Abstract
Prenatal androgen exposure (PAE) plays a pivotal role in masculinizing the developing body and brain, and extreme exposure may contribute to autism, anxiety disorder and schizophrenia. One commonly used biomarker for PAE is the pointer-to-ring-finger digit length (2D:4D) ratio. Although this biomarker is widely used in human studies, relatively few studies have investigated 2D:4D ratio in nonhuman primates, particularly rhesus macaques (Macaca mulatta), one of the most commonly used animals in biomedical research. Thus far, data suggest that sexual dimorphism in 2D:4D ratio may be in the opposite direction in some monkey species, when compared to the pattern exhibited by humans and great apes. Using a large sample size, we investigated whether rhesus monkeys’ 2D:4D ratio shows the same sex-differentiated pattern present in other Old World monkey species. We also investigated whether individual differences in 2D:4D ratio are associated with the social dominance rank of subjects’ mothers during pregnancy, and the social dominance rank the subjects attained as adults. Subjects were 335 rhesus monkeys between 3 years and 24 years of age (M = 6.6). Maternal dominance rank during pregnancy and subjects’ adult dominance rank were categorized into tertiles (high, middle and low). Results showed that, across both hands, male rhesus monkeys exhibited higher 2D:4D ratio than females, a pattern consistent with other monkey species and a reversal from the pattern typically observed in humans and apes. This sex difference was modulated by maternal dominance rank, with female offspring of high-ranking and middle-ranking mothers exhibiting masculinized 2D:4D ratio, indicating that maternal dominance rank during pregnancy may influence levels of PAE. There was no association between subjects’ 2D:4D ratio and the social dominance rank they attained as adults. These findings show a consistent sex difference in Old World monkeys’ 2D:4D ratio that diverges from the pattern observed in apes and humans, and suggest maternal social dominance rank modulates PAE in rhesus monkeys.
Highlights
Prenatal androgen exposure (PAE) plays a critical organizational role in masculinizing the developing body and brain
Because PAE may, in turn, affect temperament and personality traits related to socially dominant behavior, another purpose of this study is to investigate the association between 2D:4D ratio and the social dominance rank that monkeys attain as adults
Using a large sample of rhesus monkeys, our data show a sexually-dimorphic 2D:4D ratio pattern that is consistent with other studies of Old World monkeys (Roney et al, 2004; Abbott et al, 2012), with males exhibiting higher 2D:4D ratio than females
Summary
Prenatal androgen exposure (PAE) plays a critical organizational role in masculinizing the developing body and brain. In males, high levels of PAE are implicated in the occurrence and severity of autism spectrum disorder (Manning et al, 2001) and low levels of PAE are associated with increased anxiety (De et al, 2006; Evardone and Alexander, 2009). In both sexes, low levels of PAE may be associated with schizophrenia (Collinson et al, 2010; Paipa et al, 2018) and high levels of PAE may be associated with attention deficit hyperactivity disorder (Stevenson et al, 2007; Martel et al, 2008). While PAE is only one of the factors contributing to these disorders, and the activating effects of postnatal androgens may contribute (Arnold and Breedlove, 1985), a better understanding of the structural and functional effects of PAE on the brain could potentially lead to better preventions, treatments and interventions, as well as a better understanding of sex differences in the brain and in behavior
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