Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys.

Aspects of the prenatal environment, including steroid hormones, modulate the timing of puberty onset in many mammalian species. This study tested whether prenatal androgen manipulations altered pubertal development in male rhesus macaques (Macaca mulatta). Pregnant females received testosterone enanthate (TE), the androgen receptor blocker flutamide, or vehicle during one of two periods of gestation, and their male offspring were observed for morphological, endocrine, and behavioral development from 3 to 4.5 years of age. Males exposed to flutamide early in gestation had a greater response to exogenous GnRH prepubertally, and greater testes volume, elevated testosterone, and elevated LH at age 3.5 than did control subjects. Males exposed to flutamide late in gestation also had greater testes volumes at age 3.5 than did control males. However, these differences between flutamide treated males and control males did not persist postpubertally. By 4.5 years of age, development in control males had reached comparable levels to that of flutamide-treated males. Late gestation treatment with TE had no effect on morphological pubertal development but early TE treatment altered some aspects of endocrine function during puberty. None of the prenatal androgen manipulations affected sexual behavior. These findings suggest that prenatal androgens, in conjunction with social factors, masculinize pubertal timing in rhesus monkey males.

Variation in reproductive traits is associated with short anogenital distance in female rats.

Anogenital distance was used as a biomarker for natural variation in prenatal androgenization of female rats and was associated with individual differences in a suite of reproductive characteristics. Females with short anogenital distances were likely to have first vaginal estrus earlier than females with longer anogenital distances and to have first vaginal estrus on the same day as vaginal opening. In young adulthood, females with short anogenital distances had shorter ovarian cycles and less intense lordosis reflexes in response to manual palpation than those with longer anogenital distances, but only when living individually, not in groups. Taken together, these findings indicate that prenatal androgenization affects reproductive traits throughout the life span.

Peak occurrence of female sexual initiation predicts day of conception in rhesus monkeys (Macaca mulatta).

The present study investigated whether peaks in female sexual initiation could accurately predict conception in group-living female rhesus monkeys. Behavioral observations, 4 or 5 days per week in large, stable, social groups of monkeys, provided frequencies of female initiation of proximity, sexual solicitation, mounts, and ejaculations. Since a preovulatory peak in female sexual initiation is likely linked to the preovulatory oestradiol surge, we used the third day after a peak in behavior as the behavioral estimate of conception date. For each pregnancy, an independent estimate of conception date was derived from ultrasound determination of fetal length. Estimates of conception based on female initiation of proximity with adult males were accurate for more than 90% of pregnancies, whereas observation of ejaculations by males predicted conception in fewer than 60% of pregnancies. Behavioral and ultrasound estimates of conception date were highly correlated and differed by less than I day on average. Accordingly, predictions of delivery date based on behavioral estimates of conception date were as accurate as those based on ultrasound-derived estimates. These data suggest that female-initiated sexual behavior can be used in rhesus monkeys as a practical, non-invasive tool for producing timed matings in social groups of monkeys, providing accurate estimates of conception date, gestational age, and predicted date of birth.

Estradiol increases female sexual initiation independent of male responsiveness in rhesus monkeys.

Copulation and female initiation of sexual behavior vary across the ovarian cycle, suggesting that female hormonal condition influences female sexual motivation in rhesus monkeys. However, the effects of hormones on female sexual motivation are difficult to identify because male behavior also varies with female hormonal condition. During the nonbreeding season, male rhesus monkeys are sexually unresponsive to females; thus the effects of estradiol treatment on female sexual motivation can be examined independent of male behavior. This study administered estradiol to five ovariectomized females living in a large age-graded social group during the nonbreeding season. The behavior of these females with and without estradiol treatment was compared. Data were collected concurrently on five intact, noncycling, nonpregnant females. Estradiol treatment significantly increased sexual initiation by ovariectomized females toward males without any significant changes in male behavior. Estradiol-treated females also displayed greater sexual initiation than nonpregnant, intact females. Both estrogen and progesterone were important predictors of sexual initiation in females, with progesterone having an inhibitory effect. Endogenous progesterone levels in females were negatively correlated with male contact behavior, suggesting that female attractiveness is reduced by progesterone. This study provides further support for estrogen as the critical steroid increasing female sexual motivation in primates.

Maternal responsiveness increases during pregnancy and after estrogen treatment in macaques.

Maternal responsiveness in primates has long been considered emancipated from endocrine factors and entirely dependent on experience and cognition. Here we report that group-living pigtail macaque females increased their rate of interaction with infants in the last weeks of pregnancy in correspondence with an increase in plasma levels of estradiol and progesterone. Estrogen treatment increased the rate at which ovariectomized rhesus females interacted with infants. This is the first evidence that steroid hormones influence maternal responsiveness in anthropoid primates. All untreated ovariectomized females and nonpregnant females interacted with infants, indicating that although estrogen can enhance responsiveness to infants, ovarian or pregnancy hormones are not necessary for the expression of infant-directed behavior in female macaques. The findings of this study suggest fundamental similarities, rather than differences, in the endocrine modulation of maternal responsiveness in primates and other mammals.