Prenatal androgen exposure and parental care interact to influence timing of reproductive maturation in marmosets

Abstract

The timing of reproductive maturation is susceptible to hormonal and environmental influences, and variation in this timing can be partially attributed to the prenatal and post-natal environment. We examined associations between prenatal steroid exposure and the post-natal family environment on the variability in reproductive maturation timing in young marmosets (Callithrix geoffroyi). Urine samples from pregnant females were analyzed for cortisol (CORT) and androgens (uA). Post-natal uA was measured in males to determine age (in days) of adult-like levels of androgens associated with spermatogenesis; post-natal pregnanediol glucuronide (PdG) was measured in females to determine age (in days) of first ovulation. Maternal, paternal, alloparental, and total care (carrying, grooming, and rejection/removals) of offspring were observed. Female offspring exposed to lower prenatal uA levels and higher paternal grooming and lower maternal rejection/removals showed later first ovulation, whereas female offspring exposed to higher prenatal uA showed earlier first ovulation. Male offspring showed earlier reproductive maturation as paternal grooming increased, regardless of first trimester uA exposure. Male offspring exposed to low prenatal uA levels showed earlier reproductive maturation as maternal rejections/removals increased. In offspring exposed to low prenatal CORT, high total carrying predicted earlier first ovulation in females, but later reproductive maturation in males. Total carrying duration did not affect timing of reproductive maturation in offspring exposed to high third trimester CORT levels. Our findings expand the evolutionary theory of socialization by demonstrating that the effect of post-natal family environment on timing of reproductive maturation depends on prenatal uA exposure and also influences reproductive maturation timing in male offspring.

Cross-cultural evidence does not support universal acceleration of puberty in father-absent households

“…The simplest hypothesis about lack of paternal investment in childhood, therefore, is that this will delay children's development—assuming that early reproductive debut will increase lifetime reproductive success, which is a common finding, at least for women, across human populations [56]. This very simple explanation for the influence of paternal investment on the reproductive maturation of offspring has been tested, and appears to hold, in some other species that also have paternal care: yellow baboons [57], prairie voles [58] and male (but not female) marmosets [59].…”

“…[107]). Low levels of paternal care have also been shown to delay maturation in male marmosets, in comparison with higher levels of paternal care [59]. But there are some studies which suggest that stress and psychosocial adversity in early life may accelerate reproductive development in non-human species [108]: female rats accelerate reproduction—though male rats delay—with disrupted maternal investment [93]; and in female marmosets, lower levels of paternal care accelerate maturation.…”

Prenatal androgen excess impairs beta-cell function by decreased sirtuin 3 expression

“…As a heritable disease, the transmission of PCOS-like features from mothers to their daughters was confirmed by many recent studies (Crisosto et al 2019, Risal et al 2019, Mimouni et al 2021. Hyperandrogenism during the maternal stage was also reported to cause disorders in the endocrine system, reproductive system, and even nervous system of their offspring (Hu et al 2015, Hakim et al 2017, Huffman et al 2017, Sun et al 2020. Androgen treatment during the late gestational stage produced female F1-F3 offspring with PCOS-like reproductive and metabolic disorders, suggesting that androgen excess also has transgenerational effects (Risal et al 2019).…”

Cross-cultural evidence does not support universal acceleration of puberty in father-absent households

“…The simplest hypothesis about lack of paternal investment in childhood, therefore, is that this will delay children's development-assuming that early reproductive debut will increase lifetime reproductive success, which is a common finding, at least for women, across human populations [56]. This very simple explanation for the influence of paternal investment on the reproductive maturation of offspring has been tested, and appears to hold, in some other species that also have paternal care: yellow baboons [57], prairie voles [58] and male (but not female) marmosets [59]. While data on puberty are relatively scarce in the anthropological literature, several anthropologists have tested this simple model of paternal investment on behavioural measures of reproductive maturation such as the timing of first birth or first sex, and found that the absence of fathers is associated with delayed first births (in women: Gambia horticulturalists [60], Ache hunter -gatherers [52], pre-industrial Finns [61]; in men: Maya, Belize [51]; in both sexes: matrilineal Mosuo of southwest China [62]).…”

“…[107]). Low levels of paternal care have also been shown to delay maturation in male marmosets, in comparison with higher levels of paternal care [59]. But there are some studies which suggest that stress and psychosocial adversity in early life may accelerate reproductive development in nonhuman species [108]: female rats accelerate reproductionthough male rats delay-with disrupted maternal investment [93]; and in female marmosets, lower levels of paternal care accelerate maturation.…”