Female Mate Choice in 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

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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 , mate choice, mammals, mating systems, genetic benefits

abstract Studies of mate choice in vertebrates have focused principally on , 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 —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 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 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 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 , 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. 1993; later stages of pregnancy restrict their usually Deutsch 1994; Nefdt and Thirgood 1997). large ranges and move to areas where wa- Once on the lek, females collect on particu- ter is available and where they can drink on lar territories, and the males that defend a daily basis during the period of these territories often show high mating suc- (Rubenstein 1986). Females have a post- cess (Leuthold 1966). Larger or older males partum estrus, as do other equids, and typically defend the most popular territories males establish large territories in the vi- and commonly show higher mating success cinity of water sources in order to mate than smaller or younger territory holders with receptive females visiting these water (Balmford 1992). Although data of this kind sources. Although female movements af- are sometimes interpreted as evidence of fe- fect the distribution of male mating success male mating preferences in lek breeders in Grevy’s zebra, differences in mating suc- (Carbone and Taborsky 1996), female cess between males may simply be a conse- kob appear to prefer particular territo- quence of female habitat preferences ries rather than the particular males that rather than of preferences for mating with occupy them (Balmford 1990, 1991), and particular categories of partners. Similarly, experiments show that preferred territories in puku Kobus vardonii, mature males hold are ones that have recently been heavily used 6 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 by females, are distant from thickets or maturity other places where predators can hide, and Where younger or less powerful males are often close to the centre of the lek are likely to lose mating opportunities to (Deutsch and Nefdt 1992). Since the most older or stronger individuals unless they popular territories tend to be held by the copulate quickly, selection often favors co- most competitive males, preferences for ercive strategies in males (Clutton-Brock particular territories are likely to lead to and Parker 1992). The costs of male coer- correlations between mating success and cion to females may be high, especially in male so that these relationships systems where multiple males compete si- do not provide reliable evidence of female multaneously for the same female (Smuts preferences for mating with particular cat- and Smuts 1993), and, in many of these egories of males (Clutton-Brock et al. 1993, systems, females avoid mating with imma- 1996), and similar problems are wide- ture males that are unable to provide ef- spread in other systems. To overcome this fective defense against rivals (Fox 2002). problem, it is often necessary to manipulate For example, in elephant seals Mirounga the size or quality of male traits and to dem- angustirostris, females are commonly courted onstrate that doing so affects female prefer- by multiple males, and both females and ences and male success—but, in natural their pups can be injured or killed unless populations, experiments of this kind usually one mate can control access to them (Re- face serious logistical problems, and, conse- iter et al. 1981; Le Boeuf and Mesnick quently, conclusive evidence that female 1991). Mature males are usually able to mating preferences are responsible for vari- monopolize access to females, providing ation in male mating success is rare. effective protection against harassment by other males, while younger males are un- Female Mating Preferences In able to do so. Females show a preference Mammals for joining larger harems where they—and their pups—are likely to be safer from A substantial number of studies have sug- male harassment (Pistorius et al. 2001; Mc- gested that female mammals mate preferen- Mahon and Bradshaw 2004), and females tially with particular categories of males. In that are being courted by younger males order to organize the available evidence of give calls that attract the attention of dom- female mate choice in mammals, we have inant males, who commonly displace the focused on evidence of female preferences younger suitors (Cox and Le Boeuf 1977). for different attributes of males, including Similarly, in ungulates that form unstable their maturity, dominance status, fertility, ca- herds, estrous females risk being killed by pacity for investment, relative development competing males unless they join males of weaponry, symmetry, coloration, vocal dis- capable of protecting them against rivals plays, olfactory displays, (un)relatedness, ge- (Clutton-Brock et al. 1993; Re´ale et al. netic similarity or compatibility, and previous 1996). These species commonly show a mating success. Subsequently, we have exam- preference for joining larger groups (Car- ined evidence of variation in female prefer- ranza and Valencia 1999). Also, in some ences and of the frequency with which fe- social