Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum

The local-resource-competition hypothesis predicts that where philopatric offspring compete for resources with their mothers, offspring sex ratios will be biased in favour of the dispersing sex. This should produce variation in sex ratios between populations in relation to differences in the availability of resources for philopatric offspring. However, previous tests of local resource competition in mammals have used indirect measures of resource availability and have focused on sex-ratio variation between species or individuals rather than between local populations. Here, we show that the availability of den sites predicts the offspring sex ratio in populations of the common brushtail possum. Female possums defend access to dens, and daughters, but not sons, occupy dens within their mother's range. However, the abundances of possums in our study areas were determined principally by food availability. Consequently, in food-rich areas with a high population density, the per-capita availability of dens was low, and the cost of having a daughter should have been high. This cost was positively correlated with male bias in the sex ratio at birth. Low per capita availability of dens was correlated with male bias in the sex ratio at birth.     

Intralocus sexual conflict and offspring sex ratio

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.     

Paternal reproductive success drives sex allocation in a wild mammal

Parents should bias sex allocation toward offspring of the sex most likely to provide higher fitness returns. Trivers and Willard proposed that for polygynous mammals, females should adjust sex‐ratio at conception or bias allocation of resources toward the most profitable sex, according to their own body condition. However, the possibility that mammalian fathers may influence sex allocation has seldom been considered. Here, we show that the probability of having a son increased from 0.31 to 0.60 with sire reproductive success in wild bighorn sheep (Ovis canadensis). Furthermore, our results suggest that females fertilized by relatively unsuccessful sires allocated more energy during lactation to daughters than to sons, while the opposite occurred for females fertilized by successful sires. The pattern of sex‐biased offspring production appears adaptive because paternal reproductive success reduced the fitness of daughters and increased the average annual weaning success of sons, independently of maternal allocation to the offspring. Our results illustrate that sex allocation can be driven by paternal phenotype, with profound influences on the strength of sexual selection and on conflicts of interest between parents.     

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.     

Is offspring dispersal related to male mating status? An experiment with the facultatively polygynous spotless starling

Patterns of natal dispersal are generally sex‐biased in vertebrates, i.e. female‐biased in birds and male‐biased in mammals. Interphyletic comparisons in mammals suggest that male‐biased dispersal occurs in polygynous and promiscuous species where local mate competition among males exceeds local resource competition among females. However, few studies have analysed sex‐biased patterns of dispersal at the individual level, and facultatively polygynous species might offer this opportunity. In the spotless starling, polygynous males exhibit their mating status during courtship carrying higher amounts of green plants to nests than monogamous males. We experimentally incorporated green plants to nests during four years to analyse long‐term consequences on breeding success and offspring recruitment rates. We unexpectedly found that experimental sons recruited farther than experimental daughters, while control daughters recruited farther than control sons. A similar pattern was found using observational information from eight years. We discuss this result in the context of local competition hypothesis and speculate that sons dispersed farther from nests controlled by polygynous males to avoid competition with relatives. The amount of green plants in nests affects female perception of male attractiveness and degree of polygyny, although little is known about proximate mechanisms linking this process with the offspring dispersal behaviour. Our results support the idea that male‐biased dispersal is related to polygyny in a facultatively polygynous bird.     

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.     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.     

The evolution of sex ratios and sex-determining systems

Sex determination is a fundamental process governed by diverse mechanisms. Sex ratio selection is commonly implicated in the evolution of sex-determining systems, although formal models are rare. Here, we argue that, although sex ratio selection can induce shifts in sex determination, genomic conflicts between parents and offspring can explain why single-factor systems (e.g. XY/XX or ZW/ZZ) are common even in species that experience selection for biased sex ratios. Importantly, evolutionary shifts in sex determination do not always result in the biased production of sons and daughters sensu sex ratio theory. Thus, equal sex ratios might be an emergent character of sex-determining systems even when biased sex ratios are favored by selection.     

Variation in offspring sex ratio in women of differing social status

Since Trivers and Willard first postulated 15 years ago that offspring sex ratio might be adaptively manipulated by parents of mammalian species as well as hymenoptera, evidence has been accumulating in support of this hypothesis. Research suggests that female mammals are able to manipulate the secondary (birth) sex ratio of their offspring based upon their own social status and/or access to resources. This ability is thought to procure a reproductive advantage by maximizing number of grandchildren. This article reports, in further confirmation of the Trivers and Willard hypothesis, the apparent sex ratio manipulation of offspring by human females of differing social status, in a polygynous, naturally fertile population, the nineteenth-century Mormons.     

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1.  Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment.
2.  We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus , by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by −2/+2 pups) of their offspring in a laboratory setting.
3.  We found that mothers clearly biased their allocation to female rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring.
4.  The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial.
5.  The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.     

A theory of gene-culture coevolution of parental preference and sex ratio in humans

A theory on the evolution of human primary sex ratio is proposed. Effects of parental preference for sons, reflected in birth control based on offspring sex ratio and female biased infanticide, on the evolution of primary sex ratio are analyzed. Both are shown to select for female bias in primary sex ratio. The gene-culture coevolution of female infanticide and primary sex ratio is also studied and it is shown that female infanticide develops more in societies in which the father plays a more important role in the transmission of culture than the mother does.     

