Facultative Sex Ratio Research Articles

Offspring sex ratios are stable across the life course in Drosophila simulans.

Within populations, adult sex ratios influence population growth and extinction risk, mating behaviours and parental care. Sex ratio adjustment can also have pronounced effects on individual fitness. Accordingly, it is important that we understand how often, and why, offspring sex ratios deviate from parity. In Drosophila melanogaster, females appear to improve their fitness by producing fewer sons when paired with older males. However, facultative sex ratio adjustment in D.melanogaster is controversial, and our understanding of how sex ratio skew affects fitness is hampered by pronounced sexual conflict in this species. Additionally, it is unclear whether maternal age or quality interacts with paternal age to influence offspring sex ratios. Here, we test whether offspring sex ratios vary as a function of maternal quality, and maternal and paternal age in Drosophila simulans, a sister species of D.melanogaster that lacks overt sexual conflict. We find that offspring sex ratios are slightly male-biased overall, but constant across the female life course, and independent of female quality, or paternal age. To really understand if, how and when females skew offspring sex ratios, we need studies linking offspring sex ratios to paternal and maternal phenotypes that are predicted to shift optimal investment in sons and daughters.

Frequency-dependent two-sex models: a new approach to sex ratio evolution with multiple maternal conditions.

Mothers that experience different individual or environmental conditions may produce different proportions of male to female offspring. The Trivers‐Willard hypothesis, for instance, suggests that mothers with different qualities (size, health, etc.) will use different sex ratios if maternal quality differentially affects sex‐specific reproductive success. Condition‐dependent, or facultative, sex ratio strategies like these allow multiple sex ratios to coexist within a population. They also create complex population structure due to the presence of multiple maternal conditions. As a result, modeling facultative sex ratio evolution requires not only sex ratio strategies with multiple components, but also two‐sex population models with explicit stage structure. To this end, we combine nonlinear, frequency‐dependent matrix models and multidimensional adaptive dynamics to create a new framework for studying sex ratio evolution. We illustrate the applications of this framework with two case studies where the sex ratios depend one of two possible maternal conditions (age or quality). In these cases, we identify evolutionarily singular sex ratio strategies, find instances where one maternal condition produces exclusively male or female offspring, and show that sex ratio biases depend on the relative reproductive value ratios for each sex.

Paroxetine exposure skews litter sex ratios in mice suggesting a Trivers-Willard process.

While conducting a toxicity assessment of the antidepressant paroxetine (Paxil®), in wild-derived mice (Mus musculus), we observed that exposed dams (P0) produced female biased litters (32:68 M:F). Though numerous experimental manipulations have induced sex ratio bias in mice, none have assessed the fitness of the offspring from these litters relative to controls. Here, we retrospectively analyze experimentally derived fitness data gathered for the purpose of toxicological assessment in light of 2 leading hypothesis (Trivers-Willard hypothesis [TWH] and cost of reproduction hypothesis [CRH]), seeking to test if this facultative sex ratio adjustment fits into an adaptive framework. Control F1 males were heavier than F1 females, but no differences in mass were detected between exposed F1 males and females, suggesting that exposed dams did not save energy by producing fewer males, despite producing 29.2% lighter litters relative to controls. F1 offspring of both treatments were released into seminatural enclosures where fitness was quantified. In enclosures, the relative reproductive success of F1-exposed males (compared with controls) was reduced by ~20% compared with the relative reproductive success of F1-exposed females. Thus, exposed dams increased their fitness by adjusting litters toward females who were less negatively affected by the exposure than males. Collectively, these data provide less support that the observed sex ratio bias results in energetic savings (CRH), and more support for the TWH because fitness was increased by biasing litters toward female offspring. These mammalian data are unique in their ability to support the TWH through the use of relevant fitness data.

Temporal variation in sex allocation in the mealybug Planococcus citri: adaptation, constraint, or both?