primates, females often avoid mating males mate with multiple partners. Very with immature partners, which may reduce few studies have yet been able to measure the risk of dangerous harassment or pun- either the direct or the indirect conse- ishment by older males (Manson 1994a,b; quences of mate choice and, although di- Fox 2002), and, like female elephant seals, rect benefits appear more likely to main- females in some species incite competition tain some preferences while indirect ones between males and may gain direct bene- maintain others, in most cases, benefits of fits by doing so (Kuester and Paul 1992). both kinds are possible. An additional reason why females avoid March 2009 FEMALE MATE CHOICE IN MAMMALS 7 mating with younger partners may be that several species of antelope, females leave immature males are less likely to be fertile their usual herds as estrus approaches and (Cox and Le Boeuf 1977; Clutton-Brock move to leks where they commonly show a et al. 1982; Small 1988; Byers et al. 1994). preference for joining the larger harems that often form at the centre of such leks dominance (Clutton-Brock et al. 1988b, 1993; Nefdt In a number of mammals, females show and Thirgood 1997; Bro-Jørgensen 2002). a consistent preference for mating with Territories that attract females are usually dominant males. For example, in some ro- defended by larger and more dominant dents, females offered a choice of domi- males who obtain a high proportion of nant or subordinate partners preferen- matings, but, on natural leks, it is usually tially mate with dominant males (Huck difficult to separate female preferences for and Banks 1982; Shapiro and Dewsbury particular territories—or for joining larger 1986; Drickamer 1992; Solomon and Keane groups of females—from preferences for 2007). In natural populations of social pri- mating with particular males. In an at- mates and carnivores, females also ap- tempt to distinguish between female pref- pear to favor dominant partners (Seyfarth erences for particular territories and fe- 1978a,b; Robinson 1982; Silk and Boyd 1983; male preferences for particular males, Janson 1984; West and Packer 2002), al- Clutton-Brock (1989) forced male fallow though this is not always the case, and, espe- deer Dama dama defending territories on a cially in larger groups, dominant males com- lek to move to new territories and showed monly obtain a smaller share of matings than that their relative success on their initial priority of access models would predict territory was correlated with their success (Fedigan 1983; Manson 1992, 1994a,b; Soltis on their new territory. However, correla- and McElreath 2001; Fox 2002; Alberts et al. tions of this kind may still be generated by 2003; Manson 2006). However, in natural individual differences in the capacity of populations, it is usually difficult to exclude males to retain females or to acquire the possibility that an increase in female mat- popular territories, and, therefore, do not ings with dominant males is not a conse- provide conclusive evidence of mating quence of competition between males or of preferences (Clutton-Brock et al. 1993). their coercive tactics. Subsequent experiments with female fal- Selective mating with dominant males low deer that had been induced into full can provide direct as well as indirect ben- estrus showed that these females exhibited efits to the fitness of females. In some cer- a strong tendency to join other females, copithecine primates that live in multi- but that the characteristics of associated male groups, fathers are more likely to males apparently had little effect on their protect or support their own progeny than movements (Clutton-Brock and McComb those of other males (Stein and Stacey 1993; McComb 1994). Recent studies of 1981; Keddy-Hector et al. 1989; Borries topi Damaliscus lunatus, where males de- et al. 1999; Soltis and McElreath 2001; fending central territories on leks obtain a Buchan et al. 2003). As high-ranking males high proportion of matings, show that fe- can provide more effective care for infants males mate more rapidly after arrival on a than low-ranking males (Alexander 1970; central territory than on a peripheral one Stein 1984; Agrell et al. 1998), female pref- and that they sometimes compete with oth- erences for dominant males may affect the ers for the attentions of males (Bro- survival of their offspring while also generat- Jørgensen 2002; Bro-Jørgensen and Durant ing genetic benefits, since the traits that af- 2003). Although this has been interpreted fect dominance are often heritable (Dricka- as evidence that female mating prefer- mer 1992; Horne and Ylo¨nen 1998). ences are responsible for variation in male Studies of a number of lek-breeding success, it is also possible that females in mammals also suggest that females may full estrus collect in the centre of leks ei- show a preference for dominant males. In ther as a consequence of random move- 8 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 ments between territories (Stillman et al. likely to mate with male friends than with 1993) or as a result of improvements in the other males (Seyfarth 1978a,b; Takahata ability of males on central territories to 1982; Rasmussen 1983; Smuts 1985), but this retain females (Clutton-Brock et al. 1993, is not always the case (Manson 1994a,b; 1996). Hemelrijk et al. 1999; Manson 2006). In species where females mate preferen- fertility tially with friends, males