Hatching sex ratio and sex specific chick mortality in common terns Sterna hirundo

Bias in sex ratios at hatching and sex specific post hatching mortality in size dimorphic species has been frequently detected, and is usually skewed towards the production and survival of the smaller sex. Since common terns Sterna hirundo show a limited sexual size dimorphism, with males being only about 1–6% larger than females in a few measurements, we would expect to find small or no differences in production and survival of sons and daughters. To test this prediction, we carried out a 2-year observational study on sex ratio variation in common terns at hatching and on sex specific post hatching mortality. Sons and daughters hatched from eggs of similar volume. Post hatching mortality was heavily influenced by hatching sequence. In addition, we detected a sex specific mortality bias towards sons. Overall, hatching sex ratio and sex specific mortality resulted in fledging sex ratios 8% biased towards females. Thus, other reasons than body size may be influencing the costs of rearing sons. Son mortality was not homogeneous between brood sizes, but greater for two-chick broods. Since adults rearing two-chick broods were younger, lighter and bred consistently later than those rearing three-chick broods, it is suggested that lower capacity of two-chick brood parents adversely affected offspring survival of sons. Though not significantly, two-chick broods tended to be female biased at hatching, perhaps to counteract the greater male-biased nestling mortality. Thus, population bias in secondary sex ratio is not limited to strongly size dimorphic species, but species with a slight sexual size dimorphism can also show sex ratio bias through a combination of differential production and mortality of sons and daughters.     

Better‐surviving barn swallow mothers produce more and better‐surviving sons

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long‐term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

Maternal Investment of the Virunga Mountain Gorillas

The Trivers & Willard hypothesis (TWH) predicts that females with more resources should bias their maternal investment toward offspring of the sex that is most likely to benefit from those additional resources. This paper examines the sex allocation of 61 female mountain gorillas (Gorilla beringei beringei) of the Virunga volcanoes, Rwanda from 1967 to 2004. Like most highly dimorphic, polygynous mammals, mountain gorillas are expected to show greater variance in reproductive success among males than females, so mothers in good condition should bias their investment toward sons. Using dominance rank as the indicator of maternal condition, the TWH was tentatively supported by our results with interbirth intervals (IBI). Dominant mothers had longer IBI following the birth of sons, relative to the longer IBI that subordinate mothers had with daughters. In contrast, maternal condition did not have a significant effect on birth sex ratios. We also found no significant relationships with other variables that might influence birth sex ratios (e.g., maternal age, parity, or group size), and the overall birth sex ratio was not significantly different from a 50:50 split. Collectively, our results suggest that female mountain gorillas do not control the sex ratio of their offspring at birth, but they may adjust their subsequent maternal investment. This conclusion is consistent with recurring questions about whether any adjustments in birth sex ratios occur in primates.     

A Trivers-Willard Effect in Contemporary Humans: Male-Biased Sex Ratios among Billionaires

Background

Natural selection should favour the ability of mothers to adjust the sex ratio of offspring in relation to the offspring''s potential reproductive success. In polygynous species, mothers in good condition would be advantaged by giving birth to more sons. While studies on mammals in general provide support for the hypothesis, studies on humans provide particularly inconsistent results, possibly because the assumptions of the model do not apply.

Methodology/Principal Findings

Here, we take a subset of humans in very good condition: the Forbe''s billionaire list. First, we test if the assumptions of the model apply, and show that mothers leave more grandchildren through their sons than through their daughters. We then show that billionaires have 60% sons, which is significantly different from the general population, consistent with our hypothesis. However, women who themselves are billionaires have fewer sons than women having children with billionaires, suggesting that maternal testosterone does not explain the observed variation. Furthermore, paternal masculinity as indexed by achievement, could not explain the variation, since there was no variation in sex ratio between self-made or inherited billionaires.

Conclusions/Significance

Humans in the highest economic bracket leave more grandchildren through sons than through daughters. Therefore, adaptive variation in sex ratios is expected, and human mothers in the highest economic bracket do give birth to more sons, suggesting similar sex ratio manipulation as seen in other mammals.     

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.     

Maternal Testosterone and Offspring Sex-Ratio in Birds and Mammals: A Meta-Analysis

Sex allocation theory predicts that parents should bias offspring sex to maximize their fitness in a given context. Quantifying the fitness benefits of offspring sex-ratio biases would be facilitated by a better knowledge of their underlying mechanism(s) and associated costs. The hypothesis that steroid hormones are involved in sex determination has gained in popularity recently. Being influenced by external stimuli and involved in a range of physiological processes, they could be a ubiquitous mediator of environmental conditions influencing sex-ratio with low fitness costs. Previous studies indicated that higher maternal testosterone levels led to the overproduction of sons around conception in both birds and mammals. We conducted a systematic review (including meta-analysis) of these studies and, as predicted, we found a weak positive and significant overall effect of maternal testosterone on the proportion of sons. Neither taxa, nor the type of study (experimental/observational), or the timing of timing testosterone manipulation/measure were significant predictors of offspring sex-ratio, which may be explained by low statistical power in addition to low variability between effect sizes. Our meta-analysis provides evidence for a general positive influence of maternal testosterone around conception on the proportion of sons across birds and mammals, although less confidently so for the latter. It begs for more large-scale experimental studies, especially on mammals, and ideally in the wild. It may also have some important consequences for the poultry industry.     

Sex allocation and interactions between relatives in the bean beetle, Callosobruchus maculatus

When a small number of females contribute offspring to a discrete mating group, sex allocation (Local Mate Competition: LMC) theory predicts that females should bias their offspring sex ratio towards daughters, which avoids the fitness costs of their sons competing with each other. Conversely, when a large number of females contribute offspring to a patch, they are expected to invest equally in sons and daughters. Furthermore, sex ratios of species that regularly experience variable foundress numbers are closer to those predicted by LMC theory than species that encounter less variable foundress number scenarios. Due to their patterns of resource use, female Callosobruchus maculatus are likely to experience a broad range of foundress number scenarios. We carried out three experiments to test whether female C. maculatus adjust their sex ratios in response to foundress number and two other indicators of LMC: ovipositing on pre-parasitised patches and ovipositing with sisters. We did not find any evidence of the predicted sex ratio adjustment, but we did find evidence of kin biased behaviour.