Sexual Mimicry in Hyenas

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Citation Muller, Martin N, and Richard Wrangham. 2002. “Sexual Mimicry In Hyenas.” The Quarterly Review of Biology 77 (1): 3–16. https:// doi.org/10.1086/339199.

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SEXUAL MIMICRY IN HYENAS

Martin N. Muller Department of Anthropology, Peabody Museum, Harvard University Cambridge, Massachusetts 02138 USA e-mail: [email protected]

Richard Wrangham Department of Anthropology, Peabody Museum, Harvard University Cambridge, Massachusetts 02138 USA e-mail: [email protected] keywords sexual mimicry, spotted hyenas, androgenization, genital masculinization, monomorphism, siblicide, infanticide, natural selection, adaptation abstract Genital masculinization in female spotted hyenas has been widely explained as an incidental consequence of high androgen levels. High androgen levels, in turn, were supposed to be favored because they led to adaptive aggressive behavior. Incidental androgenization is no longer a tenable hypothesis, however, because genital masculinization has been shown to proceed in the absence of androgenic steroids. Thus, an alternative hypothesis is required. The genitals of spotted hyena females are not simply masculinized, but exhibit a detailed physical resemblance to the male genitalia. In the absence of satisfactory alternative explanations, we propose that selection may have favored sexual mimicry in females because they are more likely than males to be targets of aggression from other females. Male- like camouﬂage could theoretically be protective in three contexts: neonate sibling aggression, infanticide by conspeciﬁc females, and interclan territoriality. Current data suggest that if sexual mimicry is important, its effects are strongest among infants.

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EMALE SPOTTED HYENAS (Crocuta cro- tinguishable, though females are heavier Fcuta) present an unsolved puzzle because (Mills 1990; Glickman et al. 1993). they exhibit one of the most extraordinary genital morphologies of any mammal. In this The Nonadaptive Hypothesis review we show that as a result of recent ex- Although a number of adaptive hypotheses periments, the principal previous explana- have been proposed to account for the male- tion for their male-like genitals is no longer like genitalia of spotted hyena females, none viable. This leads us to suggest a new expla- has proved convincing (see below). Instead, nation, that female mimicry of males serves the predominant explanation is that male- to protect females from lethal aggression by like genitals are a nonfunctional conse- same-sex rivals. quence of androgenization. This hypothesis was prompted by Racey and Skinner’s report Sexual Monomorphism that serum testosterone levels in female spot- in Spotted Hyenas ted hyenas are as high as those in males (Ra- Male spotted hyenas have a long and some- cey and Skinner 1979). Racey and Skinner times prominent penis. Female spotted hye- also found that females in two other species nas have a clitoris of similar size, shape, and of hyena (striped hyenas, Hyaena hyaena, and erectile ability. They have no external vagina. brown hyena, Hyaena brunnea) do not de- Instead, females urinate, mate, and give birth velop masculinized genitalia, are not system- through the urogenital canal, which extends atically dominant to males (Mills 1990; Owens through the length of the clitoris. In addition and Owens 1996), and have much lower tes- to the pseudopenis, females have a pseudo- tosterone levels than males. They therefore scrotum created by fusion of the external la- suggested that high androgen levels in spot- bia. Fat and connective tissue inside the pseu- ted hyena females might be responsible for doscrotum bear a striking resemblance to the both their dominance and their masculinized male hyena’s testes, but are distinguishable genitalia. from these by palpation (Matthews 1939; Gould and Vrba (1982) extended Racey Deane 1962; Wickler 1969; Kruuk 1972; and Skinner’s proposal to argue explicitly Frank 1996). This suite of characteristics that the enlarged clitoris of female hyenas is makes females so male-like that close exami- nonadaptive (see also Gould 1981). They nation of the shape of the urethral meatus, noted that in the standard course of mam- the phallic glans, or the scrotum is often re- malian sexual differentiation, female exter- quired to differentiate the sexes (Frank et al. nal genitalia develop in both sexes in the ab- 1990). It is particularly difficult for field ob- sence of androgens. Androgens produced by servers to discriminate infants, juveniles, and the fetal testes are necessary for the normal subadults (Kruuk 1972; Frank 1996). development of a penis and scrotum from the Spotted hyena females exhibit a second un- undifferentiated genital tubercle and genital usual trait that has been argued to relate to folds (Wilson et al. 1981). In humans, rare dis- genital masculinization: they are more ag- orders such as congenital adrenal hyperplasia, gressive than males (Frank 1996). Hyena which produce excess androgens in the fetal clans maintain linear dominance hierarchies circulation, can cause enlarged clitorises and in which adult females are dominant to adult false scrotums in females (Breedlove 1992). males in nearly all social interactions (Kruuk Similar structures, including pseudopenises 1972; Tilson and Hamilton 1984; Frank 1986; with erectile function, are exhibited by female Henschel and Skinner 1987; Smale et al. dogs exposed to high levels of androgens in 1993). They regularly displace males from utero (Beach et al. 1983). In many mammals, kills, so effectively that Frank (1996) has ob- exposure to androgens during critical pe- served a single subadult female prevent as riods of development also leads to increased many as five adult males from feeding on a body weight and enhanced aggression (Mon- carcass. Female dominance over males occurs aghan and Glickman 1992). Thus, Gould even though the two sexes are similar in size. (1981) argued that if selection had favored Specifically, their linear dimensions are indis- high levels of circulating androgens in female March 2002 SEXUAL MIMICRY IN HYENAS 5 hyenas for reasons related to dominance, an high levels of circulating androgens in female enlarged clitoris and pseudoscrotum would hyenas if they increased body size and ag- be “automatically produced.” This explana- gressiveness, even at the expense of masculin- tion has been widely accepted. For example, ized genitalia. “the female phallus may have originated as an unselected side effect of selection for Collapse of the Nonadaptive androgen-mediated bellicosity, a major ad- Hypothesis vantage in the extraordinary competitive hy- Further work on spotted hyena endocri- aena social system” (Frank 1997:58). nology in the wild and in a captive colony at Though rooted in the supposed selective the University of California (Berkeley) ini- advantages of high androgen levels and fe- tially supported the nonadaptive hypothesis. male aggressiveness, this hypothesis views fe- Frank et al. (1985) measured circulating tes- male genital masculinization as an incidental tosterone levels in a large sample of wild hy- by-product. Critical features of this “nonadap- enas and, in contrast to Racey and Skinner tive hypothesis” are that there should be high (1979), detected significant differences be- benefits to female dominance, and few costs