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.