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Female Mate Choice in Mammals Author(S): by Tim Clutton-Brock and and Katherine Mcauliffe Reviewed Work(S): Source: the Quarterly Review of Biology, Vol

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Female Mate Choice in Mammals Author(S): by Tim Clutton-Brock and and Katherine Mcauliffe Reviewed Work(S): Source: the Quarterly Review of Biology, Vol Female Mate Choice in Mammals Author(s): By Tim Clutton-Brock and and Katherine McAuliffe Reviewed work(s): Source: The Quarterly Review of Biology, Vol. 84, No. 1 (March 2009), pp. 3-27 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/596461 . Accessed: 07/09/2012 01:00 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to The Quarterly Review of Biology. http://www.jstor.org Volume 84, No. 1 March 2009 THE QUARTERLY REVIEW of Biology FEMALE MATE CHOICE IN MAMMALS Tim Clutton-Brock Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom e-mail: [email protected] Katherine McAuliffe Department of Anthropology, Harvard University, Cambridge, Massachusetts 02138, USA e-mail: [email protected] keywords sexual selection, mate choice, mammals, mating systems, genetic benefits abstract Studies of mate choice in vertebrates have focused principally on birds, in which male ornaments are often highly developed, and have shown that females commonly select mates on the basis of particular phenotypic characteristics that may reflect their genetic quality. Studies of female mate choice in mammals are less highly developed, and they have commonly focused on female mating preferences that are likely to be maintained by benefits to the female’s own survival or breeding success. However, recent experimental studies of mate choice in mammals—especially rodents—provide increasing evidence of consistent female preferences that appear likely to generate benefits to the fitness of offspring. As yet, there is no compelling evidence that female mating preferences are less highly developed in female mammals than in female birds, although these preferences may more often be masked by the effects of male competition or of attempts by males to constrain female choice. Introduction sexual selection, the first operating through N THE DESCENT OF MAN, Darwin competition between individuals of one I(1871) describes two principal modes of sex—usually males—for access to breeding The Quarterly Review of Biology, March 2009, Vol. 84, No. 1 Copyright © 2009 by The University of Chicago. All rights reserved. 0033-5770/2009/8401-0001$15.00 3 4 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 partners of the opposite sex, leading to the mals are often philopatric (Greenwood evolution of different forms of weaponry and 1980; Clutton-Brock 1989), and males fre- other characteristics that affect fighting abil- quently compete to monopolize access to ity, and the second operating through fe- pre-existing female groups, thus restricting male mating preferences combined with opportunities for mate choice in females. Fe- competition between males to attract fe- male mammals are usually less mobile than males, leading to the evolution of various female birds, and the costs of extra-group forms of ornamentation in males. Sex differ- forays to monitor mating opportunities or to ences in weaponry among mammals pro- select alternative mating partners can be very vided Darwin with many examples of his first high, especially when relationships between mode of sexual selection, while sex differ- neighboring groups are hostile (Clutton- ences in avian ornaments provided many of Brock and Parket 1995; Holekamp and the examples that he used to illustrate the Smale 2000; Clutton-Brock et al. 2006). consequences of his second mode of sexual Since biases in the Operational Sex Ratio are selection. A similar reliance on mammalian often large and generate intense competi- examples to illustrate the evolution of male tion between males for access to females, weaponry through intrasexual competition, only males of high quality are likely to obtain and on avian examples to illustrate the evo- access to female groups. The benefits of fe- lution of male ornamentation though inter- male choice may, therefore, be relatively sexual mate choice, persists to this day (see small, and selection may favor females that Huxley 1938; Alexander et al. 1979; Brad- acquiesce to mating with males that win ac- bury and Andersson 1987; Andersson 1994; cess to their range or group (Pierce and Clutton-Brock 2004; Kraaijeveld et al. 2007). Dewsbury 1991). The reliance on mammalian examples to Although intense intrasexual competition illustrate the evolution of male weaponry, as between males is a conspicuous feature of well as the widespread evidence of intra- many mammalian breeding systems, it is sexual competition between males, has re- likely that the extent to which female mating sulted in a common perception that intra- preferences influence male success has been sexual competition