tween the sexes. Testosterone levels were associated with masculinized genitalia. found to be substantially higher in males than A strong selective advantage for female females, conforming to the general mamma- dominance in spotted hyenas is indeed clear lian pattern. Levels of androstenedione, how- (Frank 1996, 1997; Holekamp et al. 1996). ever, proved higher in females than in males, Unlike striped and brown hyenas, which tend the opposite of what occurs in most mammals to forage solitarily (Owens and Owens 1978), (Lindeque and Skinner 1982; Glickman et al. spotted hyenas regularly feed in groups 1987; van Jaarsveld and Skinner 1991; Glick- (Kruuk 1972; Hofer and East 1993a). As many man et al. 1993). This excess androstenedi- as 30 individuals can converge on a freshly- one in females appears to originate from the killed ungulate. Therefore competition for ovaries (Glickman et al. 1993). Androstene- food, both scramble (favoring rapid con- dione is an inactive “prohormone” which can sumption) and contest (favoring social dom- be converted to either estrogen or testoster- inance), is often intense (Kruuk 1972; Tilson one, depending on the presence of the en- and Hamilton 1984; Frank 1997). Frank zymes aromatase and 17b-hydroxysteroid de- (1997) notes that “within minutes” a group of hydrogenase (Milgrom 1990). Experiments hyenas can reduce a 220 kg wildebeest to by Yalcinkaya et al. (1993) showed that, due “bloody stains on the grass.” to low aromatase activity and relatively large High-ranking females and their offspring concentrations of 17b-hydroxysteroid dehy- dominate access to carcasses (Tilson and drogenase, the spotted hyena placenta is ex- Hamilton 1984; Frank 1986). They therefore tremely efficient at converting androstenedi- have markedly higher reproductive success one to testosterone. Consequently, because than subordinates, by maintaining shorter in- placental testosterone is transported to the terbirth intervals and having more surviving developing fetus via the umbilical vein, spot- offspring (Holekamp et al. 1996). They also ted hyena fetuses of both sexes are exposed begin breeding at younger ages (Holekamp to relatively high levels of testosterone in et al. 1996). Whereas subordinate females ex- utero (Licht et al. 1992; Licht et al. 1998). hibit better reproductive performance dur- These experiments made the nonadaptive hy- ing periods of prey abundance than during pothesis more compelling by offering clear periods of prey scarcity, dominant females evidence of a hormonal mechanism that show no such variance (Holekamp et al. could be expected to masculinize both be- 1996). The consequence of these inequalities havior and genitalia. is that high-ranking females enjoy an esti- Subsequent studies have revealed problems mated 2.5 to 2.75 times greater lifetime re- with the nonadaptive hypothesis, however. productive success than low-ranking females First, the costs of genital masculinization have (Frank 1996). This result lends crucial sup- been found to be high. Whereas most mam- port to the idea that selection would favor malian birth canals are straight, the spotted 6 THE QUARTERLY REVIEW OF BIOLOGY Volume 77 hyena’s curves sharply, extending through to androgens by, for example, reducing the the clitoris to a length of approximately 60 cm number of androgen receptors or reducing (Frank et al. 1995b). Because the umbilical the concentration of enzymes that convert cord is only 12–18 cm long, newborn hyenas testosterone to dihydrotestosterone? It is dif- often separate from the placenta, get caught ficult to argue that the requisite variation is in the end of the birth canal, and die from not present, as receptor densities in target tis- anoxia (Frank and Glickman 1994). In cap- sues, for example, vary within and between tivity, mortality of firstborns due to dystocia individuals, both pathologically and physio- is approximately 60% (Frank et al. 1995b). logically (Milgrom 1990). Birth complications also contribute signifi- Cognizant of these issues, Glickman et al. cantly to mortality among primiparous fe- (1993) noted that the effects of prenatal tes- males. It is possible that problems with par- tosterone exposure on sexual organization turition are exacerbated in captivity where, are indeed partly mitigated in female spotted compared to the wild, hyenas are relatively hyenas. For instance, androgen exposure dur- sedentary and overweight (Holekamp, per- ing spotted hyena development does not sonal communication). However, Frank et al. cause a reduction in maternal behavior, dis- (1995b) estimate that in the wild, more than ruption of fertility, or defeminization of sex- 8% of females die giving birth to their first ual behavior, all of which are routine effects offspring. In total, it appears that spotted hy- in other mammals. Glickman et al. concluded ena females lose between 16 and 25% of their that in hyenas, “the distribution of steroid re- expected lifetime reproduction because of ceptors (or metabolizing enzymes) in target their odd reproductive anatomy (Glickman et tissues of the nervous system might allow for al. 1993; Frank et al. 1995b; Frank 1996, selectivity of action, sparing sexual organiza- 1997). tion while promoting size and aggressiveness” These high costs imply that if genital mas- (1993:101). culinization is a nonfunctional consequence If the normal masculinizing effects of an- of other effects, the system of genital differ- drogens can be avoided in the brain and in entiation must be constrained in extraordi- the ovaries, then why not in the external gen- narily tight ways. For in the absence of some italia? This puzzle led researchers from the clear benefit, the high costs mean that there spotted hyena project in Berkeley to conduct should be strong selection pressure to miti- a series of experiments that examined in de- gate the effects of prenatal testosterone ex- tail the effects of testosterone on sexual dif- posure on female reproductive tissue. Yet ferentiation (Drea et al. 1998; Glickman et al. mammalian sexual differentiation is notable 1998; Licht et al. 1998). Remarkably, spotted for its plasticity. It is a complicated cascade of hyenas proved to deviate substantially from events that can be disrupted at numerous the standard mammalian pattern of sexual stages to produce a variety of intermediate or- differentiation. In particular, genital mascu- gans (Breedlove 1992). And while circulating linization in this species appears to be largely androgens do play an important role in the independent of androgens. process, they do not act indiscriminately. In most mammals, genital masculinization Rather, a variety of mechanisms has evolved is driven by testosterone produced by the fetal to regulate their effects. Some tissues are testes after they have developed from the in- more sensitive to androgens than others be- different gonads. The development of the tes- cause they contain higher concentrations of tes themselves is driven by the testis determi- androgen receptors. Others are less sensitive nation factor (TDF) gene, carried on the Y because they contain lower concentrations of chromosome (Wilson et al. 1981). Licht et al. the enzymes necessary to convert inactive (1998), however, found that in spotted hyenas prohormones (like androstenedione) to the external genitalia of both males and fe- their active forms. If the masculinized geni- males were masculinized by day 33 of gesta- talia of female hyenas have no adaptive value, tion, before