might be expected to signal their capacity or readiness to pro- Although males of some polygynous spe- vide care or protection to prospective cies are capable of fertilizing substantial mates. Some studies of tamarins, where numbers of females (Clutton-Brock 1982), multiple males often help to carry young the ejaculates of males that mate repeat- produced by a single female, have sug- edly over a short period often show re- gested that infant carrying by males may duced sperm counts as well as reduced fer- represent a form of courtship (Price 1990; tility (Austin and Dewsbury 1986; Huck Ferrari 1992). However, direct evidence et al. 1986; Preston et al. 2001), and the that females are more likely to mate with capacity of these males to impregnate fe- males that contributed heavily to previous males may be temporarily limited (Dews- litters is lacking (Baker et al. 1993; Tardif bury 1982a,b,c). Several studies of rodents and Bales 1997), and it seems more likely show that females mate preferentially with that carrying is an example of parental unmated males (Krames and Mastromat- care or of kin-related cooperation. teo 1973, Huck et al. 1986; Pierce and Dewsbury 1991). Some studies suggest that weaponry this tendency is more pronounced in mo- nogamous species, where males commonly Several studies of ungulates have shown care for their offspring and the costs of that variation in horn or antler size in pairing with an infertile partner may be males is correlated with phenotypic quality particularly high, than in polygamous spe- or mating success, thus suggesting that fe- cies (Pierce and Dewsbury 1991; Salo and male choice may play an important role in Dewsbury 1995; though see Solomon and the evolution of horns and antlers (Esp- Keane 2007). In addition, studies of some mark 1964; Geist 1971; Ditchkoff et al. polygynous mammals provide evidence of 2001; Vanpe´ et al. 2007). As with virtually female competition for access to males all other sexually dimorphic traits, horn (Bro-Jørgensen 2002; Bebie and McElligot size and antler size are correlated with age 2006), and one interpretation of these ob- and body size, which are, in turn, associ- servations is that the sperm supplies of ated with fighting ability, social rank and “popular” partners are limited (see Preston mating success (Clutton-Brock 1982; Bar- et al. 2001). rette and Vandal 1986; Alvarez 1990; Pri- chard et al, 1999; Coltman et al. 2002; Mys- terud et al. 2005). As a result, evidence of male investment associations between male horn size and Where males contribute to rearing or male provides no firm protecting their mates or their offspring, indication that horn size affects mating females might be expected to favor part- success directly, or that relative horn size is ners that are prepared to invest heavily in used as a signal either in the assessment their offspring. In several baboons and ma- of competitors by males or of potential caques that live in multi-male groups, fe- mating partners by females. In order to males develop close affiliative relationships demonstrate that horn size affects mating or “friendships” with particular males (Smuts preferences, it would be necessary to ma- 1985; Silk 2002). “Friends” are often males nipulate horn size and to show that this that previously held high status in the group, affected female preferences. As yet, all at- although they seldom include the current tempts to manipulate relative horn or ant- alpha male, and females are often more ler size have been unsuccessful (Lincoln March 2009 FEMALE MATE CHOICE IN MAMMALS 9

1994). In experiments where female fallow worn by symmetrical males as sexier than deer were induced into estrus and then those of asymmetrical males (Rikowski and offered a choice of males with antlers or Grammer 1999). Dancing ability, too, is males that had had their antlers removed, associated with bodily symmetry, and when no evidence of a preference for antlered other aspects of visual appearance are con- males was found (Clutton-Brock and Mc- trolled for, women show a preference for Comb 1993). Despite this, studies of the “good dancers” (Brown et al. 2005). How- evolution of horns and antlers continue to ever, although these studies suggest that suggest that females prefer mating with symmetry increases female interest, it has males with large antlers and that, conse- yet to be shown that it affects mating deci- quently, female mating preferences have sions. played an important role in the evolution of antlers and horns, even though there is , coloration, and no direct evidence that this is the case (see testosterone Vanpe´ et al. 2007). Male horns and antlers In a substantial number of mammals, are effective defensive and offensive weap- males with relatively high testosterone lev- ons, and, as yet, there is no firm evidence els are both more frequently aggressive that mate choice has played an important and more distinctively colored or pat- role in their evolution (Clutton-Brock 1982). terned than females, as well as males with In a number of ungulates, females also lower testosterone levels, and are com- carry horns or antlers that vary widely in monly preferred as mating partners (Van- size and that they commonly use in com- denbergh 1965; Setchell and Dixon 2001; petitive interactions with other females or Gerald 2001; Gerald 2003), although it is with males (Packer 1983; Robinson and often difficult to identify which of the cor- Kruuk 2007). relates