is the predominant form underestimated (Small 1988, 1989). Com- of sexual selection in mammals and that, pared to birds, a relatively high proportion where female choice does occur, females of mammals are active at dusk or after dark commonly favor mating with partners that and rely on olfactory or auditory cues rather are able to provide protection, access to re- than visual ones, so that the complexity of sources, or paternal care rather than genetic male displays and the extent of female pref- benefits to their offspring (Clutton-Brock erences are commonly hard to assess (Rob- 1988; Clutton-Brock et al. 1989). Moreover, erts and Gosling 2003; Clutton-Brock 2004). there are some reasons to expect that intra- In addition, the effects of female mating sexual competition for access to females is preferences are often difficult to distinguish more intense in male mammals than in male from those of intrasexual competition birds and that intersexual mate choice is between males and male coercive tactics more highly developed in female birds than (Clutton-Brock et al. 1993). A growing in female mammals. Most mammals are po- number of studies on mammals have pro- lygynous, and social monogamy and paternal duced evidence that females show consis- care are both relatively rare (Eisenberg 1966; tent mating preferences for particular Kleiman 1977; Eisenberg 1981). As a con- categories of males that appear likely to sequence of intrasexual competition for ac- generate fitness benefits to the females cess to mates, males are commonly larger themselves or to their offspring (Keddy- than females (Clutton-Brock and Harvey Hector 1992; Penn and Potts 1998a; Jen- 1977; Alexander et al. 1979) and often use nions and Petrie 2000; Roberts and Gos- their greater strength to constrain female ling 2003; Manson 2006). In this review, mate choice (Smuts and Smuts 1993; Clut- we assess recent studies of female mate ton-Brock and Parker 1995). Female mam- choice in mammals and attempt to dis- March 2009 FEMALE MATE CHOICE IN MAMMALS 5 tinguish the cases in which there is cred- resource-based territories in areas of grass- ible evidence that female preferences land favored by grazing females (Rosser have an important influence on male 1987; 1992). Females (including receptive mating success from those in which vari- and nonreceptive individuals) spend more ation in male success may be a conse- time grazing in territories where annual quence of intrasexual competition. In herbs are abundant, and males defend- the final section, we return to the ques- ing these territories get more matings tion of whether there is any indication than those defending less-favored territo- that patterns of mate choice in mammals ries. In such cases, variation in male differ from those in birds. mating success may be caused principally Before describing the evidence for fe- by intrasexual competition among males male choice, it is worth clarifying exactly for resource-based territories, and this, what we mean when we say that females combined with female preferences for par- choose or show a preference for particular ticular habitats, may mask the conse- mating partners. We use “female choice” to quences of any preferences that persist in mean cases where females show an active females for particular categories of mating preference for mating with particular cat- partners. We refer to examples of this kind egories of males, whether or not matings as “coincidental” mate choice in order to lead to conception. Unlike some others, emphasize that such choices do not involve our definition of female choice carries the adaptations that have evolved through a implication that not all forms of female process of sexual selection. behavior that affect the distribution of mat- In natural populations, female prefer- ing success in males should necessarily be ences for mating with particular categories of regarded as mating preferences. For exam- males are often difficult to distinguish from ple, in many animals, females show prefer- female preferences for particular areas or ences for particular habitat types because habitats, or from other forms of coincidental they offer greater protection from preda- mate choice. Studies of Uganda kob Kobus tors or improved access to resources, and kob thomasi, a lek-breeding African antelope, female habitat preferences often affect the provide a good example. In this species, fe- mating success of males holding territories males leave grazing herds as they approach in different areas. The effects of female estrus and begin to attract courting males habitat preferences on male mating success and move to leks, where male territory hold- are well-illustrated by recent studies of ungu- ers defending small territories that do not lates. For example, in the desert-adapted contain significant resources keep nonterri- Grevy’s zebra Equus grevyi, females in the torial males away (Clutton-Brock et al.
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