Low serum vitamin A mothers breastfeed daughters more often than sons in drought-ridden northern Kenya: a test of the Trivers–Willard hypothesis

The Trivers–Willard hypothesis predicts that natural selection should favor unequal parental investment between daughters and sons based upon maternal condition and offspring reproductive potential. Specifically, it predicts that mothers in good condition should increase investment toward sons, while mothers in poor condition should favor daughters. Previous tests of the hypothesis in human populations overwhelmingly focused on economic resources as maternal condition indicators. We test the Trivers–Willard hypothesis using maternal nutrition—energy and vitamin A status representing macro- and micronutrition, respectively—as the indicator for maternal condition, with breastfeeding frequency recalls serving as the indicator for parental investment. Data from exclusively breastfeeding mothers (n=83) in drought-ridden Ariaal agropastoral villages of northern Kenya were used to test the hypothesis that mothers in poor condition will breastfeed daughters more frequently than sons. Poor condition was defined as having a body mass index <18.5 or serum retinol (vitamin A) concentration <1.05 µmol/l. A linear regression model was applied using breastfeeding frequency as the dependent variable and respective maternal condition, infant's sex, and the maternal condition–infant's sex interaction as the predictors, controlling for covariates. Results supported the hypothesis only in the vitamin A model which predicts that low-vitamin-A mothers breastfeed daughters significantly more frequently than sons (11 vs. 6 times/day), while vitamin-A-sufficient mothers breastfeed daughters and sons equivalently (9 times). These results indicate that maternal nutritional status, particularly micronutrient status, can contribute to the investigation of the evolutionary hypothesis of sex-biased parental investment.     

Trivers-Willard effect in contemporary North American society.

The Trivers-Willard hypothesis joins the ideas of R.A. Fisher and A.J. Bateman to model parental investment strategies. Trivers and Willard argue that any overall investment bias favoring either daughters or sons would be maladaptive. Nevertheless, they suggest that, in effectively polygynous species, more complex, conditional sex biases could be adaptive. In particular, they predict that parents in good condition will bias their investment toward sons and that parents in poor condition will bias their investment toward daughters. Among a sample of approximately 900 U.S. mothers we examined several measures of maternal investment including birth weight, interbirth interval and lactational commitment. Maternal condition was assessed by income and by the presence or absence of a coresident adult male. Some measures of investment (five of 14 statistical tests) showed marked and significant sex-by-condition interactions of the type and in the direction predicted by Trivers and Willard; none showed significant effects in the opposite direction. No conscious mediation is required to produce the observed investment patterns.     

The Trivers–Willard hypothesis of parental investment: No effect in the contemporary United States

The Trivers–Willard hypothesis (TWH) predicts that parents will bias their sex ratio toward sons when in good condition and toward daughters when in poor condition. Many human studies have tested the related hypothesis that parents' bias allocation of resources to existing sons and daughters according to the same principle. The present study used time diary and self-report data from the parents of 3200 children in the US to test the hypothesis that as status increases, parents will allocate more resources to sons vs. daughters. It finds no evidence that higher-status parents invest more in sons or that lower status parents invest more in daughters. This finding illustrates the specificity of situations in which the TWH effects should be expected. Only certain types of parental investment — such as protection and a bias in the sex ratio — may have been selected to vary according to parental condition. Optimal allocation of resources after the child is born, however, is achieved not by the simple bias predicted by the TWH, but by allocating resources among offspring in ways that yield the largest marginal inclusive fitness gains.     

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.     

Parental investment by sex on ifaluk

Trivers and Willard (Science 179;90–92, 1973) predict that where investment by parents in good condition increases the fitness of sons more than that of their sisters, while the opposite is true of parents in poor condition, parents with much to invest will favor sons, while those with little will favor daughters. Patterns of parent-child association on Ifaluk atoll are consistent with this prediction.     

