SEX-RATIO MANIPULATION IN COLOR-BANDED POPULATIONS OF ZEBRA FINCHES

Significant correlations were found between attractiveness of leg-band color (determined by preference tests [Burley et al., 1982]) and sex ratio of offspring in two long-term breeding experiments involving zebra finches. In both experiments, birds with attractive band colors produced more same-sex offspring, while birds with unattractive band colors produced more opposite-sex offspring. The results of these experiments are consistent with those of a previous experiment (Burley, 1981). To explain the earlier results, I hypothesized that parents adjust their allocation to sons and daughters to produce offspring they “expect” to be most attractive. The purpose of such sex-ratio manipulation is to enhance fitness by the production of offspring with superior mate-getting opportunities. Two alternative hypotheses are presented here. One is that sex ratios change with parental age and/or experience. Evidence does not support this hypothesis. There were no temporal trends in sex ratio independent of band color. A second possibility is that sex ratios reflect differential parental ability to rear sons and daughters. This hypothesis cannot be conclusively tested on the basis of present evidence, but available evidence does not support it. Within color classes, weights of sons and daughters did not differ. Evidence indicates that parents effect secondary sex-ratio manipulation through the selective rejection of young, usually within six days of hatching. There is no evidence of manipulation prior to egg-laying. The costs associated with brood reduction probably set limits on the extent to which secondary manipulation can be profitably employed.     

Sex ratios and the evolution of eusociality in the hymenoptera

The potential role of sex ratio biassing in the evolution of worker behaviour in male-haploid hymenopteran insects is examined using a deterministic genetic model. The model is based on a bivoltine life cycle with annual colonies and it assumes five gene loci, each of them controlling a specific feature of the life cycle (particularly brood sex ratios). The hypothetical gene controlling worker behaviour is assumed to be expressed either in the mothers (parental manipulation models) or in the female offspring (offspring altruism models). The threshold of the worker efficiency required for the worker behaviour to evolve is 0.5 under parental manipulation and 1.0 under offspring altruism when the sex ratios are not skewed. Worker evolution by offspring altruism can evolve more easily if the first workers initially raise mainly female brood. With such a sex ratio bias, the threshold of worker efficiency allowing eusociality to evolve drops below 1.0, even close to 0.8. Worker evolution is also favoured by the elimination of males from the first of the two annually occurring offspring generations. It is concluded that the male-haploid sex determination can, through the control of sex ratios, play a significant role in the evolution of eusociality in hymenopteran insects.     

PARENTAL AGE,GAMETIC AGE,AND INBREEDING INTERACT TO MODULATE OFFSPRING VIABILITY IN DROSOPHILA MELANOGASTER

In principle, parental relatedness, parental age, and the age of parental gametes can all influence offspring fitness through inbreeding depression and the parental effects of organismal and postmeiotic gametic senescence. However, little is known about the extent to which these factors interact and contribute to fitness variation. Here, we show that, in Drosophila melanogaster, offspring viability is strongly affected by a three‐way interaction between parental relatedness, parental age, and gametic age at successive developmental stages. Overall egg‐to‐adult viability was lowest for offspring produced with old gametes of related, young parents. This overall effect was largely determined at the pupa–adult stage, although three‐way interactions between parental relatedness, parental age and gametic age also explained variation in egg hatchability and larva‐pupa survival. Controlling for the influence of parental and gametic age, we show that inbreeding depression is negligible for egg hatchability but significant at the larva–pupa and pupa–adult stages. At the pupa–adult stage, where offspring could be sexed, parental relatedness, parental age, and gametic age interacted differently in male and female offspring, with daughters suffering higher inbreeding depression than sons. Collectively, our results demonstrate that the architecture of offspring fitness is strongly influenced by a complex interaction between parental effects, inbreeding depression and offspring sex.     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

Nestling sex ratio of golden‐winged warblers Vermivora chrysoptera in an introgressed population

