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Thursday, Sept. 19, 2002

NATURAL SELECTIONS

Reproduction is no laughing matter for hyenas


In some ancient African cultures, the skulking hyena was considered to have special powers. Some of those powers, it was thought, could be attained by consuming a specific part of the hyena's body. The nose, for example, was believed to be a source of wisdom and intelligence. While attributing "special powers" to the animals is probably a bit much for most people today, scientists have found that hyenas do exhibit a range of remarkable behaviors.

Hyenas are intelligent and highly social; the complexity of social interaction within their groups rivals that of primates. They take advantage of the vulture "spotter network" to find meat -- when they see vultures gliding down to earth, hyenas race them to reach the carcass. They display incredible patience when waiting to finish off sick or wounded animals in order to avoid putting themselves at risk.

This caution is all the more pronounced when they scavenge from human settlements and has earned the hyena a reputation as a craven, cowardly animal. This reputation -- one not helped by Disney films -- is ill-deserved. When they are hungry enough, hyenas are capable of running down and killing an adult zebra or wildebeest (a group of hyenas can devour the carcass, bones and all, in 30 minutes). Usually, though, they prefer to bide their time and follow the path of least resistance.

There is one important aspect of hyena behavior, however, that cannot be said to be easy: reproduction. This is explored by biological anthropologist Christine Drea and colleagues at Duke University in Durham, North Carolina. Hyena females have a unique reproductive tract, one that makes copulation so difficult, and giving birth so torturous, that it's surprising the animals haven't gone extinct.

The female spotted hyena lacks an external vagina. Instead, she urinates, copulates and gives birth through the tip of a penis-like clitoris so enormous that males and females are almost impossible to distinguish. The clitoris has a urethra, but a urethra, however large, is hardly a good substitute for a vagina. Females have such trouble during delivery that many first pregnancies result in stillbirths.

Despite this, the hyena is highly successful -- a fact all the more surprising given that the male faces a "mechanical challenge" (in the dryly descriptive term of the researchers) not only in getting into the right position to copulate (underneath the female) but in inserting his penis into the female's clitoris. And the female's fiery temperament only adds to his difficulties. Hyena females are strongly dominant over males, who approach their aggressive mates displaying what Drea characterizes as real fear.

As you might expect from a biological anthropologist, the emotions Drea ascribes to hyenas do not stop at fear. In a chapter she contributed to "The Smile of a Dolphin: Remarkable Accounts of Animal Emotions" (published by Random House/Discovery), Drea writes: "I've witnessed various hyenas behave in ways that might suggest affection, spite or even jealousy."

Describing how a male hyena behaved after being attacked by a dominant female, Drea wrote: "He met me at the fence, falling to his carpals and continuing with his cacophony, as though recounting the morning's ordeal. His body posture epitomized hyena submissiveness -- bared teeth in an open-mouthed appeasement grin, ears plastered to his head, the look of defeat in his stance. As I entered his pen, he glued himself to me. His hindquarters turned to jelly, he sank to the floor, and like any frightened creature, he relieved himself all over my boots."

Drea continues: "In scientific terms, he was a low-ranking hyena who had suffered the stress and acute changes in circulating cortisol concentrations brought on by social interactions with higher-ranking animals. In layman's terms, he was merely a frightened hyena who needed comforting."

As long ago as 1892, Darwin suggested similar ideas in "The Expression of Emotion in Man and Animals," but his ideas have long been neglected. Work like Drea's might start to confirm them.

Meanwhile, hyena studies might increase our knowledge in other fields, such as the basis of sex differences in animals.

Writing in last week's Proceedings of the Royal Society B, Drea and colleagues describe how a flood of androgens during fetal development produces the hyena's unique reproductive tract. These male sex hormones (testosterone is an androgen) lead to the extreme masculinization of the female hyena, both in her genitalia and in her behavior. To clarify the role of the sex hormones during development, the researchers injected fetal hyenas with anti-androgens (hormones that block the action of androgens). After this treatment, female hyenas were born with feminized anatomy, more similar to the usual mammalian type. This meant that when they gave birth, the fetus didn't have to make the dangerous passage through the urethra -- and stillbirths were drastically reduced.

However, the feminization of the female hyenas was not complete -- the overall structure of the genitals was the same, suggesting that there is something else contributing to their male-like form. Moreover, male fetuses exposed to anti-androgens were born with penises too short and the wrong shape for insertion into the female. In other words, in hyenas, naturally occurring androgens produce socially dominant females that have to undergo risky clitoral delivery, but the same androgens are essential to produce males with the correct reproductive anatomy to copulate.

What does this tell us? That evolution works by tradeoffs (one thing comes at the cost of another); that there is more to sexual differences than hormonal action -- and that dominant females will always have their way.

Rowan Hooper can be contacted at rowhoop@gol.com


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