As a second insult, hyenas were widely regarded as hybrids. Sir Walter Raleigh excluded them from Noah’s ark since he believed that God had only saved thoroughbreds. Hyenas were reconstituted after the flood through the unnatural union of a dog and cat. In fact, the three living species of hyena form a family of their own within the order Carnivora. They are most closely related to the mustelids (weasels and their allies).
As a final, phony blot on their escutcheon, and in the unkindest cut of all, many ancient writers charged that hyenas were hermaphrodites, bearing both male and female organs. Medieval bestiaries, always trying to draw a moral lesson from the depravity of beasts, focused on this supposed sexual ambivalence. A twelfth-century document, translated by T. H. White, declared:
Since they are neither male nor female, they are neither faithful nor pagan, but are obviously the people concerning whom Solomon said: “A man of double mind is inconstant in all his ways.” About whom also the Lord said: “Thou canst not serve God and Mammon.”
But hyenas also had some formidable defenders against this particular calumny. Aristotle himself had declared in the Historia animalium: “The statement is made that the hyena has both male and female sexual organs; but this is untrue.”
Aristotle—and not for the first time—was right of course. But the legend had arisen for a good reason. Female hyenas are virtually indistinguishable from males. Their clitoris is enlarged and extended to form an organ of the same size, shape, and position as the male penis. It can also be erected. Their labia have folded up and fused to form a false scrotum that is not discernibly different in external form or location from the true scrotum of males. It even contains fatty tissue forming two swellings easily mistaken for testicles. Authors of the most recent paper on spotted hyenas found the appearance of males and females “so close that sex could only be determined with certainty by palpation of the scrotum. Testes could be located in the scrotum of the male compared with soft adipose tissue in the false scrotum of the female.”
British zoologist L. Harrison Matthews wrote the most extensive anatomical description of the hyena’s sexual anatomy in 1939. He described the peniform clitoris, emphasizing that it is no smaller than the male penis, is equally constricted to a single slitlike opening at the tip, and is as subject to erection as its male counterpart. He concluded his dry and precise pages of description with as forceful a statement of wonder as measured British scientific prose would allow: “It is probably one of the most unusual of the forms which the external orifice of the urogenital canal takes amongst female mammals.”
Harrison Matthews also investigated the interesting question of how hyenas do it, given a female orifice no larger than the slit of a male’s penis. “In the pre-pubertal state,” he writes, “these functions are obviously impossible, owing to the minute size of the opening.” But as the female matures the slit gradually lengthens and “creeps down round the ventral surface…travelling down the midline” until it forms an orifice 1.5 cm long and extending from the tip of the clitoris to its base. This lengthening of the slit and a subsequent enlargement of the nipples following pregnancy and parturition help distinguish older females from males. We can now understand the basis for ancient myths that hyenas were either simultaneous hermaphrodites (bearing male and female organs at the same time) or male for part of their life and then female.
Nature’s oddities cry out for explanation, and we therefore ask what advantages females gain from looking like males. Immediately, we come upon the other most striking oddity of hyena biology: females not only resemble males, they are also larger than males, contrary to the usual pattern in mammals, including humans (but see essay 1 for a discussion of the reverse pattern in most other animals). Females in Kruuk’s East African clans averaged 120 pounds in body weight versus 107 pounds for males. Moreover, they lead the clans in hunting and defense of territory and are generally dominant over males in individual contacts. Dominance is not merely a result of larger size because females also rank higher than larger males if the discrepancy in size is not too great.
Similarity of male and female genitalia in the spotted hyena. Top row, views of the male penis. Bottom row, similar views of the female clitoris. FROM HARRISON MATTHEWS, 1939.
Although the female hyena’s assumption of what are usually male roles in mammals is probably related to its evolution of sexual structures that mimic male organs, the link between these phenomena is not immediately clear. It cannot have much to do with sexual performance itself for, if anything, the female “penis” is a hindrance to copulation until its opening enlarges and its form departs from that of the male.
Kruuk suggests that the strong mimicry arose in connection with a common behavior in hyenas called the “meeting ceremony.” Hyenas live in clans that defend territories and engage in communal hunting. But individuals also spend much of their time as solitary wanderers searching the landscape for carrion. To maintain cohesion in clans and to keep strangers away, hyenas must develop a mechanism for recognizing each other and reintegrating solitary wanderers into their proper clan.
External genitalia of female spotted hyena, showing peniform clitoris and false scrotum. FROM HARRISON MATTHEWS, 1939.
When two hyenas of the same clan meet, they stand side to side, facing in opposite directions. Each lifts its inside hind leg, subordinate individual first, exposing either an erect penis or clitoris, one of the most vulnerable parts of the body, to its partner’s teeth. They then sniff and lick each other’s genitals for ten to fifteen seconds, primarily at the base of the penis or clitoris and in front of the scrotum or false scrotum.