gonadal differentiation had oc- then it seems reasonable to ask why selection curred. The implication is that if androgens has not acted to make the clitoris less sensitive are responsible for the basic process of geni- March 2002 SEXUAL MIMICRY IN HYENAS 7 tal masculinization, they must be coming experimentally, however, that a lack of andro- from the placenta rather than the fetus. gens during adolescence has little effect on To test this idea, Drea et al. (1998) treated genital morphology in spotted hyenas. This eight pregnant spotted hyenas with a combi- makes sense, as the majority of growth in both nation of antiandrogens and examined the the penis and the clitoris is achieved before effects on their infants. In most mammals the pubertal increase in circulating andro- such treatments result in female external gen- gens. Glickman et al. summarize the recent italia in both female and male offspring. This findings of the Berkeley group: “The overall general effect was found in hyenas, as males results suggest that the initial formation of exposed to antiandrogens were born with the fetal phallus, and its subsequent growth female-typical genitalia; that is, their penises during fetal and postnatal life, can proceed exhibited the “large urogenital meatus” and in a remarkably ‘normal’ (for a spotted hy- “glans with a rounded contour” characteristic aena) fashion without the influence of go- of hyena clitorises. Surprisingly, however, the nadal androgens” (1998:134). lack of prenatal androgens did not affect the Thus, the hypothesis that female genitalia in basic structure of the external genitalia in ei- spotted hyenas are masculinized by circulating ther sex. Females continued to exhibit peni- androgens has been falsified by the experi- form clitorises and fused labia. Drea et al. mental data. Accordingly, the nonadaptive concluded that while androgens do produce hypothesis—the pseudopenis and associated subtle differences in the genital morpholo- structures are maintained as an incidental by- gies of male and female hyenas, they are not product of high androgen levels—must be responsible for the basic process of clitoral wrong. enlargement and labial fusion. They suggested Recently Goymann et al. (2001) employed that “there is an androgen-independent mech- noninvasive methods to monitor androgen anism in spotted hyenas that promotes the levels in a large sample of Serengeti spotted development of clitoral-penile tissues and the hyenas. Their findings cast doubt upon a sec- fusion of the genital swellings to form a scro- ond element of the nonadaptive hypothesis; tum, or pseudoscrotum” (1998:126). They namely, that increased levels of circulating an- note that in a similar way, a nonandrogenic drogens are responsible for female domi- mechanism is responsible for sexual differ- nance and hyperaggressiveness in this spe- entiation in some marsupials, which form cies. Goymann et al. found that male hyenas either a female pouch or a scrotum from ab- had significantly higher T and DHT levels dominal tissue in an independent, genetically than females. Furthermore, they found no controlled process (Renfree and Short 1988). difference in androstenedione levels between Additional evidence that androgens are not females and postdispersal males; predispersal involved in the process of spotted hyena clit- males showed significantly lower levels than oral enlargement was reported by Frank both of these classes. Goymann et al. argue (1997), who noted that at Berkeley, “[e]fforts that earlier studies showing significantly in- to demonstrate androgen binding by andro- creased levels of androstenedione in female gen receptors in fibroblasts cultured from hyenas (Glickman et al. 1987, 1993; van Jaars- penile and clitoral tissues have been unsuc- veld and Skinner 1991) are problematic be- cessful” (1997:61). cause they either did not specify which class The hypothesis of nonandrogenic female of males was sampled or were performed with genital differentiation was further tested by captive animals, which may not accurately re- Glickman et al. (1998), who examined the ef- flect the endocrine status of animals in the fects of juvenile gonadectomy. In the stan- wild. Additionally, they note that male and fe- dard course of mammalian development, male infants are exposed to the same hor- high concentrations of circulating androgens monal milieu in utero. Thus, if prenatal an- during puberty are associated with acceler- drogen exposure is responsible for female ated penile growth. Thus, juvenile gonadec- hyperaggressiveness, the mechanism of an- tomy ordinarily has the effect of reducing drogenization must differ between males and penile growth. Glickman et al. (1998) showed females. Goymann et al. conclude that andro- 8 THE QUARTERLY REVIEW OF BIOLOGY Volume 77 gens are not likely to be involved in the hyper- ally, he points out that female hyenas are so aggressiveness of female hyenas. Whether or dominant to males that they do not need such not their study is corroborated by future re- an unwieldy mechanism to dissuade “overly search, it seems clear that androgens are not ardent males.” essential for genital masculinization in this All other major hypotheses offered to ex- species. plain the peniform clitoris of spotted hyena females have relied upon the assumption that Previous Adaptive Hypotheses the organ is a side effect of androgen expo- Rejection of the nonadaptive hypothesis sure (reviewed in Frank 1997). Accordingly, emphasizes the significance of the high costs none of the hypotheses reviewed to date ap- of genital masculinization in female spotted pear capable of accounting for masculinized hyenas, and reinforces the interest in finding genitals in female spotted hyenas. compensatory benefits. Unfortunately, however, the hyena literature contains few alter- Sexual Monomorphism as Sexual natives to the Gould and Vrba hypothesis Mimicry: The Camouflage Hypothesis (Frank 1996, 1997). Kruuk (1972) argued Genital masculinization in female spotted that the enlarged clitoris evolved as an im- hyenas is so complete that the sexes are in- portant element in the hyena “meeting cere- distinguishable when young. Sexual mono- mony.” When two hyenas come together after morphism is rare in mammals, but in other an absence, or following an aggressive inter- taxa it is sometimes known to be related to action, they often inspect each other’s erect the scrambling of recognition cues. Sexual genitals closely, sniffing or licking them for cue-scrambling has been studied principally ten to thirty seconds. Kruuk suggested that in the context of male mimicry of females, the erect genitalia function to reduce tension such as female-like male lizards remaining by diverting attention from an animal’s ca- small to avoid aggression from dominant nines. They also facilitate social bonds by males (Trivers 1976), giant cuttlefish imper- “keeping partners together over a longer sonating females to divert male attention meeting period.” This, says Kruuk, “could be while sneaking copulations (Norman et al. the selective advantage that has caused the 1999), or red-sided garter snakes exuding evolution of the females’ and cubs’ genital female-like skin lipids to distract rival males structure.” Kruuk’s explanation seems un- from females (Shine et al. 2000). Female likely, however, given the major reproductive mimicry of males, by contrast, is relatively costs associated with a masculinized repro- rare, but has been hypothesized to