Sex ratio theory has been very successful in predicting under which circumstances parents should bias their investment towards a particular offspring sex. However, most examples of adaptive sex ratio bias come from species with well-defined mating systems and sex determining mechanisms, while in many other groups there is still an on-going debate about the adaptive nature of sex allocation. Here we study the sex allocation in the mealybug Planococcus citri, a species in which it is currently unclear how females adjust their sex ratio, even though experiments have shown support for facultative sex ratio adjustment. Previous work has shown that the sex ratio females produce changes over the oviposition period, with males being overproduced early and late in the laying sequence. Here we investigate this complex pattern further, examining both the robustness of the pattern and possible explanations for it. We first show that this sex allocation behaviour is indeed consistent across lines from three geographical regions. Second, we test whether females produce sons first in order to synchronize reproductive maturation of her offspring, although our data provide little evidence for this adaptive explanation. Finally we test the age at which females are able to mate successfully and show that females are able to mate and store sperm before adult eclosion. Whilst early-male production may still function in promoting protandry in mealybugs, we discuss whether mechanistic constraints limit how female allocate sex across their lifetime.

CONTEXT-DEPENDENT SEX ALLOCATION: CONSTRAINTS ON THE EXPRESSION AND EVOLUTION OF MATERNAL EFFECTS

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates.

Facultative Sex Ratio Adjustment in Natural Populations of Wasps: Cues of Local Mate Competition and the Precision of Adaptation

Sex ratio theory offers excellent opportunities to examine the extent to which individuals adaptively adjust their behavior in response to local conditions. Hamilton's theory of local mate competition, which predicts female-biased sex ratios in structured populations, has been extended in numerous directions to predict individual behavior in response to factors such as relative fecundity, time of oviposition, and relatedness between cofoundresses and between mates. These extended models assume that foundresses use different sources of information, and they have generally been untested or have only been tested in the laboratory. We use microsatellite markers to describe the wild oviposition behavior of individual foundresses in natural populations of the parasitoid wasp Nasonia vitripennis, and we use the data collected to test these various models. The offspring sex ratio produced by a foundress on a particular host reflected the number of eggs that were laid on that host relative to the number of eggs that were laid on that host by other foundresses. In contrast, the offspring sex ratio was not directly influenced by other potentially important factors, such as the number of foundresses laying eggs on that patch, relative fecundity at the patch level, or relatedness to either a mate or other foundresses on the patch.

You are what your mother eats: evidence for maternal preconception diet influencing foetal sex in humans.

Facultative adjustment of sex ratios by mothers occurs in some animals, and has been linked to resource availability. In mammals, the search for consistent patterns is complicated by variations in mating systems, social hierarchies and litter sizes. Humans have low fecundity, high maternal investment and a potentially high differential between the numbers of offspring produced by sons and daughters: these conditions should favour the evolution of facultative sex ratio variation. Yet little is known of natural mechanisms of sex allocation in humans. Here, using data from 740 British women who were unaware of their foetus's gender, we show that foetal sex is associated with maternal diet at conception. Fifty six per cent of women in the highest third of preconceptional energy intake bore boys, compared with 45% in the lowest third. Intakes during pregnancy were not associated with sex, suggesting that the foetus does not manipulate maternal diet. Our results support hypotheses predicting investment in costly male offspring when resources are plentiful. Dietary changes may therefore explain the falling proportion of male births in industrialized countries. The results are relevant to the current debate about the artificial selection of offspring sex in fertility treatment and commercial 'gender clinics'.

