Sex and the Spotted Hyena
by Robin Meadows
Face to face with the spotted hyenas in the Berkeley hills, I find it hard to believe that these are the fearsome creatures I've been reading about for weeks. Where are the bone-crushing jaws and the propensity for a pack to strip a zebra in 15 minutes flat? These hyenas are fat and friendly, and are clearly interested in their human visitors, in a nonthreatening way. When biologist Laurence Frank enters an enclosure, he is encircled by three exuberant hyenas that look for all the world like large, shaggy, undisciplined dogs in search of love. My daughters and I are equally charmed. After my initial astonishment at the hyenas' amiability, however, I realize that this reception is not at all surprising. Frank bottle-raised this trio, which means he is the closest thing to a mother they have.
In the mid-1980s, Frank and his colleague Stephen Glickman captured 20 infant spotted hyenas in Kenya and brought them home to the University of California at Berkeley. The two researchers rightly anticipated that studies of captive hyenas would unravel the mysteries of these animals, which have been famous since the time of Aristotle for being hermaphrodites.
The misconception that spotted hyenas are bisexual was perpetuated well into the twentieth century by people from Hemingway, who as a writer of fiction can be excused, to biologists, who should have known better. The truth about spotted hyenas (Crocuta crocuta) is arguably as bizarre as the myth. To the untrained eye, females look and act almost exactly like males. The two sexes' remarkable resemblance goes right down to the nitty-gritty of their genitals, which appear to be identical. Moreover, the females of this species seem to be even more masculine than the males: Females are some 10 percent larger by weight and are so much more aggressive that they dominate males in nearly every social encounter, a fact that the Disney studio paid only lip service to when developing the hyena characters for last summer's animated movie "The Lion King." While the hyenas' ringleader was indeed female, her goofy sidekick should have been named Edwina rather than Ed. The Disney studio had ample opportunity to get it right because a team of illustrators came to Berkeley to sketch Frank and Glickman's brood.
More than mere curiosities, spotted hyenas challenge the conventional wisdom of what makes us female or male and so can give us insights into the limits and latitudes of our own sexuality. Many biologists who study female-male differences let their preconceptions affect their results. For instance, while testosterone and other so-called "male" hormones are quite common in female mammals, biologists almost always focus on their estrogen and other so-called "female" hormones, notes Frank.
Despite their dog-like appearance, the three species of hyenas belong to a superfamily that includes cats, mongooses, and civets. Spotted hyenas are named for the dark brown spots that stand out against their short, brownish-yellow fur. The demented-sounding cackle they make when squabbling gives them their other common name, the laughing hyena. Spotted hyenas live in the savannas and woodlands of sub-Saharan Africa, and their range overlaps with those of the other two species of hyenas, the striped and brown hyenas (Hyaena hyaena and Parahyaena brunnea). All three species have the long necks, powerful shoulders, and short hindlegs that give hyenas their characteristic attenuated look. Likewise, all hyenas are consummate scavengers, noteworthy for being the only carnivores that can ingest a carcass in its entirety. While carnivores' digestive tracts are typically short, those of hyenas are uncommonly long and are capable of extracting nearly all the protein and fat from bones. The mineral components of bone are reduced to a fine powder that is excreted, while the hair, ligaments, and other undigestible body parts are regurgitated in a pellet.
Spotted hyenas are distinguished from their relatives in two major ways. While striped and brown hyenas supplement their diets by catching small prey from insects to foxes, these species are predominantly scavengers. In contrast, spotted hyenas hunt for most of their food and usually prey on large animals. A single spotted hyena can catch an adult wildebeest after chasing it three miles at speeds of up to 35 miles per hour.
The second major difference is, as already mentioned, that female spotted hyenas have in many ways adopted the orthodox male role. Female spotted hyenas bear, suckle, and care for their young like any female mammal. But although their genitals are clearly female in function, they are male in form. The labia are fused into what looks like a scrotum, complete with two pads of fatty tissue that resemble testes. In addition, the clitoris is elongated to the point that it is nearly the size of a male's penis and is likewise fully erectile. Astonishingly, females mate and give birth through the long, narrow canal running down the center of this "pseudopenis." During mating it retracts much like a shirt sleeve being pushed up, and during birth it stretches so much that it looks like a water balloon. "From a human perspective, the process can be thought of as giving birth through an unusually large penis," says Frank.
While highly unusual, spotted hyenas are not as anomalous as they appear to be at first glance. Rather, they are at the extreme end of a continuum of female mammals with masculine characteristics. One-quarter of mammalian families contain species in which females are larger than males, and there are other female mammals with genitals that are masculinized to some degree. For instance, spider monkeys have a large, pendulous clitoris and the European mole has an elongated penis-like clitoris.