explain ductive anatomy, and the fact that the clitoris sexual monomorphism in certain ungulates, is not an indispensable part of the meeting where male-like females may benefit by avoid- ceremony. Frank (1996) notes that other hy- ing unwanted courtship (e.g., wildebeest: ena species engage in similar greeting behav- Geist 1974). In a similar way, certain morphs iors, but they focus their attention on the anal of the female damselfly (Ischnura ramburi) glands rather than the genitalia. look and behave like males, allowing them to East et al. (1993) also note the importance avoid unwelcome mating attempts that can of the erect “penis” in meeting ceremonies, result in increased risk of predation and but posit an additional advantage to the fused drowning (Robertson 1985; Sirot and Brock- labia exhibited by female spotted hyenas. mann 2001). They argue that this feature prevents male hy- Sexual monomorphism is also widespread enas from forcing copulation with females, in birds, though it is less clear whether mim- giving females control over mating. However, icry is responsible, and if so, who mimics Frank (1996, 1997) convincingly dismisses whom (Trail 1990; Amundsen 2000). But mim- this hypothesis by noting that no attempts at icry is possible, given that in several mono- forced copulation have been observed in any morphic birds, individuals cannot easily dis- species of hyena, and that forced copulation tinguish the sex of conspecifics (Burley 1981; is rare among mammals generally. Addition- Langmore and Bennett 1999). Male birds March 2002 SEXUAL MIMICRY IN HYENAS 9 that look like females may benefit by avoiding turely large canines. In captivity they are aggression from more dominant males (Roh- quick to attack and shake any moving objects wer et al. 1980), or by gaining a competitive that they can bite. This suggests that attacking advantage over other males through surprise and killing their siblings constitute adaptive attack (Saetre and Slagsvold 1996). tendencies. In a similar way, we suggest that sexual Females may be particularly vulnerable be- monomorphism in spotted hyenas could be cause female philopatry and strongly biased adaptive mimicry. Female spotted hyenas breeding success with high rank intensifies ri- sometimes attack and/or kill female rivals. Fe- valry among females (e.g., Silk 1983). Studies males that possess more male-like genitals in both Masai Mara (Frank et al. 1991) and could thereby gain some protection by ap- Serengeti (Hofer and East 1997) support the pearing male and, thus, be less worth attack- idea that female infants are the most frequent ing or killing (Wrangham and Peterson targets of siblicide. In Serengeti, for example, 1996). infant spotted hyenas emerging from their In theory there are at least three contexts dens exhibit unbalanced sex ratios (Hofer in which the camouflage hypothesis could ap- and East 1997; James and Hofer 1999). Fe- ply: siblicide by same-aged infants, infanticide male singletons there are more common than by adults, and adult-killing by extragroup ri- male singletons, and male twins are more vals. In practice, however, the physical resem- common than female twins, implying that fe- blance of females to males declines from in- males are more likely than males to kill their fancy onwards. Thus, during the first two to same-sex twins (Hofer and East 1997). three months of life, female and male cubs Specifically, Hofer and East (1997) re- cannot be distinguished by humans. But by ported that by three months of age, infant hy- the time they are juveniles, subtle differences enas in their study included 39 male and 52 have emerged in the shape of the glans female singletons. MM, MF, and FF twin pairs (Frank et al. 1990). Among adult hyenas, numbered 29, 69, and 16 respectively. Al- body shape, pitch of the “whoop” vocaliza- though lethal aggression was not directly ob- tion, and behavior all allow experienced hu- served, Hofer and East noted that the ob- man observers to identify the sex (Holekamp, served sex ratio could be produced in only personal communication). Parous females, in three ways: (1) a bias in the sex ratio at birth, particular, are easily distinguished by their (2) sex-specific postnatal mortality other than pulled nipples and torn clitorises (Kruuk siblicide, or (3) sex-biased siblicide. They re- 1972). If sexual mimicry is adaptive, its great- jected the first two hypotheses as being in- est significance should therefore be in in- consistent with the difference between the fancy. Because hyenas rely heavily upon sex ratios for twins and singletons, and con- senses other than sight, sexual mimicry cluded that siblicide must be more common should extend to other sensory modalities, in- in female-female pairs (see Table 1). cluding (theoretically) smell, taste, touch, Frank and colleagues (1991) employed a and sound. This possibility is discussed in fur- different definition of siblicide in Masai Mara ther detail below. from that of Hofer and East (1997). In the former study, the sex ratio of twins was ob- Camouflage as a Defense Against served two to six weeks after birth; in the lat- Siblicide ter, sex ratios were observed at three months In favor of sexual mimicry as a defense (see also James and Hofer 1999). In Masai against siblicide, intense aggression has been Mara, as in the Serengeti, mixed-sex litters reported among newborns (Frank et al. 1991; were more common than would be pre- Golla et al. 1999). Infants are born into a den dicted by chance, and among same-sex lit- in a small cavity where the mother cannot eas- ters, male-male pairs were more common ily reach them. In addition to having open than female-female pairs. Based on the as- eyes, functional incisors, and strikingly mus- sumption that litters typically contain two in- cular necks and jaws, infants have prema- fants, the rate of siblicide has been estimated 10 THE QUARTERLY REVIEW OF BIOLOGY Volume 77

TABLE 1 Against this hypothesis, infant spotted hy- Probabilities of spotted hyena siblicide enas appear so aggressive in captivity—even in the Serengeti biting a towel—that it may not matter what Sex of the Killer the victim looks or smells like. Additionally, Sex of the Victim Male Female Smale et al. (1999) have recently argued that siblicide is less common than Frank et al. Male 0.25 0.18 (1991) or Hofer and East (1997) suggest. Female 0.18 0.44 They note that evidence concerning siblicide Probabilities of siblicide in male/male, male/female, and in the wild is largely indirect, inferred from female/female twins from Serengeti ( James and Hofer 1999, calculated from the data in Hofer and East 1997). The prob- the number and sex of infants that emerge abilities are based upon an observed sample (at three months from dens. They suggest that fighting among of age) of 39 male and 52 female singletons, and MM, MF, neonates indeed occurs, but is directed more and FF twin pairs numbering 29, 69, and 16. The model as- towards establishing dominance than elimi- sumes that all litters start out as twins, and that the primary sex ratio is 0.5. Both of these assumptions have been chal- nating rivals. Since surviving losers are per- lenged (Smale et al. 1999). manently subordinate, there is no need to kill them. Smale et al. (1999) interpret the high frequency of singletons emerging from dens as a result of lone births, rather than of litters between 9.6% (Serengeti, Tanzania: Hofer reduced by siblicide; they suggest that the low and East 1997) and ca. 