Kruuk believes that the female clitoris and false scrotum evolved to provide a conspicuous structure serving for recognition in the meeting ceremony. He writes:
It is impossible to think of any other purpose for this special female feature than for use in the meeting ceremony…. It may also be, then, that an individual with a familiar but relatively complex and conspicuous structure sniffed at during the meeting has an advantage over others; the structure would often facilitate this reestablishment of social bonds by keeping partners together over a longer meeting period. This could be the selective advantage that has caused the evolution of the females’ and cubs’ genital structure.
Speculation about adaptive significance is a favorite, and surely entertaining, ploy among evolutionary biologists. But the question, “What is it for?” often diverts attention from the more mundane but often more enlightening issue, “How is it built?” In this case, speculations about adaptive significance have been in the literature for a long time, yet no one bothered to tread the obvious path for hypotheses of anatomical construction until 1979: What sexual hormones are maintained at what levels by female hyenas from conception to maturity? (See Racey and Skinner, 1979, in bibliography).
Racey and Skinner found, in short, that two androgens (male-producing hormones) had higher concentrations in testicles than in ovaries of adult spotted hyenas (scarcely surprising). Yet, when they investigated levels of the same hormones in blood plasma, they detected no differences between males and females. One female contained twin female fetuses, and both had about the same level of testosterone as adult females. Racey and Skinner therefore conclude “that high foetal androgen levels are responsible for the appearance of the male sexual facies in adult female spotted hyenas.”
Racey and Skinner affirmed their hypothesis by studying brown and striped hyenas, the other two species of the family Hyaenidae. Neither brown nor striped hyenas develop peniform clitorises or false scrotums. In both species, androgen levels in blood plasma are much lower for females than for males. (Aristotle, by the way, defended hyenas against the charge of hermaphroditism by correctly describing the genitalia of these other species—something of a dodge with respect to the spotted hyena, the source of the legend; but “the master of them that know” was right in any case.)
But why should high levels of androgenic hormones lead to the construction of false penises a
nd scrotums? The animals that form them are still, after all, genetically female. How can female genes produce mimics of male structures, even in a milieu of high androgenic hormones? A look at the developmental basis of sexual anatomy resolves this dilemma.
Mammals share a common pattern for the embryology of sexual organs, and we may therefore use humans as an example. The early embryo is sexually indifferent and contains all precursors and structures necessary for the development of either male or female organs. After about the eighth week following conception, the gonads begin to differentiate as either ovaries or testes. The developing testes secrete androgens, which induce the development of male genitalia. If androgens are absent, or present at low levels, female genitalia are formed.
The internal and external genitalia develop in different ways. For internal genitalia, the early embryo contains precursors of both sexes: the Müllerian ducts (which form the Fallopian tubes and ovaries of females) and the Wolffian ducts (which form the vas deferens—the ducts that carry sperm from the testes to the penis—in males). In females, the Wolffian ducts degenerate and the Müllerian ducts differentiate; males develop by the opposite route.
The external genitalia follow a markedly different pattern. Individuals do not begin with two distinct sets of precursors and then lose one while strengthening the other. Rather, the different organs of male and female develop along diverging routes from the same precursor. The male’s penis is the same organ as the female’s clitoris—they form from the same tissues, are indistinguishable in the early embryo, and follow different pathways later. The male’s scrotum is the same organ as the female’s labia majora. The two lips simply grow longer, fold over and fuse along the midline, forming the scrotal sac.
The female course of development is, in a sense, biologically intrinsic to all mammals. It is the pattern that unfolds in the absence of any hormonal influence. The male route is a modification induced by secretion of androgens from the developing testes.
The mystery of male mimicry in female hyenas may be solved, in large part, by recognizing these fundamental facts of developmental anatomy. We know from the work of Racey and Skinner that female hyenas maintain high levels of androgenic hormones. We may therefore conclude that the striking and complex peculiarities of sexual anatomy in female spotted hyenas are simply, indeed almost automatically, produced by a single, underlying effect: the secretion of unusually large amounts of androgens by females.
The automatic nature of peniform clitorises and false scrotums in female mammals with high androgen levels can be illustrated by unusual patterns of human development. The adrenal glands also secrete androgens, usually in small amounts. In some genetic females, adrenals are abnormally enlarged and produce high levels of androgens. These baby girls are born with a penis and false scrotum. Several years ago a drug was placed on the market to prevent miscarriages. It had the unfortunate side effect of mimicking the action of natural androgens. Female babies were born with a greatly enlarged clitoris and an empty scrotal sac formed from the fused labia.
I believe that these facts of developmental anatomy must force a revision in the usual interpretation of male mimicry in female spotted hyenas. Evolutionary biologists have too often slipped into a seductively appealing mode of argument about the phenomenon of adaptation. We tend to view every structure as designed for a definite purpose, thus building (in our imagination) a world of perfect design not much different from that concocted by eighteenth-century natural theologians who “proved” God’s existence by the perfect architecture of organisms. Adaptationists might allow a little flexibility for tiny and apparently inconsequential structures, but surely anything big, complex, and obviously useful must be built directly by natural selection. Indeed, previous literature on spotted hyenas has assumed that female sexual organs evolved directly for a definite function—as in Kruuk’s speculation about the adaptive advantages of conspicuous external genitalia for recognition in the meeting ceremony.