Sex ratio biases in avian species remain controversial, although several studies have documented apparent facultative adjustment of offspring sex ratios. While hybridizing pied and collared flycatchers have exhibited sex ratio skews that may be a response to sex‐based costs associated with hybridization, this appears not to be true of a hybridized population of blue‐winged Vermivora pinus and golden‐winged V. chrysoptera warblers. We examined the primary sex ratio of nestlings in a population of hybrid and introgressed golden‐winged warblers. The sex ratio of 298 nestlings from 81 nests in the population was approximately 50:50. We conducted paternity assignments and analyzed groups of nestlings with shared genetic parents (“genetic broods”) and found no difference from the expected binomial distribution, and no statistically significant relationship between parental species phenotype and nestling sex ratio. We saw no evidence of preferential production of male or female nestlings, and female hybrids were found to mate and breed in the population. This suggests that heterogametic (female) hybrids are both viable and fertile, and thus that Haldane's Rule does not apply to this system. While populations of hybridizing golden‐winged warblers should be monitored for evidence of costs of heterospecific pairings, it is unlikely that adjustment of sex ratios would be the form of compensation for sub‐optimal mating conditions. Our results provide support for the emerging hypothesis that hybrids suffer no disadvantage relative to golden‐winged and blue‐winged warblers.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

POTENTIAL MECHANISMS FOR SEX RATIO ADJUSTMENT IN MAMMALS AND BIRDS

Sex ratio skews in relation to a variety of environmental or parental conditions have frequently been reported among mammals and, though less commonly, among birds. However, the adaptive significance of such sex ratio variation remains unclear. This has, in part, been attributed to the absence of a low-cost physiological mechanism for sex ratio manipulation by the parent. It is shown here that several recent findings in reproductive biology are suggestive of many potential pathways by which gonadotropins and steroid hormones could interfere with the sex ratio at birth. And these hormone levels are well-known to be influenced by many parameters which have been invoked in correlating with offspring sex ratios. Hence, it is argued that the significant, but inconsistent sex ratio biases reported in mammalian and avian populations are coherent with current knowledge on reproductive physiology in those species. However, whether such variations can be viewed at as a consequence of physiological constraint or as adaptive sex ratio adjustment, has still to be determined.     

Parental care and adaptive brood sex ratio manipulation in birds

Under many circumstances, it might be adaptive for parents to bias the investment in offspring in relation to sex. Recently developed molecular techniques that allow sex determination of newly hatched offspring have caused a surge in studies of avian sex allocation. Whether females bias the primary brood sex ratio in relation to factors such as environmental and parental quality is debated. Progress is hampered because the mechanisms for primary sex ratio manipulation are unknown. Moreover, publication bias against non-significant results may distort our view of adaptive sex ratio manipulation. Despite this, there is recent experimental evidence for adaptive brood sex ratio manipulation in birds. Parental care is a particularly likely candidate to affect the brood sex ratio because it can have strong direct effects on the fitness of both parents and their offspring. We investigate and make predictions of factors that can be important for adaptive brood sex ratio manipulation under different patterns of parental care. We encourage correlational studies based on sufficiently large datasets to ensure high statistical power, studies identifying and experimentally altering factors with sex-differential fitness effects that may cause brood sex ratio skew, and studies that experimentally manipulate brood sex ratio and investigate fitness effects.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Sex ratio variation in mammals

Parents will increase their fitness by varying the sex ratio of their progeny in response to differences in the costs and benefits of producing sons and daughters. Sex differences in energy requirements or viability during early growth, differences in the relative fitness of male and female offspring, and competition or cooperation between siblings or between siblings and parents might all be expected to affect the sex ratio. Although few trends have yet been shown to be consistent, growing numbers of studies have demonstrated significant variation in birth sex ratios in non-human mammals. These are commonly cited as evidence of adaptive manipulation of the sex ratio. However, several different mechanisms may affect the birth sex ratio, and not all of them are likely to be adaptive. Valid evidence that sex ratio trends are adaptive must be based either on the overall distribution of those trends or on cases in which the sex ratio can be shown to vary with the relative fitness of producing sons and daughters. The distribution of observed sex ratio trends does not conform closely to the predictions of any single adaptive theory. Some recent studies, however, indicate that, within species, the sex ratio varies with the costs or benefits of producing male or female offspring.     