25% (Mara, Kenya: numbers of same-sex twins reported by Frank Frank et al. 1991). et al. (1991) and Hofer and East (1997) may If female newborns indeed attack and kill be a result of birth sex ratios that deviate from their sisters more than their brothers, selec- unity. tion could favor females that resemble males, Thus, the importance of siblicide as a and (as a counterstrategy) female ability to source of mortality remains uncertain. Direct detect the sex of their sibling. In theory, these observation of infants from birth to emer- opposing trends could generate a high de- gence from the den are required to assess its gree of sexual mimicry in all relevant modes, frequency and to test whether, for example, i.e., visual (including behavioral), auditory, better male mimics are more likely to escape tactile, taste, and smell. This predicts that in- intense domination by their sisters. A porta- fant spotted hyenas should be less skilled at ble ultrasound machine is currently being detecting other infants’ sex (by smell, licking, used in the field to compare litter sizes before or sound, for example) than are infant brown birth with those that emerge from the den or striped hyenas. The significance of high two to four weeks after birth (Holekamp, per- levels of circulating androgens in fetal and sonal communication). These data will even- newborn females could therefore include tually produce one test of the siblicide hy- conferring a male-like smell, both in utero pothesis. and after birth. We are unaware of any explanation for the Camouflage as a Defense Against exaggeration of penile size in infants. How- Infanticide ever, if selection favors aggression targeted towards females (by either siblings or adult con- Sexual mimicry could also be a defense specifics), it may be beneficial for males to against infanticide. Adult females are known exaggerate their maleness (thereby reducing to commit infanticide in captivity (Frank et the risk of being mistaken for a female). al. 1995a), and in the wild they exhibit a Large penile size during infancy might there- “tendency” to kill the neonates of lower- fore be the consequence of selection for ranking females (Frank 1996, 1997). This males to avoid resembling females. If so, the phenomenon has also been documented by strategy has been successfully countered by Hofer and East (1995), who state that the enlargement of the female clitoris. Behav- most important sources of juvenile mortality ioral convergence is seen in the ability of in- in Serengeti are “observed and presumed infant females to erect their clitoris. fanticide by adult clan members . . . and ob- March 2002 SEXUAL MIMICRY IN HYENAS 11 served and presumed siblicide” (1995:344). tecting the sex of neonates. Additionally, Indirect evidence for infanticide includes other species of hyena should be better than “the reluctance of small cubs to exit the bur- spotted hyenas at detecting the sex of neo- row in the presence of adults, and the care nates. If these predictions are incorrect, then they seem to show in ascertaining the iden- the hypothesis is falsified. tity of their mother before exiting” (Frank et A final prediction of both the siblicide and al. 1995a:379). infanticide hypotheses, one that has been Unfortunately there are currently no pub- tested, is that the degree of mimicry should lished data on the frequency of infanticide in be greatest in neonates during the period of hyena clans, nor on the sex distribution of its highest risk, from both infanticide and sibli- victims (Frank, personal communication). cide. Golla et al. (1999) reported that the This is not surprising, as infanticide is difficult mean age of cubs classified as probable sibli- to observe in the wild, and hyena neonates cides in their study was 59.2 days plus or mi- cannot conveniently be sexed by field re- nus 24. And Frank et al. (1995a) note that the searchers until they are two to three months risk of infanticide is greatest for infants less old ( James and East 1999). Additionally, it is than three months old. As previously noted, sometimes difficult for fieldworkers to distin- humans can only begin to distinguish the sex guish between hyena cubs killed by lions and of infant hyenas at three months. those killed by conspecifics (Frank et al. 1995a). A few cases of infanticide (unpub- Camouflage as a Defense Against lished) have been directly observed in the Intergroup Aggression long-term study sites, but these are not yet suf- Aggression is also intense in between-clan ficient to indicate the significance of infanticide for spotted hyena mortality; “it could be interactions. According to Goodall (1986), a great, or it could be trivial” (Holekamp, per- patrolling group consists of at least three sonal communication). high-ranking females. “[A] patrol almost al- However, the pattern of local resource ways gives chase if it encounters a lone hyena, competition and male dispersal in spotted hy- or a pair, even if these neighbors are in their enas is consistent with the prediction that own territory. A captured individual may be high-ranking females should selectively target mauled and left to die” (1986:527). Although female offspring for infanticide (Silk 1983). systematic data have not been published, in- In primates this pattern is evident in a range cidents of death from interclan aggression of cercopithecines, where high-ranking fe- have been described from Tanzania by Good- males selectively harass lower-ranking individ- all and van Lawick (1970) and Kruuk (1972), uals carrying female fetuses or immature fe- from South Africa by Henschel and Skinner males (Silk 1983). If female cubs are at (1991), and in Botswana by Joubert and Jou- particular risk for intragroup infanticide, they bert (1992). Intolerance of strangers is so may benefit by appearing to be male. Frank great that after females leave the clan tem- et al. (1995a) state that “[s]everal incidents of porarily and forage alone during lean times, infanticide in captive hyenas confirm that fe- they may be attacked by their own clan on males of the same social group may be a lethal their return. Males who leave the clan and threat to cubs under 3 months of age” return, however, do not experience such ag- (1995a:379). As mentioned previously, this is gression (Holekamp et al. 1993). the age at which fieldworkers can distinguish As indirect evidence for intergroup aggres- the sexes with some reliability. sion, hyena females in all study sites defend Although additional field observations are territories by scent marking, vocalizing, mak- needed to assess the significance of infanti- ing regular boundary patrols, and respond- cide among spotted hyenas, tests of the hy- ing aggressively to intruders (Goodall and pothesis could be conducted in captivity. The van Lawick 1970; Kruuk 1972; Henschel and prediction is that adult hyenas should be bet- Skinner 1991; Hofer and East 1995). Hen- ter at detecting the sex of juveniles (or infants schel and Skinner (1991) reported that spot- older than three months) than they are at de- ted hyenas in Kruger National Park spent 12 THE QUARTERLY REVIEW OF BIOLOGY Volume 77