A Test of the Trivers-Willard Hypothesis with Three Samples of High-achieving Men: a Tenuous Fit for an Altricial, Fathering-intensive Species

The Trivers-Willard hypothesis argues for a facultative (secondary) sex ratio in sexually reproducing species. To wit: Given that males have a potentially greater variance in numbers of offspring than do females, mothers would bias toward sons if the rearing environment for the son would be superior to that of competitors and, thus, give the son an added ply of attractiveness to females. Conversely, mothers would bias toward daughters if the rearing environment of the daughter would be inferior to that of competitors. A highly attractive daughter portends many grandchildren, but not as many as her equally attractive brother, and fewer grandchildren, but not as few as her unattractive brother, if she is unattractive. Data from three samples of high-achieving men offer more support for Fisher's basic theory than for the Trivers-Willard hypothesis. It is suggested that a highly altricial and fathering-intensive species, e.g. Homo sapiens, would render the Trivers-Willard hypothesis problematic. Key Words: Trivers-Willard hypothesis; Fisher; Facultative (secondary) sex ratio; Social father. The great tragedy of science the slaying of a beautiful hypothesis by an ugly fact - Thomas Huxley Tis a happy thing to be the father unto many sons - William Shakespeare (Henry VI) The gender of an organism is an important, if not decisive, predictor of that organism's life-chances and, thereby, life-trajectory. Humans are neither an exception nor transcendent. This article examines two ideas which provide a context to the sex ratio at birth (secondary sex ratio) . Facultative Sex Ratio: Fisher Fisher (1930) developed a theory stating that the gender of an individual in a sexually reproducing species would not follow a coin flip analogy across the population /specie s. In essence, total parenting energies in rearing their young would be equally divided between the two genders. Thus, if an individual in one gender - e.g. female - required, on average, more energy to rear than an individual in the alternate gender - e.g. male - then a greater number of the less costly gender would be born (if not conceived, primary sex ratio). Accordingly, the total energy of rearing the two genders would reach equilibrium at birth. Given that males, as a class, are more vulnerable to lethal agents prior to puberty, a cohort of males would require less energy than a cohort of their less vulnerable sisters. Hence, we would expect that more sons are born than daughters, and such is the case. Across the world's community of populations, the secondary sex ratio is approximately 105 sons born per 100 daughters (Central Intelligence Agency 2008). ' This biased ratio is independent of virtually any plausible variable. For the U.S., the reported sex ratio at birth has held steady for decades (U.S. Bureau of the Census, 2008). Facultative Sex Ratio: Trivers-Willard Trivers & Willard (1973) refined this core idea with the following model: Given that (1) males generally invest less time and resources in the rearing of their offspring than do females, and that (2) males can be much more prolific than females, i.e. the variance of male reproductive success can be greater than that of the female, then a route to large numbers of descendants by a parent would be to rear sons who would be highly attractive to many females. However, a son is somewhat of a gamble. If he is unwaveringly unattractive to females, the son may well remain chaste and celibate throughout his life with no descendants for his parents at all. Compared to their brothers, females are more limited in the potential numbers of children they can procreate. But daughters are less of a gamble. Even unattractive females have little trouble finding suitors who will mate with them. Hence, a daughter is more of a guarantee of some descendants, but is less capable of generating as large a number of descendants as is her brother: her mother's son. …

Facultative sex ratio adjustment by western bluebird mothers with stay-at-home helpers-at-the-nest

Although population sex ratios rarely deviate from unity, the sex ratio of individual mothers should be labile, allowing them to bias their sex ratios in favour of the more successful sex when they can expect a difference in the mean reproductive value of their daughters and sons. Just how mothers should bias sex allocation is particularly complicated in cooperative breeders, because the adaptive sex ratio may be influenced by conflicting impacts of helpers on their parents' fitness via ‘local resource enhancement’ and ‘local resource competition’. In western bluebirds, Sialia mexicana, breeding-age helpers-at-the-nest are exclusively male and increase their parents' nesting success in the current year. As such, they are viewed as helpers, not hinderers, even though by failing to gain a breeding position they reduce their parents' annual inclusive fitness below that of parents with a breeding son. In this study, I tested the hypothesis that nonbreeding, stay-at-home helpers indicate poor breeding prospects for locally competing sons, and investigated one prediction of this hypothesis that such helpers also indicate a tendency for parents to produce substandard sons. A female removal experiment showed that female mates were in short supply. Pairs had daughter-biased broods when they had a stay-at-home helper son that failed to get a mate in the first place, but not when they had a helper that had been breeding on his own, but returned home to help sometime after his mother finished laying her eggs. Stay-at-home sons were not developmentally delayed relative to breeders of the same cohort, suggesting that helpers may not be inferior to breeders. Although the population sex ratio fluctuates about unity, a multiyear data set showed a negative relationship between the frequency of helping and the annual brood sex ratio for the population. These results suggest that local resource competition outweighs local resource enhancement in driving individual and population sex ratio variation in western bluebirds, a pattern that would not be predicted based on the simple question of whether helpers help or hinder at the nest.