In addition to having male-like genitals, female spotted hyenas enjoy the social position accorded to males in most mammal species: dominance. Except for when they are ready to mate, female spotted hyenas completely dominate the adult males that join their clan. (As is true of many social mammals, female hyenas stay in the clan where they were born while males disperse when they reach puberty at about two years of age.) Most tellingly, males abandon kills once females show up--Frank has seen a single juvenile female keep five full-grown males from feeding on a buffalo carcass. Males typically skirt the edges of kill sites, snatching scraps dropped by females.
Aggression is a way of life for female spotted hyenas. "Rank is inherited from mothers, and higher-ranking females teach youngsters what their rank is through aggression," says Frank. "A mother-daughter pair or two sisters will attack a subordinate when her young are around [which teaches the subordinate's young where they stand]." Dominant females threaten a subordinate by walking toward her shoulder-to-shoulder with their manes and tails raised.
While many such displays are just meant to show who's boss, subordinates sometimes sustain considerable damage. After being separated for a few hours, spotted hyenas engage in "greeting" displays that entail lifting their legs and exposing their erect pseudopenises for inspection. Subordinate females often initiate greetings and this is the only known case
of an erection being a submissive gesture. "This unusual display is not without its risks [because] each hyena puts its reproductive organs in immediate proximity to very powerful jaws," says Frank. "On the rare occasions when the aggression escalates to fighting, the resulting damage may be severe enough to destroy or seriously compromise the reproductive competence of the injured party."
The big questions about spotted hyenas are obvious. Why do the females sport such extraordinary anatomy and behavior? And why are hyenas the only mammals with females that are masculinized to such an extreme degree? Attempts to answer the first question were confounded until Frank, who coordinates the field work, and Glickman, who directs the project, established their hyena colony. Studies on the 40-odd captive hyenas are explaining the physiological basis of behaviors that Frank and his colleagues have seen in their 16-year field study of spotted hyenas in the Talek clan living in Kenya's Masai Mara National Reserve.
One of Frank and Glickman's most striking findings is that compared to males, female spotted hyenas have much higher blood levels of a steroid hormone called androstenedione, which is an androgen or classically "male" hormone. Androstenedione is particularly interesting because it can be metabolized into either the "male" hormone testosterone or the "female" hormone estrogen depending on what enzyme is present: One enzyme converts androstenedione to estrogen, while another converts it to testosterone.
Placentas typically contain both enzymes but Glickman, University of California at Berkeley endocrinologist Paul Licht, and colleagues at the University of California at San Francisco, found that the balance is skewed in spotted hyenas. Human placentas (and presumably those of most mammals) convert maternal androgens to estrogen, thus protecting female fetuses from being masculinized. Spotted hyena placentas, on the other hand, actually convert the maternal androstenedione to testosterone.
Testosterone's effect on female fetuses has been well-documented in laboratory studies. Prenatal exposure to testosterone in female rats, dogs, and monkeys causes male-like genitals as well as increased body size, aggression, and dominance--in short, the suite of characteristics found in female spotted hyenas.
However, science is just like any other part of life in that the answers are not always easy. As the pundits say, there are three kinds of logic: deductive, inductive, and "seductive," that is, plausible but not necessarily true. The third kind of logic may apply to the argument that female spotted hyenas are masculinized due to prenatal exposure to testosterone. "Everything we know about sexual differentiation is simple: Testosterone makes males," says Frank. "But because of a whole series of hints, it looks like that may not be the whole picture in spotted hyenas." One of these hints is that treatments that reduce penis size in other species--prenatal exposure to compounds that inhibit androgens, and castration before puberty--have little effect on genital size in either sex in spotted hyenas. Such findings have led the researchers to speculate that, "an as yet undiscovered novel mechanism may contribute to sexual differentiation in this species." That is, the answers are not yet in on what separates the girls from the boys.
Frank and Glickman's studies of the captive spotted hyenas have also led to the surprising discovery that they fight violently at birth. The young of predatory birds including boobies, eagles, and egrets are known to attack and ultimately kill their younger siblings soon after hatching, which may be because the second egg serves only as parental insurance in case the first fails to hatch. However, this is the first such case known in mammals. Spotted hyenas typically give birth at the mouths of abandoned aardvark burrows, which are filled with passages that narrow as they diverge from the entrance. While the burrows protect the babies from lions and other hyenas, the narrow passages also prevent the mother hyena from reaching her cubs. When ready to nurse, she lies at the entrance and makes a low, groaning sound to call her babies to the surface. After the baby hyenas have lived in the security of their burrow for a few weeks or so, their mother carries them to a communal den shared by other hyena young.
Although spotted hyenas usually have twins, observations during the first decade of the Talek clan field study showed that mothers brought many more single cubs to the communal den than expected. Instead of being mostly twins, by a few weeks of age, more than 40 percent of the litters comprised lone cubs.