20% of their total activity period and distance who more closely resemble males might be on territorial patrol, mostly along borders selected less often as the target of interclan with the clans that intruded most frequently. attacks by neighbors. Against this hypothesis, Additionally, in playback studies in both the interclan killings do not necessarily occur at Kalahari (Mills 1990) and the Timbavati high rates. Thus they have not been recorded Game Reserve (Bearder 1984), hyenas either in Frank’s long-term study in Mara, Kenya answered or did not react to the calls of other (Frank 1996), nor in the Kalahari (South Af- clan members, but moved aggressively to- rica) where spotted hyena densities are low wards the speaker when the calls of nonclan (Mills 1990). members were played. An additional problem with applying the The fission-fusion nature of spotted hyena mimicry hypothesis to adult hyenas is that the social organization would seem to make hye- physical similarities between the sexes clearly nas particularly vulnerable to lethal aggres- diminish with increasing age. Thus, human sion by neighbors. In the Serengeti, Hofer observers can readily distinguish adult males and East (1993a,b,c) have described a “com- from adult females by the pitch of the muter system” in which members of a clan “whoop” vocalization, body shape, and social must often leave their territory when the mi- behavior. Parous females are particularly easy gratory species that they feed upon are not to distinguish, due to distinctive changes in locally abundant. During these periods, hye- their nipples and clitorises. Since hyenas are nas fission into small groups of 1–8 individ- known to distinguish individuals on the basis uals and go on “commuting trips.” Territory of their vocalizations (Holekamp et al. 1999), holders react aggressively to invaders when they can also be expected to distinguish be- they encounter them. In such encounters ter- tween the sexes. Hyenas can also probably ritory holders also generally have the advan- determine the sex of other adults by smell tage of numbers. During 52 recorded en- (Holekamp, personal communication). A fi- counters, residents outnumbered commuters nal complication for the theory is that, among in 83%, and equaled them in 17%. A vast ma- adults, the clitoris is often retracted into the jority of commuters in Hofer and East’s study abdomen, where it cannot be observed by con- were solitary. By appearing to be male from a specifics (Frank and Glickman, personal com- distance, solitary individuals might decrease munication). the probability of pursuit and attack by resi- Thus, under most circumstances the bene- dent females. fits of sexual mimicry appear unlikely to be In our scenario, the benefits to females of important for adults. Theoretically, mimicry mimicking males in interclan interactions de- might be possible for nulliparous females en- rive from two features of spotted hyenas. First, countering strangers at a distance, where females and males have the same body di- scent cues are unavailable. In the commuting mensions (Glickman et al. 1993). Similar system described above, females traveling in body size makes close mimicry possible, un- border areas or through strange territories like lions (Panthera leo) for example. Second, frequently encounter groups of hostile resi- spotted hyenas have female philopatry. This dents with whom they are not familiar (Hofer means that females are likely to be more de- and East 1993b). The hypothesis would re- termined defenders of a clan range than quire that in such situations nulliparous females (since females have no options of mov- males refrain from vocalizing, maintain their ing to a new clan, unlike males). It also means distance, and adopt a male-like submissive that a clan’s coalitionary power is reduced posture (including an erect clitoris), in order more predictably by eliminating a female to maximize the likelihood of successful mim- than a male, since females are recruited only icry. In fact, Hofer and East (1993b) report by maturation, whereas males can be re- that nonresident hyenas commonly exhibit cruited from other clans. For both these rea- such behaviors upon encountering territory sons, therefore, if territorial competition is in- holders. It is not clear, however, whether res- tense, it should benefit clans to attempt to kill idents are actually confused about the iden- neighboring females. Accordingly, females tity of intruders during territorial encounters. March 2002 SEXUAL MIMICRY IN HYENAS 13

Thus, in spite of this possibility, the theoreti- 1. Female cubs should be more at risk from cal benefits of sexual mimicry appear to be aggression than male cubs. much more important for infants than adults. 2. Aggressors should have difficulty dis- Conclusion tinguishing the sex of their potential victims (whether through sight, smell, For at least two decades the large and mas- taste, touch, or sound). culinized genitals of female spotted hyenas have been regarded as a nonadaptive con- 3. Sexual mimicry (in all relevant sensory sequence of selection for high androgen lev- modalities) should be greatest during els. The nonadaptive hypothesis was never the period of highest risk. robustly tested, however, because no explanations were sought for why females were 4. Other species of hyena should discrim- androgenized in some traits (e.g., clitoral inate between infant females and males morphology) but not in others (e.g., repro- better than spotted hyenas. ductive physiology). A series of experiments If any of these predictions is shown to be in- on the development of spotted hyena infants correct, then the mimicry hypothesis is falsi- has now shown that contrary to expectation, fied. female spotted hyena genitals develop their Gould (1981) criticized adaptationism as typical masculine form even in the absence naı¨ve on the basis that “organic material is of androgenic steroids. This falsifies the non- not putty, and natural selection is not omnip- adaptive hypothesis for maintenance of gen- otent.” Natural selection can indeed be con- ital masculinization. It remains possible, nev- strained in important ways (reviewed in ertheless, that genital masculinization began Dawkins 1982). However, by reducing the by- as an incidental consequence of high andro- product explanation of spotted hyena genital gen levels in females, providing the chance masculinization to the status of a Just-So opportunity for selection to act. Story, the data from wild and captive hyenas Certainly the fact that genital masculiniza- illustrate that the naı¨vete´ of previous hypoth- tion is now largely independent of andro- eses lay not in their relationship to natural genic action, together with the evidence that selection, but in asserting their validity with- masculinization causes high costs to females, out a strong empirical test. Whether or not suggests that the size, shape, and musculature the camouflage hypothesis is ultimately falsi- of female spotted hyena genitals have subse- fied, the hyena case suggests that there is no quently been subject to positive selection to a priori reason for favoring nonadaptive over resemble those of males. Adaptive hypotheses adaptive hypotheses. are therefore required. We propose that masculinization of female spotted hyena genitals acknowledgments represents the endpoint of an arms race for We thank David Haig and Kern Reeve for discussions, female mimicry of males, favored by a ten- and Richard Estes, David Haig, and Craig Stanford dency for females to direct more intense ag- for comments. We also thank Laurence Frank, Ste- gression towards females than to males. Field phen Glickman, Kay Holekamp, and an anonymous and captive observations can provide tests of reviewer for extended commentaries on the manu- the following predictions: script.

