Alexander Baxter and Dr. J. Dee Higley, Psychology Department
Prenatal androgen exposure (PAE) is the organizational force that masculinizes the brain. It has impact on other parts of the body as well. For example, PAE induces growth in the ring finger. Consequently, the pointer-to-ring-finger digit ratio (2D:4D ratio) is frequently used to assess PAE.1 Though this phenotype is sexually dimorphic, research indicates that PAE’s effect on digit ratio may be in the opposite direction when comparing humans and nonhuman primates.22 Very few studies have investigated 2D:4D ratio in rhesus macaques (Macacca mulatta), and to our knowledge, none have reported a sex difference in digit ratio. The purpose of this study is to investigate 2D:4D ratio in this species. We hypothesize that rhesus monkeys will display the nonhuman primate pattern of 2D:4D ratio, with males having higher digit ratio than females.
Another purpose of this study is to investigate 2D:4D ratio and anxiety. In humans, anxiety is influenced by both PAE3 and circulating androgens.4 Because prenatal androgens masculinize the brain, it may partially explain why males, on average, tend to show less anxiety than females.5 In this study, we assess whether 2D:4D ratio is associated with infant anxiety in rhesus monkeys. We hypothesize that high 2D:4D (indicative of high PAE) will be associated with low levels of infant anxiety.
Subjects were 344 adult rhesus macaques (250 females, 94 males) housed at the California National Primate Research Center (mean age = 7 years old). Fingers were measured using a digital caliper during routine health inspections, when the animals were sedated. One person performed the measurements, one person (me) held the monkey’s hand flat on the table, and one person recorded the measurements. Subjects’ left- and right-hand index-fingers (2nd Digit) and ring-fingers (4th Digit) were measured at least twice. Digit ratio was calculated for each hand by dividing the average 2nd Digit length by the average 4th digit length. Infant anxiety was measured earlier in subjects’ lives at 3-4 months of age, as part of a biobehavioral assessment program. Infants were separated from their mother for 25 hours, and observed for anxious behaviors during 5-minute focal observations. Behavioral indicators of anxiety included freezing, threatening, self-directed behaviors, and distress vocalizations. Data were analyzed using SPSS V.23 (IBM) using t-tests and Pearson correlation.
An independent samples t-test revealed a sex difference in left-hand 2D:4D ratio (t(256) = 2.64, p = .009; see Figure 1). Males had higher left-hand 2D:4D ratio (M = 0.815) than females (M = 0.802). There was also a sex difference in right-hand 2D:4D ratio (t(259.70) = 2.25, p = .025, equal variances not assumed; see Figure 1). Males had higher right-hand 2D:4D ratio (M = 0.811) than females (M = 0.784). There was no correlation between digit ratio and any measures of anxiety.
As hypothesized, we found a sex difference in rhesus monkeys’ left-hand and righthand 2D:4D ratio. Like other nonhuman primate species,2 in rhesus monkeys, males had higher 2D:4D ratio than females. To our knowledge, this is the first study to find a sex difference in this species’ 2D:4D ratio. Though it is not known why rhesus monkeys show a reversed pattern of 2D:4D sex differences compared to humans, it is possible there are species differences which account for this finding.5 Rhesus monkeys may have a different distribution of androgen receptor distributions in their ring finger, or different windows of sensitivity to prenatal androgens during development. We plan to collect more data to test these hypotheses.
Though we predicted 2D:4D ratio would correlate with anxiety, we found no association. Though human research has linked high 2D:4D ratio (low PAE in humans) with adult anxiety,3 this association may emerge during infancy. Further longitudinal research is needed to investigate how PAE affects the expression of anxiety during development.
Rhesus monkeys show sexually dimorphic 2D:4D ratio. Like other nonhuman primates, males have higher 2D:4D ratio than females. The association between prenatal androgens and infant anxiety is not reflected in this species’ 2D:4D ratio.
- Manning, J. T. (2011). Resolving the role of prenatal sex steroids in the development of digit ratio. Proceedings of the National Academy of Sciences, 108(39), 16143-16144.
- Roney, J. R., Whitham, J. C., Leoni, M., Bellem, A., Wielebnowski, N., & Maestripieri, D. (2004). Relative digit lengths and testosterone levels in Guinea baboons. Hormones and Behavior, 45(4), 285-290.
- Evardone, M., & Alexander, G. M. (2009). Anxiety, sex-linked behaviors, and digit ratios (2D: 4D). Archives of Sexual Behavior, 38(3), 442-455.
- Jin, E. S., Rice, L. K., & Josephs, R. (2016). Intranasal testosterone administration reduces acute subjective anxiety in women in response to laboratory stressor. Psychoneuroendocrinology, 71, 31
- Donner, N. C., & Lowry, C. A. (2013). Sex differences in anxiety and emotional behavior. Pflügers Archive-European Journal of Physiology, 465(5), 601-626.