But another scenario is possible and strikes me as more likely. I don’t doubt that the basic peculiarity of hyena social organization—the larger size and dominance of females—is an adaptation to something. The easiest pathway to such an adaptation would be a marked rise in the production of androgenic hormones by females (these exist in small amounts in all female mammals). High levels of androgens would entail complex secondary effects as automatic consequences—among them, a peniform clitoris and a false scrotum (we cannot, after all, label the same condition in some abnormal human baby girls as an adaptation). Once these effects are present, some use might be evolved for them—as in the meeting ceremony. But their current utility does not imply that they were built directly by natural selection for the purpose they now serve. (Yes, I know that my scenario might be run in reverse: conspicuous female genitalia are required for the meeting ceremony and are evolved by enhanced androgen levels, thus yielding large female size and dominance as a consequence. I do, however, point out that under our usual preferences for seeing direct adaptation everywhere, my scenario would not even be considered. Indeed, it wasn’t in the major works on spotted hyenas.)
We do not inhabit a perfected world where natural selection ruthlessly scrutinizes all organic structures and then molds them for optimal utility. Organisms inherit a body form and a style of embryonic development; these impose constraints upon future change and adaptation. In many cases, evolutionary pathways reflect inherited patterns more than current environmental demands. These inheritances constrain, but they also provide opportunity. A potentially minor genetic change—a rise of androgen level in this case—entails a host of complex, nonadaptive consequences. The primary flexibility of evolution may arise from nonadaptive by-products that occasionally permit organisms to strike out in new and unpredictable directions. What “play” would evolution have if each structure were built for a restricted purpose and could be used for nothing else? How could humans learn to write if our brain had evolved for hunting, social cohesion, or whatever, and could not transcend the adaptive boundaries of its original purpose?
In the second show of his Cosmos series, Carl Sagan told the tale of a Japanese crab that carries a portrait of a samurai warrior on its back. He argued that humans have built this face after their own image because local fisherman have been throwing back the most facelike crabs for centuries, thus imposing strong selection pressure for samurai look-alikes (the others get eaten). He used this example as a lead-in for a rapturous discourse on the pervasive power of natural selection.
I doubt this story very much and suspect that the conventional explanation is correct—that the resemblance is accidental and, at best, only slightly strengthened by human intervention. But even if Sagan were right, I believe that he is marveling at the wrong item (or at least failing to give equal time to another remarkable aspect of the case). I am most impressed by a crab’s ability to do such an uncrablike thing in the first place—just as the capacity of an inherited developmental system to produce (and so easily) such marked changes in the sexual anatomy of female hyenas grabs me far more than any putative adaptive significance for the change.
The capacity of crabs to make a face on their back did not arise from any selective value such a face might have, since crabs so rarely use this latent ability. Rather, this capacity reflects several deeper facts of crab biology: the bilateral symmetry of the carapace (corresponding by analogy with the bilateral symmetry of the human face), and the fact that many crabs are ornamented by creases along the midline (where a “nose” might form) and perpendicular to it (where “eyes” and “mouths” might be constructed).
The accidental production of a human portrait represents a stunning example of the evolutionary flexibility arising from consequences of an inherited design. Organic material is not putty and natural selection is not omnipotent. Each organic design is pregnant with evolutionary possibilities, but restricted in its paths of potential change. Fishermen might throw back selected starfishes with their five-part symmetry, or snails wi
th their spiral design, for tens of millions of years and never carve a samurai into their hard parts.
Peter Medawar has described science as the “art of the soluble.” Evolution might be labeled “the transformation of the possible.”
12 | Kingdoms without Wheels
SISERA’S MOTHER thought fondly of the booty that her son might bring back—“a prey of divers colors of needlework”—after meeting the armies of Israel led by Deborah and Barak (Judges, chapters 4–5). Yet he was overdue, and she began to worry: “Why tarry the wheels of his chariots?” she inquired anxiously. And rightly did she fear, for Sisera would never return. The Canaanite armies had been routed, while Jael had just transfixed Sisera through the head with a nail (a tent post in modern translations)—ranking her second to Judith among Jewish heroines for the gory dispatch of enemies.
Generals of the biblical armies rode on chariots; their apparatus traveled on carts. But two thousand years later, by the sixth century A.D., the question posed by Sisera’s mother could no longer be asked, for wheels virtually disappeared as a means of transportation from Morocco to Afghanistan. They were replaced by camels (Richard W. Bulliet, The Camel and the Wheel, 1975).
Bulliet cites several reasons for this counterintuitive switch. The Roman roads had begun to deteriorate and camels were not bound to them. Craftsmanship in harnesses and wagons had suffered a sharp decline. But, most important, camels (as pack animals) were more efficient than carts pulled by draft animals (even by camels). In a long list of reasons for favoring camels to nonmechanized transport by wheels, Bulliet includes their longevity, endurance, ability to ford rivers and traverse rough ground, and savings in manpower (a wagon requires a man for every two animals, but three to six pack camels can be tended by a single person).