Scientists of antiquity believed that spotted hyenas were hermaphrodites (having both male and female reproductive organs). The mistake is understandable because from birth, the female hyena has a clitoris that is as large as the penis of males (as Figure 1 shows), through which she urinates, receives semen, and gives birth. Female hyenas are also larger, more aggressive, and socially dominant over males.
What difference in the hyena’s prenatal development causes this sexual monomorphism? In other mammals the placenta rapidly aromatizes androgens into estrogens; this conversion may be a way to protect the mother and fetal females from androgens produced by fetal males. But the spotted-hyena placenta is remarkably deficient in the aromatase enzyme (Licht et al., 1992).
Because the hyena mother produces large amounts of the androgen androstenedione (Glickman et al., 1987), and the placenta fails to convert the androstenedione to estrogens, all the fetuses receive considerable amounts of androgens, which may help account for their masculine appearance. (However, female hyenas treated prenatally with androgen-blocking drugs still develop masculinized exteriors [Drea et al., 1998], suggesting that an additional mechanism must be involved.) One remarkable observation is that female pups, which are born with teeth, fight viciously with siblings immediately from birth. Sisters fight particularly violently, and in wild populations it is common for a pup to kill its sibling (Frank et al., 1991), at least during periods when food is scarce (Smale et al., 1999). It remains to be established whether this extreme aggression is due to prenatal stimulation of the brain with androgens.
Even if the extreme aggressiveness of the female hyena is due to fetal androgens, females do mate with males, so their brains have not been made permanently unreceptive (as would happen in prenatally androgenized rats). Indeed, female hyenas seem to have a typically feminine sexually dimorphic nucleus of the POA (SDN-POA) (Fenstemaker et al., 1999) and spinal nucleus of the bulbocavernosus (SNB) (Forger et al., 1996) (see the textbook). Just the same, mating in the spotted hyena is a tense affair: the female seems to just barely tolerate the male’s proximity, and the male alternates between approaching and retreating from his alluring but dangerous mate.
Drea, C. M., Weldele, M. L., Forger, N. G., Coscia, E. M., et al. (1998). Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti-androgens. Journal of Reproduction and Fertility 113: 117–127.
Fenstemaker, S. B., Zup, S. L., Frank, L. G., Glickman, S. E., et al. (1999). A sex difference in the hypothalamus of the spotted hyena. Nature Neuroscience 2: 943–945.
Forger, N. G., Frank, L. G., Breedlove, S. M., and Glickman, S. E. (1996). Sexual dimorphism of perineal muscles and motoneurons in spotted hyenas. Journal of Comparative Neurology 375: 333–343.
Frank, L. G., Glickman, S. E., and Licht, P. (1991). Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science 252: 702–704.
Glickman, S. E., Frank, L. G., Davidson, J. M., Smith, E. R., et al. (1987). Androstenedione may organize or activate sex-reversed traits in female spotted hyenas. Proceedings of the National Academy of Sciences, USA 84: 344–347.
Licht, P., Frank, L. G., Pavgi, S., Yalcinkaya, T. M., et al. (1992). Hormonal correlates of “masculinization” in female spotted hyenas (Crocuta crocuta). 2. Maternal and fetal steroids. Journal of Reproduction and Fertility 95: 463–474.
Smale, L., Holekamp, K. E., and White, P. A. (1999). Siblicide revisited in the spotted hyaena: Does it conform to obligate or facultative models? Animal Behaviour 58: 545–551.