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Sexual Mimicry in Hyenas Sexual Mimicry in Hyenas The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters 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. Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:41467428 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Volume 77, No. 1 March 2002 The Quarterly Review of Biology 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 con- sequence 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. The Quarterly Review of Biology, March 2002, Vol. 77, No. 1 Copyright ᭧ 2002 by The University of Chicago. All rights reserved. 0033-5770/2002/7701-0001$15.00 3 4 THE QUARTERLY REVIEW OF BIOLOGY Volume 77 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
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