Wasp sex ratios when females on a patch are related

Optimality theory of sex allocation in structured populations has proved remarkably successful in explaining patterns of facultative sex ratio behaviour in numerous species. Extensions to the basic theory have included more specific aspects of species biology, including the relatedness of interacting individuals. We considered the sex ratio decisions made by female Nasonia vitripennis wasps when they were ovipositing on a patch with either relatives or nonrelatives. Theory predicts that females should produce more female-biased sex ratios when ovipositing with relatives, for example sisters, than with unrelated females. This is because related females should limit the level of local mate competition between their sons for female partners. Contrary to theory, two experiments showed that female sex ratio behaviour was unaffected by the relatedness of their oviposition partner, and was also unrelated to an environmental cue that could signal relatedness, i.e. whether females responded differently to sisters emerging from the same or a different host. Instead, in both experiments, we found that only wasp strain significantly influenced sex ratio. A meta-analysis of studies conducted on a range of species on the effects of the relatedness of oviposition partners on sex ratio failed to show the predicted pattern. We discuss why females appear to behave in a maladaptive way when allocating sex under these conditions, and suggest that weak selection and/or conflict between females over optimal sex ratios may influence the evolution of kin discrimination.

Facultative sex ratio adjustment in response to male tarsus length in the Varied Tit Parus varius

During the last decade, evidence from a number of studies has suggested systematic deviations from a 1 : 1 primary sex ratio in birds, in spite of the fact that birds have chromosomal sex determination systems; the mechanism of sex allocation is not fully understood. However, it still remains uncertain whether adaptive manipulations of primary sex ratio occur, especially in Parus species. We studied sex ratio variation in the Varied Tit Parus varius, which is a socially monogamous species similar to the Great Tit P. major and the Blue Tit P. caeruleus. In total, 362 chicks that hatched from 72 broods over 3 years were sexed. Of all nestlings, 51.9% (188/362) were male. The nestling sex ratio did not differ significantly from unity. However, the proportion of sons in each brood was significantly and positively related to the father's tarsus length. This corresponds with our predictions, given that larger males have higher resource holding potential if tarsus length is a heritable character between fathers and sons.

Further evidence for Emlen's hypothesis from two parrot species

Recent studies have demonstrated that chromosomal sex determination does not necessarily prevent facultative sex ratio adjustment in birds. However, it is not known how the sex ratio adjustment is achieved. One hypothesis states that birds might adjust the sex of the first‐laid egg only, but published data from Eclectus parrots indicated that the sex ratio of second‐laid eggs was also biased. In broods where two young were fledged together, the two nestlings were often of the same sex. According to a re‐analysis, this finding, however, was not significant. In addition, new data from German breeders are presented and, according to these data, there is no evidence for a biased sex ratio in second‐laid eggs either. Furthermore, I analyse recently published data from kakapo. In this species there is a significantly biased sex ratio for the first eggs, but again not for later eggs. Thus, the sex ratio adjustment in both parrot species could arise through post‐ovulation adjustment according to Emlen's hypothesis.

