Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels

Abstract

Adrenarche is characterized by the onset of adrenal secretions of increasing amounts of dehydroepiandrosterone-sulfate (DHEA-S). While the function of adrenarche remains a matter of speculation, evidence suggests that the morphological and physiological changes related to it are restricted to humans and closely related primates. Within the primate order, adrenarche has been described only in humans and chimpanzees, but bonobos, the sister species of chimpanzees, have not yet been studied regarding the early ontogenetic changes such as adrenarche. While bonobos and chimpanzees share many morphological and behavioral characteristics, they differ in a number of behavioral traits, and there is a growing interest in terms of the physiological differences that can be linked to species-specific patterns of social behavior. In this study, we measured urinary DHEA-S levels to determine whether bonobos experience physiological changes that are indicative of adrenarche. We measured DHEA-S in urine using ELISA and analyzed its levels in the samples from 53 bonobos aged 1-18 years. Our results show that bonobos experience an increase in DHEA-S levels after 5 years of age, which is comparable with the patterns observed in humans and chimpanzees. This indicates that bonobos do undergo adrenarche and that the timing of onset is similar to that of the two Pan species. The extraction procedures described in this report demonstrate the use of urine for monitoring ontogenetic changes in DHEA-S excretion. If applicable to other species, the technique would facilitate more research on the evolutionary origin of adrenarche and other developmental processes.

Nutritional Phases in Prader-Willi Syndrome: Evolutionary and Clinical Interpretations

“…Adrenarche occurs at around the age of weaning in great apes: bonobos wean after four years [22] with increases in adrenal androgens after five years [23]; orangutans wean after seven years [24] with increases in adrenal androgens after eight years [25]. Campbell noted that increased production of adrenal androgens accompanies independence from mothers at weaning in rodents and monkeys but occurs much later than weaning in humans [26].…”

The tempo of human childhood: a maternal foot on the accelerator, a paternal foot on the brake

“…16,17 Hormonal changes also occur as primates undergo these nutritional shifts. Adrenal androgens increase at about 5 years of age in semi-captive bonobos, chimpanzees, and gorillas 18,19 and at about 8 years of age in orangutans, 20 roughly corresponding with ages at weaning: 7-8 years in orangutans and 3-5 years in the other great apes (Table 1). This correlation, based on limited data, suggests that adrenal androgens may play a role in the increased independence observed in juvenile apes at weaning.…”

Hormones and Human and Nonhuman Primate Growth

“…It has been proposed that relatively low levels of DHEA/DHEAS until later in postnatal life – a substrate that could be converted into other more potent androgens and estrogens – serves to delay the onset of puberty in chimpanzees and humans relative to macaques (see below). Gorillas show a transient, early increase in DHEA/DHEAS – earlier than chimpanzees but similar in overall pattern [47]. The results from this comparative study suggests that similarity in human and African great ape DHEA/DHEAS levels, together with conserved promoter sequences and transcription factor binding sites in enzyme-regulatory genes key in the DHEA/DHEAS production pathway, predicted that tissue-specific expression of these enzymes would localize similarly in humans and African apes [49].…”

“…A comparative gas-liquid chromatograph analysis of chimpanzee, orangutan, and rhesus macaque plasma supported the notion that great apes show the closest similarity in patterning of steroid sulfates as humans in pregnancy as well as postnatal life [44]. While early cross-sectional studies in captive chimpanzees [45] and studies of fecal samples collected from wild chimpanzees failed to replicate the finding of an age-related increase in DHEA/DHEAS similar to humans in chimpanzees [46], other studies have corroborated this finding – in bonobos [47] as well as chimpanzees [48, 21]. It has been proposed that relatively low levels of DHEA/DHEAS until later in postnatal life – a substrate that could be converted into other more potent androgens and estrogens – serves to delay the onset of puberty in chimpanzees and humans relative to macaques (see below).…”