Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating

Abstract

Among all extant mammals, only the female spotted hyena (Crocuta crocuta) mates and gives birth through the tip of a peniform clitoris. Clitoral morphology is modulated by foetal exposure to endogenous, maternal androgens. First births through this organ are prolonged and remarkably difficult, often causing death in neonates. Additionally, mating poses a mechanical challenge for males, as they must reach an anterior position on the female's abdomen and then achieve entry at the site of the retracted clitoris. Here, we report that interfering with the actions of androgens prenatally permanently modifies hyena urogenital anatomy, facilitating subsequent parturition in nulliparous females who, thereby, produce live cubs. By contrast, comparable, permanent anatomical changes in males probably preclude reproduction, as exposure to prenatal anti-androgens produces a penis that is too short and has the wrong shape necessary for insertion during copulation. These data demonstrate that the reproductive costs of clitoral delivery result from exposure of the female foetus to naturally circulating androgens. Moreover, the same androgens that render an extremely unusual and laborious process even more reproductively costly in the female are apparently essential to the male's physical ability to reproduce with a normally masculinized female.

Sexual Selection in Males and Females

“…One possibility is that the costs of female expenditure on competition or ornamentation depress fecundity or parental investment and that these effects constrain the development of secondary sexual characters below the level at which they have measurable costs to female survival (33). For example, where increased competitive success in females is associated with elevated testosterone levels, these may have adverse effects on the fecundity of females (63) or on the development of their offspring (64), which constrain the evolution of further increases. Contrasts in the operation of sexual selection in the two sexes raise the question of whether adaptations to intrasexual competition in females should be regarded as products of sexual selection.…”

Courtship and mating in free-living spotted hyenas

“…This unique female morphology makes intromission by the male considerably more difficult than it is in other mammals (Drea et al, 2002a) and also makes copulation by force physically impossible (East et al, 1993). Although a sexually receptive female hyena retracts her clitoris into the abdomen to permit penetration by the male's penis, her clitoral opening is far anterior to the position occupied by the external vagina in other female carnivores, so the male hyena typically experiences unusual difficulty locating this opening and achieving intromission (Drea et al, 2002a). Thus males must overcome the mechanical challenges posed by having to reach an anterior position on the female's abdomen during mating, and then achieving intromission at the site of the retracted clitoris (Drea et al, 2002a).…”

“…Second, female Crocuta possess heavily masculinized genitalia (Matthews, 1939). There is no external vagina, as the labia are fused to form a pseudoscrotum, and the clitoris is elongated and fully erectile such that it strongly resembles the male's penis in size and structure (Matthews, 1939;Neaves et al, 1980;Hamilton et al, 1986;Drea et al, 2002a). This pseudopenis is traversed to its tip by a central urogenital canal, through which the female urinates, copulates and gives birth (Drea et al, 2002a).…”

“…There is no external vagina, as the labia are fused to form a pseudoscrotum, and the clitoris is elongated and fully erectile such that it strongly resembles the male's penis in size and structure (Matthews, 1939;Neaves et al, 1980;Hamilton et al, 1986;Drea et al, 2002a). This pseudopenis is traversed to its tip by a central urogenital canal, through which the female urinates, copulates and gives birth (Drea et al, 2002a). This unique female morphology makes intromission by the male considerably more difficult than it is in other mammals (Drea et al, 2002a) and also makes copulation by force physically impossible (East et al, 1993).…”

“…This pseudopenis is traversed to its tip by a central urogenital canal, through which the female urinates, copulates and gives birth (Drea et al, 2002a). This unique female morphology makes intromission by the male considerably more difficult than it is in other mammals (Drea et al, 2002a) and also makes copulation by force physically impossible (East et al, 1993). Although a sexually receptive female hyena retracts her clitoris into the abdomen to permit penetration by the male's penis, her clitoral opening is far anterior to the position occupied by the external vagina in other female carnivores, so the male hyena typically experiences unusual difficulty locating this opening and achieving intromission (Drea et al, 2002a).…”