of high testosterone levels are used in mate choice. For example, in African symmetry lions Panthera leo, males with dark manes Low levels of fluctuating asymmetry are have higher testosterone levels than light thought to be an indicator of developmen- maned individuals and are more likely to tal stability and genetic quality, and several take the lead in encounters with other studies of birds suggest that females prefer prides (West and Packer 2002), and recep- males with symmetrical (Møller tive lionesses commonly mate with the and Pomiankowski 1993; Møller and Swad- darkest maned male in their group. Exper- dle 1997). Some studies of ungulates have iments in which lionesses were presented also suggested that there may be an associ- with life-sized models of light and dark ation between the mating success of males maned lions showed that lionesses were and the symmetry of their horns (Møller more likely to approach lions with darker et al. 1996), although detailed studies of manes, whereas lions presented with the red deer provided no evidence that sym- same models were more likely to approach metry is related to mating success, and the those with light manes (West and Packer heritability of this trait appears to be low 2002). Dark manes retain heat more than (Kruuk et al. 2003). In humans, women light ones, so mane color could be a hand- are more attracted to men with symmetri- icap, providing females with a reliable in- cal faces (Rikowski and Grammer 1999; dication of male quality (Zahavi 1975), but Thornhill and Gangestad 1999; Johnston an alternative explanation is that females et al. 2001), and it is thought that facial gain direct benefits from choosing males symmetry may be related to testosterone with dark manes since they have longer levels in men (Thornhill and Gangestad breeding tenures (Packer et al. 1988). Ter- 1999). In addition, male body in hu- ritorial males are darker than females mans is associated with . or nonterritorial males in a number of Women asked to rate the odor of T-shirts lek-breeding antelopes (including Kafue worn by different male subjects rated those lechwe Kobus leche kafuensis and white-eared 10 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 kob Kobus kob leucotis) (Clutton-Brock et al. testosterone levels, thus making them more 1993), which may indicate that females favor likely to be aggressive and pose greater risks darker males here as well. than duller males to females who ignore In some primates, such as vervet monkeys their advances. Cercopithecus aethiops (Gartlan and Brain 1968; Gerald 2001), gelada baboons Thero- vocal displays pithecus gelada (Dunbar 1984), rhesus ma- In many mammals, male displays may caques Macaca mulatta (Vandenbergh 1965), play an important role in the mating deci- and mandrills Mandrillus sphinx (Setchell sions of females and can have direct effects and Dixson 2001), males of high status have on hormonal levels in females, even influ- more brightly colored faces, perineal re- encing the timing of ovulation. For exam- gions, or testes than subordinates, and fe- ple, in red deer, exposure to the roaring males are attracted to the brightest males displays of males advances the timing of (Gerald 2001). For example, in mandrill estrus in females (McComb 1987). In ad- groups, which include large numbers of in- dition, male displays may be used by fe- dividuals, one male is typically brighter than male mammals in the selection of mating all the others, and females interact, groom, partners. In red deer Cervus elaphus and and mate more frequently with the brightest fallow deer Dama dama, the repeated roars male than with other mature males (Setchell of harem-holding stags attract the atten- 2005). Although brightly colored males tend tion of receptive females, who are more to have high status within their groups likely to join the harems of males with high (Setchell and Dixson 2001), the effects of male coloration are stronger than those of roaring rates (McComb 1991; McElligott rank and remain when the influence of male and Hayden 2001). Similar preferences for rank is allowed for. Experiments with rhesus males with high calling rates have been macaques also suggest that females are demonstrated in other mammals, includ- strongly attracted to brighter males; captive ing the grey mouse lemur Microcebus muri- females presented with redder versus paler nus (Craul et al. 2004). versions of male faces spent more time gaz- Specific acoustic properties of male calls ing at the redder versions of male faces may also be important in attracting females (Waitt et al. 2003). (Davidson and Wilkinson 2004). For exam- One possible explanation for female ple, the formant frequencies of red deer preferences for brightly colored males is roars decrease with increasing body size, that they increase the chance that a fe- and females preferentially approach speak- male’s daughters will inherit that ers producing roars with lower formant val- provide effective resistance to parasites ues (Charlton et al. 2007). In white-lined (Folstad and Karter 1992). This argument bats Saccopteryx bilineata, males that defend is based on the fact that bright skin color- mating territories in tree buttresses pro- ing is commonly associated with testoster- duce complex vocalizations that attract one levels (Vandenbergh 1965) and testos- females (Catchpole 1980; Hiebert et al. terone suppresses immune function, so 1989), and males with more complex that