Social rank and sex ratio of captive long-tailed macaque females (Macaca fascicularis)

Variation in birth sex ratios in primates can be accounted for by two hypotheses: the local resource competition hypothesis [Silk: American Naturalist 121:56–66, 1983] and the hypothesis of Trivers & Willard [Science 179:90–92, 1973] concerning the maternal effect on the quality of a male. We examined the effects of female dominance rank on aspects of reproduction in three well-established captive groups of long-tailed macaques (Macaca fascicularis). High-ranking females produced a higher proportion of sons than low-ranking females, and factors other than rank did not have significant effects on birth sex ratios. Interbirth intervals following daughters were longer than those following sons, but they were independent of the mother's rank. The sons of high-ranking mothers had better survival prospects than sons of low-ranking mothers in some of the groups; no such difference was found for daughters. Overall, there was no sex difference in survival up to 5 years of age. These results support the Trivers-Willard hypothesis rather than the local resource competition hypothesis. An analysis of interbirth intervals suggested that the deviation in birth sex ratio is already established at conception.     

Trivers-Willard at birth and one year: evidence from US natality data 1983-2001

Trivers & Willard (TW) hypothesized that evolution would favour deviations from the population sex ratio in response to parental condition: parents in good condition would have more sons and parents in poor condition would have more daughters. We analyse the universe of US linked births and infant deaths to white mothers 1983-2001, covering 48 million births and 310,000 deaths. We find that (i) married, better educated and younger mothers bore more sons and (ii) infant deaths were more male if the mother was unmarried and young. Our findings highlight the potential role of offspring sex ratio as an indicator of maternal status, and the role of infant mortality in shaping a TW pattern in the breeding population.     

Sex ratio manipulation within broods of house wrens, Troglodytes aedon

Trivers & Willard (1973, Science, 179, 90-92) developed an economic theory of parental investment to explain how the relative profitability of sons and daughters varies under specific ecological conditions. In their maternal condition hypothesis they proposed that in polygynous species, the sex of an offspring should be associated with the amount of parental care likely to be made available to it. In these species, the amount of parental investment directed towards offspring may differentially influence the fitness of male and female offspring because males in better than average condition as adults may enjoy larger fitness gains than a female would if she were in better than average condition, while the reverse may be true when conditions are poor. I tested this hypothesis by determining the sex of specific offspring within house wren broods. Because hatching is asynchronous and fledging is synchronous in this polygynous species, last-hatched young fledge having received less parental care than their broodmates. I predicted that last-hatched offspring would be more likely to be female. I found that these young were indeed more likely to be females, were more likely to have hatched from last-laid eggs and were fledging in poor condition relative to their broodmates. I propose that female house wrens behave in a manner consistent with the predictions of the Trivers & Willard hypothesis by producing female offspring last in the laying sequence of their clutches. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

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.     

Waiting for Trivers and Willard: Do the rich really favor sons?

Parental investment theory has been put forward as a major evolutionary argument explaining male or female biased birth sex ratio, the Trivers-Willard (T-W) hypothesis, predicting that parents living in good circumstances will bias their investment to sons, whereas parents in poor circumstances will bias their investment toward daughters. Tests of the T-W hypothesis on human beings have shown limited evidence for parents appearing to differentiate their investment to sons or daughters according to the reproductive potential of each sex. The present study tests the T-W hypothesis among a large contemporary Polish sample using first birth interval and extent of breastfeeding as measures of parental investment, and economic status and level of parental education as measures of parental condition. The extents to which parental investment and markers of parental condition vary by sex of the child were examined using log-linear analysis. Weak support for the T-W effect is found among families where fathers were best educated, where a greater proportion of first-born boys are breastfed longer than girls, while the opposite trend is observed among families with fathers with lowest levels of education. Although the present study does not fully support the T-W hypothesis, it gives evidence of greater investment in female offspring at the lower extremes of income, and greater investment in males at higher levels of income.     

The effects of the minimum threshold condition for breeding on offspring sex-ratio adjustment in the lesser kestrel

We propose a model for sex-ratio adjustment complementary to that of Trivers and Willard. In addition to the three basic assumptions of the Trivers-Willard model, our model assumes that the sex with more variable reproductive success (normally male) is also the sex less constrained for reproduction. This assumption seems realistic, because several studies have demonstrated that poor-condition males may adopt alternative mating strategies and sire some offspring, whereas females have physiological constraints for gestation or egg production that cannot be avoided. Thus, under these circumstances, sons of both poor and good condition would be more valuable for parents than daughters, whereas daughters would be relatively more valuable than sons at intermediate condition. This model predicts, therefore, a U-shaped relationship between parental condition and offspring sex ratio. We present a case study for the monogamous lesser kestrel (Falco naumanni) that fulfills the assumptions and predictions of the model. The minimum body condition for breeding, measured as pectoral thickness, was lower for sons than for daughters. Below this minimum, males had a higher chance of breeding than females. Above this minimum, however, the lifetime reproductive success was condition dependent in males but not in females. Thus, males in better body condition attain, on average, higher reproductive success than females. Offspring sex ratio varied with the size of the father's ornaments and mother condition according to the U-shaped pattern predicted by the model.     

