Fetal androgens and sexual mimicry in spotted hyaenas (Crocuta crocuta)

Abstract

Sexual differentiation of the Müllerian duct system and gonad in female fetuses conformed to the general mammalian pattern, whereas the external genital anlage in male and female fetuses developed into the male facies. Interstitial cells occurred in the primary germinal cords of both male and female fetal gonads and are suggested to be the source of androgen production in spotted hyaena fetuses. Maternal transfer of androgens to the fetus via the placenta was negligible. Male fetuses had higher gonadal and plasma concentrations of testosterone than female fetuses, and vice versa for androstenedione. Plasma testosterone was nearly as high in a female 31-day-old fetus as in the twin male, and masculinization of the genital tubercle probably results from an episode of androgen secretion by the fetal gonad although the Wolffian ducts in the female do not respond.

Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta). 2. Maternal and fetal steroids

“…For example, 'testosterone' concen¬ trations were slightly higher in the males of mixed-sex twins (Lindeque & Skinner, 1982; this study). Secondly, 'testosterone' concentrations dropped more in a female fetus than in a male fetus after disconnection from the placenta, although the 10 min difference in sampling time complicates interpretation of these data.…”

“…Increments in androgens and other steroids during pregnancy are common in many mammalian species. During our studies, there were marked increments in several androgens, oestrogen and progesterone during pregnancy, which were not fully appreciated by earlier more limited measurements on hyaenas (Racey & Skinner, 1979;Lindeque & Skinner, 1982). Androgens, in particular, could have important effects on the developing fetus, since female spotted hyaenas have conspicuously masculinized genitalia at birth.…”

“…Matthews (1939) first suggested that the masculinization of female hyaenas might be caused by androgens secreted by the maternal ovary, but Racey & Skinner (1979) rejected this hypothesis because of the low concentrations of androgens in the maternal ovary and adrenal gland; they proposed that the fetal ovary or adrenal gland was the primary source of these androgens. This conclusion, which tends to diminish the importance of the high androgen in the mother, was reiterated by Lindeque & Skinner (1982) based on comparisons between several maternal and fetal samples. First, they note that maternal 'testosterone' was about six times lower than concentrations in fetal blood (approximately 1 -4 versus 5 ng ml~l ) in a set of twins estimated to be 31 days of gestational age; values were comparable in presumed male and female fetuses.…”

“…Repetitive blood samples were obtained, before and after removal of the fetus and placenta, from maternal peripheral, uterine and ovarian veins to evaluate placental contri¬ butions to plasma steroids. Measurements were also obtained from the fetal umbilical and peripheral circulation to examine potential androgenic influence on the fetus of maternal or placental activity and to evaluate the claim (Lindeque & Skinner, 1982) that there was no significant maternal androgenic contribution to the fetus.…”

“…Androgens, in particular, could have important effects on the developing fetus, since female spotted hyaenas have conspicuously masculinized genitalia at birth. Racey & Skinner (1979) and later Lindeque & Skinner (1982) concluded that the fetal ovaries are the primary source of androgens and masculinize the fetal hyaena. To examine further the contributions of the placenta to circulating steroid concentrations, we analysed steroids in plasma from several compartments of the maternal and fetal circulations.…”