atricapilla , males are larger than females suggesting they may be more costly to raise than females. Female condition affects competitive ability in contests for mates, and thus may be related to variance in fecundity. Females prefer high-ranking males as both social and extrapair partners. These observations suggest that females might vary the sex ratio of their broods based on the predictions of any of the above models. Here, we report on the results of PCR based sex determination of 1093 nestlings in 175 broods sampled from 1992 to 2001. Population-wide, we found a mean brood sex ratio of 0.525±0.016, with no significant deviation from a predicted binomial distribution. We found no effect of clutch size, female condition, hatch date, parental rank or paternity. Our results reject the idea that female black-capped chickadees systematically vary sex allocation in their broods.     

When should a female avoid adding eggs to the clutch of another female? A simultaneous oviposition and sex allocation game

Summary Avoidance of double oviposition (ADO) is the strategy not to oviposit on food patches where another female has oviposited before. If two females oviposit on the same patch, competitive and mating interactions within and between broods may lead to both a clutch size game and a sex allocation game between the two visitors. Though the two games interact, they are usually considered separately. Here, the ESS conditions for ADO are investigated in an analysis that combines the two games into one. The analysis strengthens the notion that it is really ADO that needs to be explained, because role-dependent net pay-off from an additional egg is most likely to favour double oviposition (DO). To a first female, the net payoff includes the effect on the eggs already present, whereas to a second female only the egg's gross pay-off matters. ADO is the evolutionary stable strategy (ESS) if there are enough patches still without eggs and either (1) the fitness of an additional egg is so low that the first female would not lay it even in the absence of detrimental effects on earlier offspring, so neither would a second female, or (2) differences in either the survival probability of the offspring or their reproductive success are sufficient to counterbalance the differential interest in the eggs already present. The first condition requires that eggs are relatively large, because then the decrease in pay-off between two successive eggs can be large. The second condition may be met when there is a time interval between ovipositions of subsequent females. The resulting developmental lag of the second clutch will (1) diminish its ability to compete for food and (2) lower its reproductive success when there is local mate competition and sons are too late to mate with daughters of the first female. If sons of first and second females compete on equal terms, however, ADO is unlikely. Male migration between patches reduces the influence of sex allocation strategies on clutch size decisions; the same holds for small clutch sizes. To illustrate the importance of considering sex allocation and clutch size decisions in an integrated way, oviposition strategies of plant-inhabiting predatory mites (Acari: Phytoseiidae) are discussed.     

Sex ratio schedules in a dynamic game: the effect of competitive asymmetry by male emergence order

Studies of sex allocation have provided some of the most successfultests of theory in behavioral and evolutionary ecology. Forinstance, local mate competition (LMC) theory has explainedvariation in sex allocation across numerous species. However,some patterns of sex ratio variation remain unexplained by existingtheory. Most existing models have ignored variation in malecompetitive ability and assumed all males have equal opportunitiesto mate within a patch. However, in some species experiencingLMC, males often fight fiercely for mates, such that male matingsuccess varies with male fighting ability. Here, we examinethe effect of competitive ability on optimal sex allocationschedules using a dynamic programming approach. This model assumesan asymmetric competitive ability derived from different mortalitiesaccording to the timing of male emergence. If the mortalityof newly emerging males is larger than that of already emergedmales, our model predicts a more female-biased sex ratio thanexpected under traditional LMC models. In addition, femalesare predicted to produce new males constantly at a low rateover the offspring emergence period. We show that our modelsuccessfully predicts the sex ratios produced by females ofthe parasitoid wasp Melittobia, a genus renowned for its vigorouslyfighting males and lower than expected sex ratios.     