Effects of brood manipulation costs on optimal sex allocation in social hymenoptera

In eusocial Hymenoptera, queens and workers are in conflict over optimal sex allocation. Sex ratio theory, while generating predictions on the extent of this conflict under a wide range of conditions, has largely neglected the fact that worker control of investment almost certainly requires the manipulation of brood sex ratio. This manipulation is likely to incur costs, for example, if workers eliminate male larvae or rear more females as sexuals rather than workers. In this article, we present a model of sex ratio evolution under worker control that incorporates costs of brood manipulation. We assume cost to be a continuous, increasing function of the magnitude of sex ratio manipulation. We demonstrate that costs counterselect sex ratio biasing, which leads to less female-biased population sex ratios than expected on the basis of relatedness asymmetry. Furthermore, differently shaped cost functions lead to different equilibria of manipulation at the colony level. While linear and accelerating cost functions generate monomorphic equilibria, decelerating costs lead to a process of evolutionary branching and hence split sex ratios.     

Long-term fitness benefits of egg sex modification by the Seychelles warbler

Sex-ratio theory states that if the fitness costs to the parents of producing one offspring's sex relative to the other are higher, parents should discount these costs by producing fewer individuals of the more costly sex. In the co-operatively breeding Seychelles warbler (Acrocephalus sechellensis) mothers adaptively modify the sex of their single egg toward daughters, the helping sex, when living on territories with rich resources where helpers increase parental reproductive success, but toward sons, the dispersing sex, when living on territories where resources are scarce and/or no helping benefits accrue. By modifying offspring sex ratio, parents maximize their inclusive fitness benefits. Pairs in high-quality territories gained significantly more inclusive fitness benefits (through helping and reproducing offspring) from the production of daughters than from sons, and vice versa in low-quality territories (through reproducing offspring). Experimental manipulation of the offspring's sex shows that the consequences of sex allocation are adaptive for parents on high-quality territories. On high-quality territories with female production, breeding pairs raising step-daughters gained significantly higher inclusive benefits (through indirect and direct fitness gains) than by raising step-sons.     

Haldane rules: costs of outbreeding at production of daughters in sand lizards

Haldane's rule is one of the most widely applicable paradigms in evolutionary biology, stating that in species crossings, the heterogametic sex will suffer more severely in terms of sterility and inviability. We address this in a within‐species outbreeding situation by assessing the risk of producing inviable offspring depending on the sex ratio of the clutch produced in between‐population crossings in the laboratory. In crossings between male and female sand lizards (Lacerta agilis) from two different sampling regions, one in Sweden, one in central Europe, risk of gametic incompatibility is unaffected by outbreeding, but offspring from between‐population crossings show 300% higher malformation frequency and 10% lower hatching success. The risk of having inviable offspring increases with the production of daughters, i.e. the hemizygous sex in this species (ZW). Such sex‐specific genetic costs of offspring production need to be incorporated into life history ecology, e.g. sex allocation theory.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.     

Manipulation of offspring sex ratio by second-mated female house wrens

In 1973, Trivers and Willard proposed that offspring sex ratio should be associated with the quality of parental care likely to be provided to the offspring. We tested this hypothesis by comparing fledgling sex ratios in nests of first- and second-mated female house wrens (Troglodytes aedon). In our Wyoming population, second-mated females typically receive little or no male parental assistance and fledge fewer and lower-quality young compared with first-mated females. Assuming that being of lower quality has stronger negative effects on the future reproductive success of males than that of females in this polygynous population, we predicted that fledgling sex ratios in the nests of second-mated females would be female-biased compared with the fledgling sex ratios of first-mated females. Additionally, we asked whether any sex bias at fledging could have resulted from male-biased nestling mortality caused by sex-biased parental provisioning. As predicted, mean fledgling sex ratios in nests of second-mated females were more female-biased than fledgling sex ratios in nests of first-mated females. However, we found no evidence of either sex-biased nestling mortality or sex-biased parental provisioning. These findings suggest that females are responding to their status as second-mated females and to the associated low-quality parental care that their young are likely to receive by producing female-biased clutches rather than manipulating the offspring sex ratio through sex-biased nestling mortality.     