Nestling sex ratio variation in the cooperatively breeding acorn woodpecker ( Melanerpes formicivorus )

We examined sex ratio variation in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) over a 27-year period in central coastal California. The sex ratio of eggs is even or possibly biased toward females. However, hatching asynchrony and brood reduction differentially favor the slightly larger males such that the sex ratio when young become self-sufficient is 54.0% males, slightly but significantly different from 50:50. This bias, or at least the differential mortality that produces it, does not appear to be explainable by any of the major hypotheses for an overall sex bias. These include the repayment model, local resource competition, and sexual size dimorphism, all of which predict a female bias or a male bias significantly smaller than that observed. On an individual level, we found no evidence for facultative sex ratio manipulation related to annual differences in the acorn crop, apparent seasonal declines in food availability, or differences in territory quality. We also found no evidence for a non-binomial distribution of sexes within broods despite the potential fitness benefits of creating large coalitions of same-sexed siblings. Males inherit their natal territories more frequently than do females, and we speculate that birds may invest more in sons either to increase the probability that they will be able to pass along their territory to their descendants or to facilitate their sons' ability to compete as future cobreeders. Alternatively, acorn woodpeckers may be unable to fully compensate for the ancillary bias caused by differential juvenile survivorship, leading to unequal investment in the sexes contrary to the prediction of Fisher. Opposite to what has been found in other birds and mammals, the faster growth and larger size of male nestlings appears to confer a survival benefit rather than a cost.

Is variation in brood sex ratios adaptive in the great tit (Parus major)?

Life-history theory predicts skewed offspring sex ratios in a range of situations in which the costs and benefits of producing the two sexes differ. In recent years, many studies have demonstrated biased sex ratios in a variety of bird species. However, many of these investigations have been based on small sample sizes, on data from a single year, or both. Using a recently developed polymerase chain reaction-based molecular DNA technique, 912 great tit (Parus major) nestlings from 118 broods in 5 different years were sexed. As found in a number of previous studies on the same species, there were significant predictors of offspring sex ratio in individual years. However, there were no consistent trends across years, and none of the measured variables significantly predicted sex ratio over all years combined. Furthermore, brood sex ratio of the population did not depart from the expected binomial distribution. Although there are theoretical advantages to manipulating the sex ratio in this and other species, the physiological mechanism by which it is achieved in birds remains obscure. We argue that data from several years are needed to confirm whether facultative sex ratio manipulation is a consistent breeding strategy used by birds.

Unexpected offspring sex ratios in response to habitat quality in a size-dimorphic bark beetle

Facultative sex ratio manipulation has been examined in a limited number of diploid species, mainly vertebrates. We tested the prediction that mothers would preferentially place males in conditions conducive to large size in the diploid pine engraver bark beetle, Ips pini. In this species, males are the larger sex and therefore male reproductive success was expected to be more dependent on body size than female reproductive success. Because body size is largely environmentally determined in bark beetles, mothers were expected to alter sex ratios in response to habitat quality. Contrary to predictions, offspring sex ratios tended to be more female biased in situations conducive to large offspring size than in situations producing offspring of small size. We were able to rule out nonadaptive explanations such as differential mortality or development times of males and females, suggesting that the observed pattern is adaptive. This study provides a rare example of sex ratio manipulation in diploid insects. However, the unexpected direction of sex ratio biases suggests that daughters gain a yet unknown benefit from being reared in high-quality conditions that surpasses the fitness that would be gained from producing relatively larger sons.

Studies of Sex Allocation in Birds and Molecular Tools for Sex Identification

The recent development of molecular methods for sex identification makes large-scale studies of sex allocation in birds possible. This review identifies three types of sex allocation studies of birds. These relate either to the population primary sex ratio, the facultative manipulation of the sex ratio, or to sex-skewed provisioning. Many recent studies have suggested that facultative sex ratio manipulation may be more widespread among birds than has previously been considered. In contrast, only a few studies have been made of the population primary sex ratio, and of sexskewed provisioning. Despite all these studies, the mechanism for adjusting the sex ratio remains a mystery. In particular, estimating the cost of making sex ratio adjustments is indispensable for quantitative predictions of sex allocation. The relationships between the three aspects outlined above have not yet been sufficiently clarified. In both Budgerigars Melopsittacus undulatus and Great Reed Warblers Acrocephalus arundinaceus, fathers provide extra-feeding for a certain sex of offspring, while mothers manipulate the primary sex ratio. I suggest that the distinction between the sexes in terms of providing extra-feeding or manipulating the sex ratio, may in fact affect the population primary sex ratio and cause a bias towards the sex for which fathers provide extra-feeding.