Sex ratio response of the parasitoid wasp Muscidifurax raptor to other females

This study examines the sex ratio response of the parasitoid wasp Muscidifurax raptor to conspecific and confamilial females in relation to two groups of functional sex ratio models, local mate competition and host quality models. In some but not all experiments, M. raptor females produced a greater proportion of sons in the presence of a conspecific female than when alone, and this sex ratio effect carried over for a day after the females were isolated from each other M. raptor females also produced a greater proportion of sons in the presence of a female of the confamilial parasitoid Spalangia cameroni than when alone (although only on the second day of exposure to S. cameroni, not on the first). M. raptor's sex ratio increase in the presence of conspecifics is consistent with local mate competition models but not with host quality models because the presence of a conspecific female did not cause there to be more, and thus potentially smaller, offspring developing per host. In contrast, the presence of a S. cameroni female did cause there to be more offspring developing per host than when a M. raptor female was alone; thus M. raptor's sex ratio increase in the presence of S. cameroni may be explained by host quality models. An alternative explanation for the sex ratio increase in response to confamilials is that only a sex ratio response to conspecifics may be adaptive, due to local mate competition; but M. raptor females may be unable to distinguish between conspecific and S. cameroni females.     

Lack of Sex-Biased Maternal Investment in spite of a Skewed Birth Sex Ratio in White-Headed Langurs (Trachypithecus leucocephalus)

Numerous hypotheses have been developed to explain sex allocation. In male-dispersing, female cooperatively breeding species, the local resource competition model predicts male-biased birth sex ratio, the local resource enhancement model predicts female-biased birth sex ratio, and the population adjustment model predicts that biased birth sex ratio should not be favored if the two sexes are equally costly to rear. The male quality model predicts that, in polygynous species, females in better physical condition will either produce more sons than daughters or invest more heavily in sons than in daughters. White-headed langurs are a female philopatry and female cooperatively breeding species. During a 11-yr study, a total of 133 births were recorded, among which birth sex ratio (M:F = 73:49) was significantly male-biased. This is consistent with the prediction of the local resource competition model. On the other hand, if mothers balanced their investment between the two sexes, according to Fisher's population adjustment model, males should be the less-costly-to-rear sex. However, we found no sex difference for infant mortality (12.3% in males and 12.2% in females), and sons induced slightly longer interbirth interval (son: 26.4 ± 1.1 mo, daughter: 24.1 ± 0.6 mo) and lactational period (son: 20.9 ± 1.0 mo, daughters: 19.6 ± 0.5 mo) for their mothers. Thus, the population adjustment model was not supported by this study. The local resource enhancement model was not supported because birth sex ratio did not bias to females who provided more reproductive assistance. On the individual level, probit regression showed no relation between birth sex ratio and group size. Because the group size was considered to be negatively related to female physical condition, our study did not support the male-quality model. We suggested several possibilities to explain these results.     

Sex ratio genetics and the competitiveness of parasitic wasps

In the first part of the paper we analyse dynamics of the genetic mechanisms responsible for maintaining biased sex ratios in host-parasitoid interactions. We begin by reviewing recent results relating to the maintenance of sibmating in haplo-diploid populations. We then investigate the evolutionary stable sex ratio in populations in which all or some of the females mate with their brothers. In particular, we derive a diallelic one-locus model for studying evolutionary stable sex ratios in partially sibmating haplo-diploid populations. In the second part of the paper we review the impact of sex ratio on host-parasitoid populations. We then analyse how the sex ratio strategy of one parasitoid species may affect its interaction with another parasitoid species competing for the same host. In particular we show that, although a female biased sex ratio may enhance the inherent competitiveness of one species, it may also destabilize the ecological interaction of the three species so that all become extinct.     

Adaptive seasonal trend in brood sex ratio: test in two sister species with contrasting breeding systems

Evolutionary theory predicts adaptive adjustment in offspring sex ratio by females. Seasonal change in sex ratio is one possibility, tested here in two sister species, the Common sandpiper and the Spotted sandpiper Actitis hypoleucos and A. macularia. In the monogamous Common sandpiper, males are the most competitive sex. In each of 3 years, there was a change from mainly sons in early clutches to mainly daughters in late clutches. This seasonal adjustment of clutch sex ratio took place within the female before the eggs were laid, not by differential egg or chick survival. The sex of all eggs laid in the clutches used here was determined molecularly from chick blood taken at the time of hatching. The Spotted sandpiper in contrast is polyandrous, with partly reversed sex roles. There was no seasonal trend from sons to daughters in this species. When tested together, the two species differed significantly as predicted by the hypothesis of adaptive sex ratio adjustment by females.     