What was happening during those initial weeks in the aardvark burrows where the cubs were born? Because the narrow passages make the burrows inaccessible to predators and biologists alike, Frank was unable to solve this puzzle until the first hyenas were born in the Berkeley colony. Then he saw that unlike most carnivores, which are helpless at birth, spotted hyenas are born with both the equipment and inclination to attack. Their eyes are open, their incisors and canine teeth are fully erupted, and they are able to bite within minutes of birth. And bite they do, dotting each other's shoulders and necks with tell-tale puncture wounds until dominance is established. This aggression notwithstanding, spotted hyenas don't kill their siblings directly. Rather, the subordinate sibling is so cowed by the constant attacks that it stays away from the burrow entrance and so from its mother, which means it ultimately starves to death. In the wild, as many as one-quarter of all cubs apparently die in the depths of their natal aardvark burrows.
While Frank and Glickman have made considerable progress in determining the physiological basis for the female spotted hyenas' masculinization, the answer to why spotted hyenas are the only mammals with females that are so extremely masculinized is not as clear. The generally accepted theory is that the masculinization is a consequence of the species' highly competitive communal feeding. Higher-ranking females and their young get to eat first, and the argument goes that this favors increased aggression in females, which in turn favors increased "male" hormones in females. According to this scenario, the females' masculinized genitals and intense aggression from birth are just side-effects of the increased androgens. However, Frank cautions that many other carnivores also eat together, suggesting that competition for food is not the only reason behind the female spotted hyena's masculinization. "The ancestral spotted hyenas' endocrinology must have preadapted them to this development," says Frank.
Whatever the cause, female masculinization is apparently a very successful strategy for the spotted hyena, which is the most abundant large predator in its range. But this success comes at a cost that is tremendously high for the spotted hyena--and presumably prohibitively high for other species. Notably, giving birth is difficult and dangerous, especially for first-time mothers. The fact that the pseudopenis has such a long, narrow birth canal is enough to make it a poor organ for delivering a baby. But there is the added complication that the end of the pseudopenis cannot stretch enough to accommodate passage of the baby: In a first-time mother, the baby tears its way out. "It's the only time I've ever heard hyenas cry out in pain," notes Frank.
Even worse, the umbilical cords are so short that many first-born babies die. At only six-inches long, the umbilical cord is far too short to traverse the foot-long canal down the pseudopenis, which means that either the placenta detaches or the cord breaks before the baby is born. (For comparison, in women the birth canal is only a few inches long and the umbilical cord is a generous foot and a half long.) The longer a hyena's labor, the more likely her baby is to suffocate and be stillborn--and the more likely the mother is to die. In captivity, first-time mothers labor as long as 48 hours and nearly three-quarters of first-born cubs die. Without veterinary help, many of these mothers probably would have died along with their babies; in the wild, many females die at three to four years, the age when hyenas typically first give birth.
The high rate of siblicide is another significant cost to the female spotted hyena's masculinization. Producing babies that die shortly after birth is a tremendous waste of a mother's energy. Intriguingly, female spotted hyenas have apparently managed to wring what advantage they can out of their babies' inclination to kill each other. Frank believes that mothers use siblicide to manipulate the sex ratio of their offspring.
It is well known that many female mammals bias the sex ratio of their offspring. Biologists speculate that, for example, having sons may be advantageous to bushbabies, muskrats, and other species in which daughters grow up to share territories with--and so compete for resources with--their mothers. Frank found that high-ranking females in the Talek clan generally raised more sons than daughters when the population of the clan was high. But since 1990, when about a third of the adult females left to establish a new clan, high-ranking females in the Talek clan have raised more daughters than sons.
However, while most species somehow adjust the sex ratio before their babies are born, spotted hyenas appear to adjust the sex ratio of their babies after birth. Frank has seen that in the wild, female spotted hyenas sometimes put newborn twins into separate aardvark burrows, which keeps the babies from fighting and so greatly increases the likelihood that both will survive. The implication is that mother hyenas can intervene and save their babies if they are the desired sex. Ever since they were mistaken for hermaphrodites, spotted hyenas have been among the most misunderstood species on earth. Most people follow the lead of the Disney script-writers and cast hyenas as the bad guys of the animal world for their gruesome lifestyles. But as Frank and Glickman's work shows, the qualities for which they are reviled seem to arise from a noble goal: Like any mothers, the female hyenas are just trying to provide the best for their children. As for the rest, spotted hyenas, like many of us, are largely captives of their biology.
Robin Meadows is a contributing editor to ZooGoer.
(ZooGoer 24(3) 1995. Copyright 1995 Robin Meadows. All rights reserved.)
