Winning the Genetic Lottery: Biasing Birth Sex Ratio Results in More Grandchildren

Abstract

Population dynamics predicts that on average parents should invest equally in male and female offspring; similarly, the physiology of mammalian sex determination is supposedly stochastic, producing equal numbers of sons and daughters. However, a high quality parent can maximize fitness by biasing their birth sex ratio (SR) to the sex with the greatest potential to disproportionately outperform peers. All SR manipulation theories share a fundamental prediction: grandparents who bias birth SR should produce more grandoffspring via the favored sex. The celebrated examples of biased birth SRs in nature consistent with SR manipulation theories provide compelling circumstantial evidence. However, this prediction has never been directly tested in mammals, primarily because the complete three-generation pedigrees needed to test whether individual favored offspring produce more grandoffspring for the biasing grandparent are essentially impossible to obtain in nature. Three-generation pedigrees were constructed using 90 years of captive breeding records from 198 mammalian species. Male and female grandparents consistently biased their birth SR toward the sex that maximized second-generation success. The most strongly male-biased granddams and grandsires produced respectively 29% and 25% more grandoffspring than non-skewing conspecifics. The sons of the most male-biasing granddams were 2.7 times as fecund as those of granddams with a 50∶50 bias (similar results are seen in grandsires). Daughters of the strongest female-biasing granddams were 1.2 times as fecund as those of non-biasing females (this effect is not seen in grandsires). To our knowledge, these results are the first formal test of the hypothesis that birth SR manipulation is adaptive in mammals in terms of grandchildren produced, showing that SR manipulation can explain biased birth SR in general across mammalian species. These findings also have practical implications: parental control of birth SR has the potential to accelerate genetic loss and risk of extinction within captive populations of endangered species.

Do mothers prefer helpers or smaller litters? Birth sex ratio and litter size adjustment in cotton‐top tamarins (Saguinus oedipus)

“…Clearly, primates and other mammals can maximize their fitness returns by allocating sex, even in captivity (Thogerson et al. ), but the results of the current study suggest that reproductive decisions are not so unequivocal. Other reproductive decisions, such as how many infants to gestate and support, may take initial precedence in terms of maximizing fitness returns.…”

“…A recent study has highlighted the potential for natural selection to act on the facultative adjustment of birth sex ratio; Thogerson et al. () found, using data from captive breeding programmes for 198 mammalian species, that grandparents which produced sex ratios which were biased in the predicted direction had more grand‐offspring. Clearly, primates and other mammals can maximize their fitness returns by allocating sex, even in captivity (Thogerson et al.…”

“…Despite this, population sex ratios across the vertebrates are often biased (Sheldon and West ; Silk and Brown ), and Thogerson et al. () showed clearly the adaptive value of sex allocation in terms of grand‐offspring production in the mammals. Sex allocation in the primates has yielded a substantial body of literature, and the predictions differ with social system and life history.…”

Sex Differences in Early Embryogenesis: Inter‐Chromosomal Regulation Sets the Stage for Sex‐Biased Gene Networks

“…[104] However, the relationship between male and female expression differences and sexually dimorphic traits is not necessarily direct. [88] Few studies in mammals associating alterations in environment with developmental events related to sex allocation have been reported, [107,108] although the evidence for dimorphisms soon after fertilization should arouse interest in this direction. [105] This requires empirical studies integrating the expression level differences and sex-specific fitness, something that has only been achieved in non-mammalian animal models.…”

Sperm selection in the female mammalian reproductive tract. Focus on the oviduct: Hypotheses, mechanisms, and new opportunities

“…Nevertheless, all semen samples contain two genetically well-defined sperm subpopulations that differ in terms of the X-or Y-chromosomes within the sperm head. Sex ratio skewing in natural mammalian populations has long been recognized [108], and a recent cross-species and multigenerational analysis [109] attributed the effect to the existence of specific individuals with the ability to bias sex ratios. Although it is difficult to understand how this could happen in terms of sperm function, a recent experimental study in which X-and Y-sex-sorted porcine spermatozoa were introduced surgically into the left and right oviducts of the same animals goes some way to providing clues [110].…”