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. 2020 Nov;62(7):979-991.
doi: 10.1002/dev.21899. Epub 2019 Aug 1.

Sexual Dimorphism in Titi Monkeys' Digit (2D:4D) Ratio is Associated with Maternal Urinary Sex Hormones During Pregnancy

Alexander Baxter  1   2   3 , Elizabeth K Wood  1 , Lynea R Witczak  2   3 , Karen L Bales  2   3 , J Dee Higley  1
Affiliations

Sexual Dimorphism in Titi Monkeys' Digit (2D:4D) Ratio is Associated with Maternal Urinary Sex Hormones During Pregnancy

Alexander Baxter et al. Dev Psychobiol. 2020 Nov.

Abstract

The second-to-fourth digit (2D:4D) ratio is a sexually-dimorphic biomarker for prenatal sex hormone exposure. We investigated whether titi monkeys (Plecturocebus cupreus) exhibit sexually-dimorphic 2D:4D ratio, and whether variation in 2D:4D ratio correlates with maternal testosterone and estrogen levels during early pregnancy. Subjects were 61 adult titi monkeys (32 males, 29 females). For 26 subjects, maternal urine samples were collected approximately 15-20 weeks before birth and assayed for testosterone and estrone conjugate (E1 C). Titi monkeys exhibited a human-like pattern of sexual dimorphism in right-hand 2D:4D ratio, with females exhibiting higher 2D:4D ratio than males (β = -0.29, p = 0.023). For left-hand 2D:4D ratio, high levels of maternal E1 C predicted low offspring 2D:4D ratio (β = -0.48, p = 0.009). For right-hand 2D:4D ratio, high levels of testosterone (β = -0.53, p = 0.005) and testosterone-to-E1 C ratio (β = -0.41, p = 0.028) predicted low offspring 2D:4D ratio. For 2D:4D ratio asymmetry (right-hand - left-hand), high levels of testosterone (β = -0.43, p = 0.03) and testosterone-to-E1 C ratio (β = -0.53, p = 0.003) predicted low (right-biased) asymmetry. This is the first report of sexually-dimorphic 2D:4D ratio in New World monkeys, and the results support a growing literature suggesting prenatal sex hormones may modulate offspring 2D:4D ratio.

Keywords: 2D:4D ratio; maternal hormones; prenatal androgen; prenatal estrogen; sexual dimorphism; titi monkey; urinary sex hormones.

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Conflict of interest statement

Conflict of Interest:

The authors have no conflicts of interest to declare.

Figures

Figure 1.
Figure 1.. Sex Difference in Titi Monkeys’ Right‐hand 2D:4D Ratio.
Description: The graphs show titi monkeys’ left‐hand 2D:4D ratio, right‐hand 2D:4D ratio, and 2D:4D ratio asymmetry (right‐hand – left‐hand) by sex. The x‐axis represents subjects’ sex, and the y‐axis represents 2D:4D ratio (the left and middle panels) or 2D:4D ratio asymmetry (the right panel). The white circles represent the mean for females, the black circles represent the mean for males, and the error bars represent ±1 standard error. The * with dashed lines indicates a significant comparison at p < 0.05, and the ns with dashed lines indicates the difference between means is not significant (p > 0.05).
Figure 2.
Figure 2.. Maternal Sex Hormones are Associated with Offspring 2D:4D Ratio Differentially Across the Hands.
Description: The graph depicts the association between maternal urinary sex hormones during pregnancy and offspring left‐hand 2D:4D ratio, right‐hand 2D:4D ratio, and 2D:4D ratio asymmetry (right‐hand – left‐hand) measured in adulthood. In the left and middle column panels, the y‐axis depicts offspring 2D:4D ratio; in the right column panels, the y‐axis depicts offspring 2D:4D ratio asymmetry. In all graphs, the solid black line represents the line of best fit and the shaded gray region represented the standard error of prediction. In the bottom left‐hand corner of each graph, p < 0.05 indicates the association is significant, and ns indicates the association is not significant (p > 0.05).
Figure 3.
Figure 3.. Sex Differences in Primates’ 2D:4D Ratio Exhibits Phylogenetic Variation Across Primate Superfamilies.
Description: The figure depicts the direction of sex differences in 2D:4D ratio across primate phylogeny. The tree is based on commonly accepted phylogenetic estimates (Arnold, Matthews, & Nunn, 2010; Perelman et al., 2011). Abbreviations: OW indicates Old World; NW indicates New World; Males < Females indicates that, on average, males exhibit lower 2D:4D ratio than females; Males > Females indicates that on average, males exhibit higher 2D:4D ratio than females; Males = Females indicates no sex differences observed in 2D:4D ratio. For a note on studies omitted from this table, see the supplementary material. References in Figure: Hönekopp & Watson (2010) (among many others); 2 McIntyre et al. (2009); 3 Baxter et al. (2018); 4 Abbott et al. (2012); 5 Roney et al. (2004); 6 Huber et al. (2017); 7 The Current Study
See this image and copyright information in PMC

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