REFERENCES

Amundsen T. 2000. Why are female birds ornamented? 156 in The Encyclopedia of Mammals, edited by D Trends in Ecology & Evolution 15:149–155. Macdonald. New York: Facts on File. Beach F A, Buehler M G, Dunbar I F. 1983. Sexual Breedlove S M. 1992. Sexual differentiation of the cycles in female dogs treated with androgen dur- brain and behavior. Pages 39–70 in Behavioral En- ing development. Behavioral and Neural Biology docrinology, edited by J B Becker et al. Cambridge 38:1–31. (MA): MIT Press. Bearder S K. 1984. How hyenas communicate. Page Burley N. 1980. The evolution of sexual indistinguish- 14 THE QUARTERLY REVIEW OF BIOLOGY Volume 77

ability. Pages 121–137 in Natural Selection and Social Glickman S E, Frank L G, Davidson J M, Smith E R, Behavior, edited by R D Alexander and D W Tinkle. Siiteri P K. 1987. Androstenedione may organize New York: Chiron Press. or activate sex reversed traits in female spotted hy- Dawkins R. 1982. The Extended Phenotype. Oxford: Ox- enas. Proceedings of the National Academy of Sciences ford University Press. 84:3444–3447. Deane N N. 1962. The spotted hyaena Crocuta crocuta Glickman S E, Frank L G, Holekamp K E, Smale L, crocuta. The Lammergeyer 2:26–44. Licht P. 1993. Costs and benefits of “androgeniza- Drea C M, Weldele M L, Forger N G, Coscia E M, tion” in the female spotted hyena: the natural se- Frank L G, Licht P, Glickman S E. 1998. Androgens lection of physiological mechanisms. Pages 87–117 and masculinization in the spotted hyaena (Crocuta in Perspectives in Ethology, edited byPPGBateson. crocuta). 2. Effects of prenatal anti-androgens. Jour- New York: Plenum Press. nal of Reproduction and Fertility 113:117–127. Golla W, Hofer H, East M L. 1999. Within-litter sibling East M L, Hofer H, Wickler W. 1993. The erect ‘penis’ aggression in spotted hyaenas: effect of maternal is a flag of submission in a female-dominated so- nursing, sex and age. Animal Behaviour 58:715–726. ciety: greetings in Serengeti spotted hyenas. Behav- Goodall J. 1986. The Chimpanzees of Gombe: Patterns of ioral Ecology and Sociobiology 33:355–370. Behavior. Cambridge (MA): Harvard University Frank L G. 1986. Social organisation of the spotted Press. hyaena (Crocuta crocuta). II. Dominance and repro- Goodall J, van Lawick H. 1970. Innocent Killers. Boston: duction. Animal Behaviour 34:1510–1527. Houghton Mifflin. Frank L G. 1996. Female masculinization in the spot- Gould S J. 1981. Hyena myths and realities. Natural ted hyena: endocrinology, behavioral ecology, and History 90:16. evolution. Pages 78–131 in Carnivore Behavior, Ecol- Gould S J, Vrba E S. 1982. Exaptation—a missing term ogy, and Evolution, edited by J L Gittleman. Ithaca in the science of form. Paleobiology 8:4–15. (NY ): Cornell University Press. Goymann W, East M L, Hofer H. 2001. Androgens and Frank L G. 1997. Evolution of genital masculinization: the role of female “hyperaggressiveness” in spotted why do female hyaenas have such a large ‘penis’? hyenas (Crocuta crocuta). Hormones and Behavior 39: Trends in Ecology & Evolution 12:58–62. 83–92. Frank L G, Davidson J M, Smith E R. 1985. Androgen Hamilton W J, Tilson R L, Frank L G. 1986. Sexual levels in the spotted hyaena Crocuta crocuta: the in- monomorphism in spotted hyenas, Crocuta crocuta. fluence of social factors. Journal of Zoology 206:525– Ethology 71(1):63–73. 531. Henschel J R, Skinner J D. 1987. Social relationships Frank L G, Glickman S E. 1994. Giving birth through and dispersal patterns in a clan of spotted hyaenas a penile clitoris: parturition and dystocia in the Crocuta crocuta in the Kruger National Park. South spotted hyena (Crocuta crocuta). Journal of Zoology African Journal of Zoology 22:18–23. 234:659–690. Henschel J R, Skinner J D. 1991. Territorial behaviour Frank L G, Glickman S E, Licht P. 1991. Fatal sibling by a clan of spotted hyaenas Crocuta crocuta. Ethology aggression, precocial development, and androgens 88:223–235. in neonatal spotted hyenas. Science 252:702–704. Hofer H, East M. 1993a. The commuting system of Frank L G, Glickman S E, Powch I. 1990. Sexual di- Serengeti spotted hyaenas: how a predator copes morphism in the spotted hyena (Crocuta crocuta). with migratory prey. I. Social organization. Animal Journal of Zoology 221:308–313. Behaviour 46:547–557. Frank L G, Holekamp K E, Smale L. 1995a. Domi- Hofer H, East M. 1993b. The commuting system of Ser- nance, demography, and reproductive success of engeti spotted hyaenas: how a predator copes with female spotted hyenas. Pages 364–384 in Serengeti migratory prey. II. Intrusion pressure and commut- II: Dynamics, Management, and Conservation of an ers’ space use. Animal Behaviour 46:559–574. Ecosystem, edited by A R E Sinclair and P Arcese. Hofer H, East M. 1993c. The commuting system of Chicago: University of Chicago Press. Serengeti spotted hyaenas: how a predator copes Frank L G, Weldele M L, Glickman S E. 1995b. Mas- with migratory prey. III. Attendance and maternal culinization costs in hyenas. Nature 377:584–585. care. Animal Behaviour 46:575–589. Geist V. 1974. On the relationship of social evolution Hofer H, East M. 1995. Population dynamics, popu- and ecology in ungulates. American Zoologist 14:205– lation size, and the commuting system of Serengeti 220. spotted hyenas. Pages 332–363 in Serengeti II: Dy- Glickman S E, Coscia E M, Frank L G, Licht P, Weldele namics, Management, and Conservation of an Ecosys- M L, Drea C M. 1998. Androgens and masculini- tem, edited by A R E Sinclair and P Arcese. Chicago: zation of genitalia in the spotted hyaena (Crocuta University of Chicago Press. crocuta). 3. Effects of juvenile gonadectomy. Journal Hofer H, East M L. 1997. Skewed offspring sex ratios of Reproduction and Fertility 113:129–135. and sex composition of twin litters in Serengeti March 2002 SEXUAL MIMICRY IN HYENAS 15