SEX-RATIO MANIPULATION IN RESPONSE TO HOST SIZE BY THE PARASITOID WASP SPALANGIA CAMERONI: A LABORATORY STUDY

The prediction of Charnov et al.'s (1981) host-size model that there should be a negative relationship between host size and wasp sex ratio (proportion sons) was supported for Spalangia cameroni, a solitary parasitoid wasp. The relationship was shown to be a result of offspring sex manipulation by females in response to host size rather than a result of differential mortality of the sexes. A major assumption of the host-size model is that host size has a greater effect on the ultimate reproductive success of emerging female wasps than of males. This assumption was not supported. Host size had a positive effect on the size of both male and female S. cameroni. However, neither host size nor wasp size affected longevity, production of offspring by females, or ability of males to compete for mates. Host size may differentially affect the reproductive success of female and male wasps through effects on other aspects of reproductive success. Tests of the assumptions of offspring sex-ratio manipulation hypotheses are scarce but critical, not only for parasitoid wasps, but also for other organisms.     

Extra-pair young in house wren broods are more likely to be male than female

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a female''s extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.     

Putting your sons in the right place: the spatial distribution of fig wasp offspring inside figs

Abstract. 1. Pollinating fig wasps (Hymenoptera, Agaonidae) display sex ratio adjustment, producing less female‐biased combined sex ratios as the number of ovipositing females (foundresses) inside a fig increases. Because males have low mobility, the oviposition sites (galled ovules) chosen by each foundress are likely to have consequences for the mating structure of wasp populations within the figs. 2. In this study, the spatial location of male and female progeny of the pollinating fig wasp Liporrhopalum tentacularis developing within figs of its host plant Ficus montana was examined to investigate two questions: (i) are male and/or female wasp offspring clustered together or interspersed? and (ii) is their distribution affected by whether one or two foundresses are present? Microsatellite markers were used to identify the progeny of different foundresses in dual‐foundress figs. 3. More offspring developed in the central part of the figs, compared with the ostiolar and basal parts, irrespective of foundress number. Neither male nor female wasp offspring were clustered within a fig. 4. The sons of the second foundress to enter a fig were positioned at similar minimum distances to both sibling and non‐sibling females, whereas the sons of the first foundress were closer to their sibling females than to non‐sibling females. If male wasps mate predominantly with females in adjacent galls, then the positioning of sons by the second foundresses is beneficial for them both in terms of reduced sibling mating and because they are provided with ready access to the female progeny of the first foundress.     

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.     

Maternal influences on brood sex ratios: an experimental study in tree swallows

When the reproductive value of sons and daughters differ, parents are expected to adjust the sex ratio of their offspring to produce more of the sex that provides greater fitness returns. The body condition of females or environmental factors, such as food abundance and mate quality, may influence these expected fitness returns. In a previous study of tree swallows (Tachycineta bicolor), we found that females produced more sons in their broods when they were in better body condition (mass corrected for size). We tested this relationship by experimentally clipping some flight feathers to reduce female body condition. As predicted, we found that females with clipped feathers had a lower proportion of sons in their broods and poorer body condition. However, female body condition alone was not a significant predictor of brood sex ratio in our experiment. We suggest that brood sex ratio is causally related to some other factor that covaries with body condition, most likely the foraging ability of females. The hypothesis that brood sex ratios are influenced by individual differences in female foraging ability is supported by a high repeatability of brood sex ratio for individual females. Thus, maternal effects may have a strong influence on the sex ratios of offspring.     

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

1. Neonicotinoid insecticides are potent neurotoxins of significant economic importance. However, it is clear that their use can adversely impact beneficial insects in the environment, even at low, sub‐lethal doses. 2. It has recently been shown that the neonicotinoid imidacloprid disrupts adaptive sex allocation in the parasitoid wasp Nasonia vitripennis (Walker) by limiting their ability to respond to the presence of other females on oviposition patches. In the present study, that work was extended to explore whether sex allocation when superparasitising – laying eggs on a host that has already been parasitised – is also disrupted by imidacloprid. 3. Under superparasitism, sex allocation theory predicts that females should vary their offspring sex ratio in relation to their relative clutch size. It was found that sex allocation under superparasitism in Nasonia is disrupted in a dose‐dependent manner, with exposed females producing more daughters. 4. Importantly, imidacloprid does not appear to influence the ability of females to estimate the number of eggs already present on a host, suggesting a disassociation between the sex ratio and clutch size cues. 5. The present work highlights the fitness costs to beneficial insects of exposure to neonicotinoids, but also provides clues as to how female Nasonia use information when allocating sex.     