Trivers-willard rules for sex allocation

We present a quantitative model of sex allocation to investigate whether the simple “rules of thumb” suggested by Trivers and Willard (1973) would really maximize numbers of grandchildren in human populations. Using demographic data from the !Kung of southern Africa and the basic assumptions of the Trivers-Willard hypothesis, we calculate expected numbers of grandchildren based on age- and sex-specific reproductive value. Patterns of parental investment that would maximize numbers of expected grandchildren often differ from the Trivers-Willard rules. In particular, the optimum parental behavior is sensitive to population dynamics, type of parental investment, and, most important, relative ages of sons and daughters. It is doubtful whether a parent blindly following the simple Trivers-Willard rules would maximize numbers of expected grandchildren, on average. In addition, we show that sex-specific infanticide will almost never achieve the goal of maximizing expected numbers of grandchildren.     

Factors associated with exclusive breastfeeding at discharge during the COVID-19 pandemic in 17 WHO European Region countries

Both the consumption of breastmilk in infancy and a person’s season of birth influences his or her health, educational, professional, and behavioral outcomes. Further, season of birth effects differ by sex. However, current research, for the most part, neglects to examine if season of birth and breastfeeding are related. This paper examines the impact of sex-based variations in season of birth on breastfeeding likelihood and duration in the U.S. Using data from children born to female respondents of the National Longitudinal Survey of Youth 1979 (born between 1970 and 2012), this study examines with Probit, Negative Binomial, and Ordinary Least Squares (OLS) regressions if a child’s season of birth and sex are correlated with breastfeeding incidence and duration. The breastfeeding incidence and duration data are self-reported by the mother. Season of birth has a small but statistically significant impact on the incidence and duration of breastfeeding, which varies depending on the sex of the infant. Mothers giving birth to sons in the spring are 13.5% less likely to breastfeed than those giving birth to sons in the winter (with a p - value of 0.0269). Mothers with daughters born in the summer or fall (autumn) breastfeed slightly longer than mothers with daughters born in the spring. On average, mothers of summer-born daughters breastfeed 4.1% longer (with a 95% confidence interval of 0.3 - 7.8) and those with fall-born daughters 3.8% longer (with a 95% confidence interval of 0 - 7.5). Mothers giving birth to daughters in the spring are also significantly less likely to reach the breastfeeding six-week duration target (compared to fall and winter births) and the one-year duration target (compared to fall births). These findings suggest that the costs and benefits of breastfeeding an infant vary with the season of birth and the sex of the child. This finding could explain some of the season of birth effects previously identified in the literature. Further, policymakers seeking to increase breastfeeding rates should consider the reduced breastfeeding rates and durations for children born in the spring.     

Maternal diet and other factors affecting offspring sex ratio: a review

Mammals usually produce approximately equal numbers of sons and daughters, but there are exceptions to this general rule, as has been observed in ruminant ungulate species, where the sex-allocation hypothesis of Trivers and Willard has provided a rational evolutionary underpinning to adaptive changes in sex ratio. Here, we review circumstances whereby ruminants and other mammalian species, especially rodents and primates, appear able to skew the sex ratio of their offspring. We also discuss some of the factors, both nutritional and nonnutritional, that potentially promote such skewing. Work from our laboratory, performed on mice, suggests that age of the mother and maternal diet, rather than the maternal body condition per se, play directive roles in controlling sex ratio. In particular, a diet high in saturated fats but low in carbohydrate leads to the birth of significantly more male than female offspring in mature laboratory mice, whereas when calories are supplied mainly in the form of carbohydrate rather than fat, daughters predominate. As the diets fed to the mice in these experiments were nutritionally complete and because litter sizes did not differ between treatments, dietary inadequacy seems not to be the cause for sex-ratio distortion. A number of mechanisms, all of which are testable, are discussed to provide an explanation for the phenomenon. We conclude the review by discussing potential implications of these observations to human medicine and agriculture.     

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.     

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.     

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

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