Human‐like adrenal development in wild chimpanzees: A longitudinal study of urinary dehydroepiandrosterone‐sulfate and cortisol

Abstract

The development of the adrenal cortex varies considerably across primates, being most conspicuous in humans, where a functional zona reticularis-the site of dehydroepiandrosterone-sulfate (DHEA/S) production-does not develop until middle childhood (5-8 years). Prior reports suggest that a human-like adrenarche, associated with a sharp prepubertal increase in DHEA/S, may only occur in the genus Pan. However, the timing and variability in adrenarche in chimpanzees remain poorly described, owing to the lack of longitudinal data, or data from wild populations. Here, we use urine samples from East African chimpanzees (Pan troglodytes schweinfurthii) collected over 20 years at Kanyawara in Kibale National Park, Uganda, to trace the developmental trajectories of DHEAS (n = 1,385 samples, 53 individuals) and cortisol (n = 12,726 samples, 68 individuals). We used generalized additive models (GAM) to investigate the relationship between age, sex, and hormone levels. Adrenarche began earlier in chimpanzees (~2-3 years) compared with what has been reported in humans (6-8 years) and, unlike humans, male and female chimpanzees did not differ significantly in the timing of adrenarche nor in DHEAS concentrations overall. Similar to what has been reported in humans, cortisol production decreased through early life, reaching a nadir around puberty (8-11 years), and a sex difference emerged with males exhibiting higher urinary cortisol levels compared with females by early adulthood (15-16 years). Our study establishes that wild chimpanzees exhibit a human-like pattern of cortisol production during development and corroborates prior reports from captive chimpanzees of a human-like adrenarche, accompanied by significant developmental increases in DHEAS. While the role of these developmental hormone shifts are as yet unclear, they have been implicated in stages of rapid behavioral development once thought unique to humans, especially in regard to explaining the divergence of female and male social behavior before pubertal increases in gonadal hormones.

Sex differences in early experience and the development of aggression in wild chimpanzees

“…These pathways, which are thought to be activated by testosterone during puberty, may also be activated during adrenarche (82), a prepubertal developmental milestone that marks the maturation of the adrenal gland and is accompanied by increases in the adrenal androgen dehydroepiandrosterone (DHEA) and its sulfate (DHEAS, denoted jointly as DHEA/S) (83). In both captivity (84,85) and our study population of wild chimpanzees (86) increasing DHEAS is detectable several years prior to puberty. Although its effects are weaker than testosterone, DHEA/S is associated with increased aggression in birds and mammals (87).…”

“…Although its effects are weaker than testosterone, DHEA/S is associated with increased aggression in birds and mammals (87). While male and female chimpanzees exhibit similar DHEAS levels throughout development (86), this abundant androgen hormone could still contribute to developmental increases in aggression among chimpanzees by activating prenatally organized differences in neural pathways (29,81,82).…”

Wild chimpanzee offspring exhibit adult‐like foraging patterns around the age of weaning

“…Because this inspection suggested a nonlinear relationship between age and proportion of time spent eating, we initially modeled feeding time using generalized additive mixed models (GAMMs) using the gamm4 package (Wood & Scheipl, 2015). These models fit smooth functions to nonlinear data without making assumptions about the shape of the relationship, can incorporate random effects for uneven and repeated measures on the same subject, and have proven to be appropriate for modeling developmental changes in chimpanzees (Lonsdorf, Anderson, et al, 2014; Lonsdorf, Markham, et al, 2014; Matsumoto, 2017; Sabbi et al, 2019). However, the GAMM approach resulted in an overdispersed model; therefore, we used the glmmTMB package to account for overdispersion (Brooks et al, 2017).…”

The evolution of perennially enlarged breasts in women: a critical review and a novel hypothesis

“…We suggest that the most probable candidate is dehydroepiandrosterone (DHEA/S). Adrenarche, which sees the post-natal rise of DHEA/S (adrenal precursor of sex steroids), is unique to humans, chimpanzees (Sabbi et al, 2019), bonobos (Pan paniscus) (Behringer et al, 2012), and gorillas (Gorilla gorilla) (Edes, 2017), but DHEA/S is much higher in adolescent girls than in other young primates (Blevins et al, 2013). DHEA/S is an important source of E2 in maturing girls during the adrenarche phase of puberty (Labrie et al, 1998), and the highest rise in BMI during puberty is accompanied by an increase in DHEA/S levels (Kaplowitz, 2008).…”