Sex Allocation in a Colobine Monkey

In polygynous, sexual dimorphic species with higher variance in male reproductive success compared with females, females are expected to invest more heavily in sons than daughters within the constraints imposed by their physical condition (Science 1973; 179:90). Mothers in good condition, usually those of high rank, should produce more sons than females in poor condition or of low rank. We investigated sex allocation and sex‐biased maternal investment in a population of wild Hanuman langurs using rank and group size as approximations of female physical condition. Our results show that reproductive costs of sons were higher with both significantly longer interbirth intervals following male births and longer lactational periods for sons. Not in all groups did analyses of rank‐dependent sex allocation reveal the expected pattern of high‐ranking mothers producing more sons. However, sex ratio was significantly influenced by group size, with females from larger groups, i.e., in worse physical condition, producing a daughter‐biased sex ratio. In fact, only females of population‐wide superior physical condition can be expected to produce sons, because in Hanuman langurs males disperse and compete population‐wide. Thus, our results support the Trivers–Willard model and may explain the mixed evidence accruing from studies of single groups. We present a graphical model of how group size and dominance‐related differences in energy gain may influence sex allocation under different competitive regimes relative to overall resource availability. Tests of adaptive sex allocation models should consider whether reproductive competition of the preferred sex takes place primarily within a group or within the population.     

Split sex ratios in the social Hymenoptera: a meta-analysis

The study of sex allocation in social Hymenoptera (ants, bees,and wasps) provides an excellent opportunity for testing kin-selectiontheory and studying conflict resolution. A queen–workerconflict over sex allocation is expected because workers aremore related to sisters than to brothers, whereas queens areequally related to daughters and sons. If workers fully controlsex allocation, split sex ratio theory predicts that colonieswith relatively high or low relatedness asymmetry (the relatednessof workers to females divided by the relatedness of workersto males) should specialize in females or males, respectively.We performed a meta-analysis to assess the magnitude of adaptivesex allocation biasing by workers and degree of support forsplit sex ratio theory in the social Hymenoptera. Overall, variationin relatedness asymmetry (due to mate number or queen replacement)and variation in queen number (which also affects relatednessasymmetry in some conditions) explained 20.9% and 5% of thevariance in sex allocation among colonies, respectively. Theseresults show that workers often bias colony sex allocation intheir favor as predicted by split sex ratio theory, even iftheir control is incomplete and a large part of the variationamong colonies has other causes. The explanatory power of splitsex ratio theory was close to that of local mate competitionand local resource competition in the few species of socialHymenoptera where these factors apply. Hence, three of the mostsuccessful theories explaining quantitative variation in sexallocation are based on kin selection.     

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.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.     

Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density

Sexual size dimorphism is often a likely outcome of the interplay between natural selection and sexual selection, with female size dictated primarily by natural selection that maximizes fecundity and male size by sexual selection that maximizes reproductive opportunities. Attention to male fitness has focused heavily on direct male-male conflict selecting for superior male size and/or fighting ability, although male reproductive traits vary immensely among animals. An alternative, advanced by Michael Ghiselin, posits highly mobile dwarf males as a strategy for finding relatively immobile females in low-density populations. Adult male crab spiders Misumena vatia , sit-and-wait predators, are strikingly smaller, much more active, and relatively longer-legged than their females. This size difference results largely from males having two fewer instars than females, which simultaneously results in marked protandry. Populations of M. vatia often were small and of low density, with a female-biased sex ratio and an operational sex ratio that changed strikingly over the season. Sexual selection through scramble competition (locating the female first) should favour this suite of characters in males of low-density populations. Although direct male-male contests favoured large males, the low densities of adult males and the dispersed, relatively immobile females led to low levels of direct intrasexual contest. Females exaggerated the problem of males in finding them by providing few cues to their presence, a pattern consistent with indirect mate choice. In addition to favouring high mobility, scramble competition favoured males that selected flowers attracting many prey, the sites most often occupied by females.