Maternal investment and factors affecting offspring size in polar bears (Ursus maritimus)

AbstractWe examined data on live‐captured polar bears (Ursus maritimus) from western Hudson Bay relative to differential maternal investment and facultative sex ratio theory. In spring, shortly after den emergence, we found no differences in mass or body length of cubs in litters of one or two. In triplet litters captured in spring, male cubs were larger than females in both mass and body length, possibly due to sibling competition for limited maternal resources. In cubs captured during autumn, sex‐based differences in mass and body length were found only in litters of one with males larger than females. Yearling males captured in autumn were heavier and longer than females in litters of one and two. In twin litters of one male and one female cub in spring and autumn, we found no differences in mass or body length. Except singleton female cubs in spring and female and male triplets in spring, cub and yearling mass were correlated with maternal mass. Mothers with singletons in spring were more likely to have male cubs but, in general, there was little evidence to suggest that mass or age of mothers influenced offspring sex. Litter size, maternal mass, and maternal age all influenced cub and yearling size, but offspring sex was less important. Results suggest that female polar bears do not normally invest differentially between offspring of different sexes except in triplet litters in spring.

Maternal investment and factors affecting offspring size in polar bears (Ursus maritimus)

We examined data on live-captured polar bears (Ursus maritimus) from western Hudson Bay relative to differential maternal investment and facultative sex ratio theory. In spring, shortly after den emergence, we found no differences in mass or body length of cubs in litters of one or two. In triplet litters captured in spring, male cubs were larger than females in both mass and body length, possibly due to sibling competition for limited maternal resources. In cubs captured during autumn, sex-based differences in mass and body length were found only in litters of one with males larger than females. Yearling males captured in autumn were heavier and longer than females in litters of one and two. In twin litters of one male and one female cub in spring and autumn, we found no differences in mass or body length. Except singleton female cubs in spring and female and male triplets in spring, cub and yearling mass were correlated with maternal mass. Mothers with singletons in spring were more likely to have male cubs but, in general, there was little evidence to suggest that mass or age of mothers influenced offspring sex. Litter size, maternal mass, and maternal age all influenced cub and yearling size, but offspring sex was less important. Results suggest that female polar bears do not normally invest differentially between offspring of different sexes except in triplet litters in spring.

Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata

Where maternal condition affects condition and reproductive potential of offspring differentially with respect to sex, mothers in relatively good condition should produce more of the sex whose fitness is more dependent on condition. We experimentally manipulated body-condition in unmated zebra finches by feeding them for three months on high- or low-quality diets. Birds were then allowed to breed, while keeping the same diets. Females on the lower quality diet were in better condition and hatched significantly more males than females. Poorer condition females hatched an equal sex ratio. Chicks fed on the low-quality diet, but not on the high-quality diet, showed female-biased mortality. These results show that facultative sex ratio manipulation and sex-biased mortality can act together to produce extreme sex ratios in this vertebrate.

Weinberg's rule and facultative sex ratios

The author refers to a paper by Coney and Mackey entitled `Weinbergs Rule versus facultative sex ratio...and argues that the number of mechanisms underlying variations in mammalian sex ratio at birth (e.g. steroid hormone levels) is presumably much smaller than the number of variables by which it varies. He suggests that research strategy would dictate investigating whether these underlying mechanisms (rather than the ad hoc variables) operate in conformity with facultative theory. (EXCERPT)