spotted hyaenas (Crocuta crocuta) are a conse- havioural Ecology of Two Species. London: Unwin quence of siblicide. Applied Animal Behavior Science Hyman. 51:307–316. Monaghan E P, Glickman S E. 1992. Hormones and Holekamp K E, Boydston E E, Szykman M, Graham I, aggressive behavior. Pages 261–285 in Behavioral Nutt K J, Birch S, Piskiel A, Singh M. 1999. Vocal Endrocrinology, edited by J B Becker et al. Cam- recognition in the spotted hyaena and its possible bridge (MA): MIT Press. implications regarding the evolution of intelli- Norman M D, Finn J, Tregenza T. 1999. Female im- gence. Animal Behaviour 80:383–395. personation as an alternative reproductive strategy Holekamp K E, Ogutu J O, Dublin H T, Frank L G, in giant cuttlefish. Proceedings of the Royal Society of Smale L. 1993. Fission of a spotted hyena clan: con- London B 266:1347–1349. sequences of prolonged female absenteeism and Owens D, Owens M. 1996. Social dominance and re- causes of female emigration. Ethology 93:285–299. productive patterns in brown hyaenas, Hyaena Holekamp K E, Smale L. 1995. Rapid change in off- brunnea, of the central Kalahari desert. Animal Be- spring sex ratios after clan fission in the spotted haviour 51:535–551. hyena. American Naturalist 145:261–278. Owens M J, Owens D D. 1978. Feeding ecology and its Holekamp K E, Smale L. 1998. Behavioral develop- influence on social organization in brown hyenas ment in the spotted hyena. BioScience 48:997–1005. (Hyaena brunnae, Thunberg) of the Central Kala- Holekamp K E, Smale L, Szykman M. 1996. Rank and hari Desert. East African Wildlife Journal 16:113– reproduction in the female spotted hyena. Journal 135. of Reproduction and Fertility 108:229–237. Racey P A, Skinner J D. 1979. Endocrine aspects of James W H, Hofer H. 1999. A note on sex ratios and sexual mimicry in spotted hyaenas Crocuta crocuta. sex combinations in Serengeti spotted hyaenas: Journal of Zoology 187:315–326. siblicide and sub-binomial variance. Applied Animal Renfree M B, Short R V. 1988. Sex determination in Behaviour Science 65:153–158. marsupials: evidence for a marsupial-eutharian di- Joubert D, Joubert B. 1992. Eternal Enemies. Bo- chotomy. Philosophical Transactions of the Royal Soci- tswana: Wildlife Films. ety of London B 322:41–53. Kruuk H. 1972. The Spotted Hyena: A Study of Predation Robertson H M. 1985. Female dimorphism and mat- and Social Behavior. Chicago: University of Chicago ing behaviour in a damselfly, Ischnura ramburi: fe- Press. males mimicking males. Animal Behaviour 33:805– Langmore N E, Bennett A T D. 1999. Strategic con- 809. cealment of sexual identity in an estrildid finch. Rohwer S, Fretwell S D, Niles D M. 1980. Delayed mat- Proceedings of the Royal Society of London B 266:543– uration in passerine plumages and the deceptive 550. acquisition of resources. American Naturalist Licht P, Frank L G, Pavgi S, Yalcinkaya T M, Siiteri P K, 115:400–437. Glickman S E. 1992. Hormonal correlates of “mas- Saetre G-P, Slagsvold S. 1996. The significance of fe- culinization” in the female spotted hyaena (Crocuta male mimicry in male contests. American Naturalist crocuta). II. Maternal and fetal steroids. Journal of 147:981–995. Reproduction and Fertility 95:463–474. Shapiro D Y, Reeve H K, Pfennig D W. 1997. Recog- Licht P, Hayes T, Tsai P, Cunha G, Kim H, Golbus M, nition systems. Pages 69–96 in Behavioural Ecology: Hayward S, Martin M C, Jaffe R B, Glickman S E. An Evolutionary Approach, edited by J R Krebs and 1998. Androgens and masculinization of genitalia N B Davies. Oxford: Blackwell Scientific Publica- in the spotted hyena (Crocuta crocuta). 1. Urogen- tions. ital morphology and placental androgen produc- Shine R, Lemaster M P, Moore I T, Mason R T. 2000. tion during fetal life. Journal of Reproduction and Fer- The transvestite serpent: why do male garter tility 113:105–116. snakes court (some) other males? Animal Behaviour Lindeque M, Skinner J D. 1982. Fetal androgens and 59:349–359. sexual mimicry in spotted hyaenas (Crocuta cro- Silk J B. 1983. Local resource competition and facul- cuta). Journal of Reproduction and Fertility 65:405– tative adjustment of sex ratios in relation to com- 410. petitive abilities. American Naturalist 121:56–66. Matthews L H. 1939. Reproduction of the spotted hy- Sirot L K, Brockmann H J. 2001. Costs of sexual inter- aena (Crocuta crocuta Erxleben). Philosophical Trans- actions to females in Rambur’s forktail damselfly, actions Series B 230:1–78. Ischnura ramburi (Zygoptera: Coenagrionidae). Milgrom E. 1990. Steroid hormones. Pages 385–437 Animal Behaviour 61:415–424. in Hormones: From Molecules to Disease, edited by Smale L, Frank L G, Holekamp K E. 1993. Ontogeny E-E Baulieu and P A Kelly. New York: Chapman of dominance in free-living spotted hyaenas: juve- and Hall. nile rank relations with adult females and immi- Mills M G L. 1990. Kalahari Hyaenas: Comparative Be- grant males. Animal Behaviour 46:467–477. 16 THE QUARTERLY REVIEW OF BIOLOGY Volume 77

Smale L, Holekamp K E, White P A. 1999. Siblicide social and reproductive development. Journal of Re- revisited in the spotted hyaena: does it conform to production and Fertility 93:195–201. obligate or facultative models? Animal Behaviour Whateley A. 1980. Comparative body measurements 58:545–551. of male and female spotted hyaenas from Natal. Smuts B B, Watanabe J M. 1990. Social relationships The Lammergeyer 28:40–43. and ritualized greetings in adult male baboons (Pa- Wickler W. 1969. The Sexual Code. London: Weidenfeld pio cynocephalus anubis). International Journal of Pri- & Nicolson. matology 11:147–172. Wilson J D, George F W, Griffin J E. 1981. The hor- Tilson R L, Hamilton W J. 1984. Social dominance and monal control of sexual development. Science feeding patterns of spotted hyaenas. Animal Behav- 211:1278–1284. iour 32:715–724. Wrangham R W, Peterson D. 1996. Demonic Males: Apes Trail P. 1990. Why should lek-breeders be monomor- and the Origins of Human Violence. Boston: Hough- phic? Evolution 44:1837–1852. ton Mifflin. Trivers R L. 1976. Sexual selection and resource-accru- Yalcinkaya T M, Siiteri P K, Vigne J-L, Licht P, Pavgi S, ing abilities in Anolis garmani. Evolution 30:253–269. Frank L G, Glickman S E. 1993. A mechanism for van Jaarsveld A S, Skinner J D. 1991. Plasma androgens virilization of female spotted hyenas in utero. Sci- in spotted hyaenas (Crocuta crocuta): influence of ence 260:1929–1931.