High-income women may prenatally masculinize their sons at the expense of the fitness of their daughters; low-income women may prenatally feminize their daughters at the fitness expense of their sons

Parental income inequality and children’s digit ratio (2D:4D): a ‘Trivers-Willard’ effect on prenatal androgenization? J.T. Manning et al. Journal of Biosocial Science, February 2021. https://www.cambridge.org/core/journals/journal-of-biosocial-science/article/parental-income-inequality-and-childrens-digit-ratio-2d4d-a-triverswillard-effect-on-prenatal-androgenization/CE6A605963BB8D8D921ECBDD4988B01E

Abstract: Income inequality is associated positively with disease prevalence and mortality. Digit ratio (2D:4D) – a negative proxy for prenatal testosterone and a positive correlate of prenatal oestrogen – is related to several diseases. This study examined the association of income inequality (operationalized as relative parental income) and children’s 2D:4D. Participants self-measured finger lengths (2D=index finger, and 4D=ring finger) in a large online survey conducted in July 2005 (the BBC Internet Study) and reported their parents’ income. Children of parents of above-average income had low 2D:4D (high prenatal testosterone, low prenatal oestrogen) while the children of parents of below-average income had high 2D:4D (low prenatal testosterone, high prenatal oestrogen). The effects were significant in the total sample, present among Whites (the largest group in the sample), in the two largest national samples (UK and USA) and were greater for males than females. The findings suggest a Trivers-Willard effect, such that high-income women may prenatally masculinize their sons at the expense of the fitness of their daughters. Women with low income may prenatally feminize their daughters at the fitness expense of their sons. The effect could, in part, explain associations between low income, high 2D:4D (low prenatal testosterone) and some major causes of mortality such as cardiovascular disease.

Keywords 2D:4D Income disparity Trivers-Willard hypothesis

Discussion

The present study found that parental income affects children’s 2D:4D such that below-average income is related to high 2D:4D (feminization of the fetus) and above-average parental income is associated with low 2D:4D (masculinization of the fetus). These findings applied to the total study sample, the most numerous ethnic group in the study (i.e. Whites) and the most numerous national samples (UK and USA). Regarding the total sample, for male children, the effect was present for right and left 2D:4D and for all pairwise comparisons between parental income groups above and below the population average. For female children, the effect was also present on right and left hand 2D:4D and was found in pairwise comparisons between parental income groups above and below the population average. However, the female effects were weaker than the male effects, with only two significant pairwise comparisons for right hand 2D:4D and three for left hand 2D:4D.

The present findings are consistent with the Trivers-Willard hypothesis concerning maternal resources and its links to the influence of the mother’s sex steroids on fetal 2D:4D. Thus, mothers with high income will secrete elevated levels of T relative to E during the 1^st trimester of their pregnancy, i.e. they will masculinize their male and female children. In contrast, women with low income will secrete low levels of T:E in the early stages of pregnancy. This hormonal milieu will feminize their male and female children. That is, high-income mothers will increase the fitness of their sons at the expense of their daughters while low-income mothers will increase the fitness of their daughters at the expense of their sons. Thus, there will be sexually antagonistic effects on the children of both high- and low-income mothers (Manning et al., 2000). There is evidence for an effect of female condition on the production of sex steroids and sexually antagonistic effects of maternal sex steroids on the developing fetus.

There is only weak support for a link between the 2D:4D of women selected at random from the population and their production of T and E (Muller et al., 2011). However, in contrast to women with low income, high-income women may benefit from high levels of nutrition. There may be associations between high income, good nutrition and the production of androgens in women. Elite women athletes with high standards of nutrition and in good condition (with high lean mass and low body fat levels) show negative relationships between their 2D:4D and the breakdown products of T (Eklund et al., 2020) or salivary levels of T (Crewther & Cook, 2019). It appears that women in good condition can, and probably do, secrete elevated levels of T, particularly if they have low 2D:4D.

The Trivers-Willard hypothesis was originally formulated in the context of maternal manipulation of the sex ratio of progeny. There is indeed evidence that masculinized women (with high WHR and/or low 2D:4D) have more sons than feminized women (low WHR and/or high 2D:4D). This may be the result of the deleterious effects of high prenatal T on female fetuses and/or the advantageous effect of high prenatal T on male fetuses (Manning et al., 1996; Singh & Zambarano, 1997; Manning & Bundred, 2001; Kim et al., 2015).

Maternal manipulation of the prenatal sex steroid environment of their children is likely to have later-life health consequences. For example, male children of low-income mothers will be feminized and more prone to several diseases. Prominent among these is likely to be the poverty influenced male-biased burden of cardiovascular diseases. A low income level has been consistently associated with cardiovascular disease, especially in high-income countries. In addition, disparities based on sex (males>females) have been shown in several studies. High 2D:4D in men has been linked to poor outcomes for cardiovascular disease such as early myocardial infarction, high blood pressure, atherosclerotic plaque development, high fibrinogen levels and markers of obesity (Manning & Bundred, 2001; Fink et al., 2006; Lu et al., 2008, 2015; Ozdogmus et al., 2010; Kyriakidis et al., 2010 ; Wu et al., 2013; Manning et al., 2019; Bagepally et al., 2020). Associated with all of these factors is a high level of parental poverty (Kucharska-Newton et al., 2011; Mosquera et al., 2016).

One possible limitation of the present study is that estimates of parental income in the early years of the family are dependent on their children’s recall. Inaccuracies that may result from faulty recall are likely to reduce the Trivers-Willard influence on 2D:4D. Thus, the reported effects may be conservative estimates of maternal influence on offspring 2D:4D. In order to minimize the recall effects of children’s estimates of parental income it is suggested that future studies should also include parental reports of family income.

In conclusion, inequality in parental income may be associated with the 2D:4D of their offspring. Children of parents of above-average income had low 2D:4D (high prenatal T:E) while the children of parents of below-average income had high 2D:4D (low prenatal T:E). The differences in offspring 2D:4D across income groups may arise because of maternal manipulation of sex steroids. Interpreting the findings of the present study through the lens of the Trivers-Willard hypothesis suggests that high-income mothers may masculinize their sons via increased levels of prenatal T. Male reproductive success shows higher variance than female reproductive success. Therefore, the fitness rewards from the sons of high-income mothers are likely to outweigh the deleterious effects of T on the daughters of high-income mothers. In contrast, mothers with low income are expected to feminize their children via increases in prenatal E. The fitness gain from feminized daughters is likely to outweigh the fitness loss of feminized sons. Moreover, the health costs of maternal manipulation of prenatal sex steroids may include hypertension, cardiovascular disease, high levels of fibrinogen and early myocardial infarction and could be focused on the feminized (low T, high E) sons of low-income mothers.