A trade-off between current and future sex allocation revealed by maternal energy budget in a small mammal

Sex-allocation theories generally assume differential fitness costs of raising sons and daughters. Yet, experimental confirmation of such costs is scarce and potential mechanisms are rarely addressed. While the most universal measure of physiological costs is energy expenditure, only one study has related the maternal energy budget to experimentally controlled offspring sex. Here, we experimentally test this in the bank vole (Myodes glareolus) by simultaneously manipulating the litter's size and sex ratio immediately after birth. Two weeks after manipulation, when mothers were at the peak of lactation and were pregnant with concurrent litters, we assessed their energy budget. We found that maternal food consumption and daily energy expenditure increased with the size of the litters being lactated. Importantly, the effects of offspring sex on energy budget depended on the characteristics of the simultaneously gestating litters. Specifically, the mothers nursing all-male litters and concurrently pregnant with male-biased litters had the highest energy expenditure. These had consequences for the next generation, as size of female offspring from the concurrent pregnancy of these mothers was compromised. Our study attests a higher cost of sons, consequently leading to a lower investment in them, and reveals the significance of offspring sex in moulding the trade-off between current and future maternal investment.     

Pair bond duration influences paternal provisioning and the primary sex ratio of brown thornbill broods

Parents should vary their level of investment in sons and daughters in response to the fitness costs and benefits accrued through male and female offspring. I investigated brood sex ratio biases and parental provisioning behaviour in the brown thornbill, Acanthiza pusilla, a sexually dimorphic Australian passserine. Parents delivered more food to male-biased than female-biased broods. However, factors determining parental provisioning rates differed between the sexes. Female provisioning rates were related to brood sex ratio in both natural and experimental broods with manipulated sex ratios. In contrast, male provisioning rates were not affected by brood sex ratio in either natural or experimental broods. However, males in established pairs provisioned at a higher rate than males in new pairs. Data on the sex ratio of 109 broods suggest that female brown thornbills adjust their primary sex ratio in response to pair bond duration. Females in new pairs produced broods with significantly fewer sons than females in established pairs. This pattern would be beneficial to females if the costs of rearing sons were higher for females in new than established pairs. This may be the case since females in new pairs provisioned experimental all-male broods at elevated rates. The condition of nestlings also tended to decline more in these all-male broods than in other experimental broods. This will have additional fitness consequences because nestling mass influences recruitment in thornbills. Female thornbills may therefore obtain significant fitness benefits from adjusting their brood sex ratio in response to the status of their pair bond. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Variation in offspring sex ratio of a long‐lived sexually dimorphic raptor,the Eastern Imperial Eagle Aquila heliaca

Sex ratio theory attempts to explain observed variation in offspring sex ratio at both the population and the brood levels. In the context of low‐fecundity organisms producing high‐investment offspring, the drivers of adaptive variation in sex ratio are incompletely understood. For raptors that display reverse sexual dimorphism (RSD), preferential allocation of resources to the putatively cheaper sex (male) may be a response to environmental, social or demographic stressors. To assess the extent of skew in offspring sex ratios and to evaluate possible dietary, environmental and demographic correlates of such skew to long‐lived RSD avian species, we evaluated the offspring sex ratio of 219 chicks from 119 broods in 30 territories of Eastern Imperial Eagles Aquila heliaca across 7 years and four regions at a nature reserve in Kazakhstan. Only in one region in 1 year of our study did the offspring sex ratio differ significantly from parity (10 males : 1 female in 11 territories). Whereas offspring sex ratios were independent of dietary diversity, precipitation, temperature and productivity, we found that year had a moderate effect on brood sex ratio within territories. Our results provide limited evidence of brood sex manipulation in these populations of Eastern Imperial Eagles, and no mechanistic insight into predictions associated with it. Stochastic variation is likely to explain much of the fluctuation we observed in sex ratios, but our observations are also consistent with the hypothesis that sex‐ratio manipulation may occur irregularly, in concurrence with atypical environmental or demographic conditions that fluctuate at a time scale longer than that of our 7‐year study.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.