male brightness may signal an individ- “songs” have more females on their terri- ual’s resistance to infection. While this may tories (Davidson and Wilkinson 2004). It be the case, there are several other possible has yet to be shown if the complexity of reasons why females pay more attention to male songs has a direct effect on female brightly colored males. For example, if mating preferences or male success. Al- bright males are likely to have low parasite though these studies support the sugges- levels, mating with them may reduce the tion that male displays are important to female’s own chances of becoming in- female mate choice, the same displays fected (Loehle 1997). Also, females may commonly discourage potential challeng- pay greater attention to brighter males be- ers (Clutton-Brock and Albon 1979), so cause they are more likely to have higher that it is always difficult to assess the extent March 2009 FEMALE MATE CHOICE IN MAMMALS 11 to which female preferences are responsi- tant role in attracting females (Yamaguchi ble for variation in male success. et al. 1981; Hayashi 1990; Mossman and Drickamer 1996; Rich and Hurst 1998; olfactory displays Humphries et al. 1999; Thomas 2002). The Olfactory cues may play an important size of male scent glands, the frequency of role in female mating preferences in many scent marking, and the chemical structure mammals (Gosling and Roberts 2001a,b). of scent marks are all heritable (Horne and Females commonly investigate male scent Ylo¨nen 1998; Roberts and Gosling 2003), marks, which may reflect male condition and, in some rodents, females not only and other male characteristics (Moore and show a consistent preference for mating Marchinton 1974; Sawyer et al. 1989; Gos- with dominant males but for mating with ling and Roberts 2001a,b). In several ro- the sons of these males as well (Drickamer dents, females are less attracted to 1992). from males infected with parasites than to those of uninfected males (Clayton 1991; relatedness Kavaliers and Colwell 1995a,b; Penn and Breeding with close relatives commonly Potts 1998b; Klein et al. 1999; Willis and depresses the number and fitness of off- Poulin 2000; Ehman and Scott 2001), and spring (Keller and Waller 2002; Solomon females given a choice between infected and Keane 2007), and outbreeding is one and uninfected males are less likely to of the most common forms of mate choice mate with infected ones, but, if they do (Solomon and Keane 2007). Females often indeed mate with infected males, fewer avoid inbreeding by a combination of dis- male offspring will be produced as a result persal, delaying sexual maturity if their fa- (Hillgarth and Wingfield 1997; Barnard ther is still resident in the group (Pusey 1987; et al. 1998; Ehman and Scott 2002). Since Krackow and Matuschak 1991; Pusey and resistance to parasites can be heritable Wolf 1996; Hoogland 2001), and avoiding (Enriquez et al. 1988) and parasite load mating with closely related males or with can affect male status (Hausfater and males that have not immigrated into their Watson 1976; Freeland 1981; Gosling and group during their lifetime (Packer 1979; Roberts 2001a,b), female preferences for Pusey and Wolf 1996; Cooney and Bennett uninfected males are likely to have indirect 2000; Constable et al. 2001; Manson 2006). benefits for their offspring. For example, cross-fostering experiments Female preferences for mating with with rodents show that unrelated individuals dominant partners may often be caused by reared together subsequently avoid breeding olfactory cues. Dominant individuals com- with each other whereas relatives reared monly scent mark more frequently than apart breed with one another readily, thus subordinates, often over-marking the indicating that inbreeding avoidance is scent marks of rivals (Gosling and Rob- based on the avoidance of mating with famil- erts 2001a,b). In some species, females iar individuals (Dewsbury 1988; Pusey and appear to use the frequency of scent Wolf 1996). Humans may use similar cues in marking by males, or the frequency with selecting mates, for individuals commonly which they over-mark the scents of rivals, show a strong aversion to breeding with as a basis for assessing potential mates childhood associates, whether or not they (Desjardins et al. 1973; Johnston et al. are related (Wolf 1995). 1997; Rich and Hurst 1998, 1999; Gosling In some mammals, dispersing females et al. 2000; Roberts and Gosling 2003). continue to avoid breeding with close rela- Analysis shows that the odors produced by tives encountered outside their natal group dominant males differ qualitatively from or territory (Pusey and Wolf 1996), while, in those produced by subordinates and re- others, females that have dispersed from flect their higher androgen levels (No- their natal group will breed with related votny et al. 1990). The compounds present males if they subsequently encounter them. in scent marks may also play a more impor- For example, in reindeer Rangifer tarandus, 12 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 females will breed with related males that heterozygous partners over more homozy- dispersed from their natal herd if they en- gous ones (Potts et al. 1991; von Schantz counter them, although the chance of such et al. 1997; Penn and Potts 1998a,b; Foerster enounters is low (Holand et al. 2007). Stud- et al. 2003). When heterozygous males have ies of rodents suggest that differences in the higher fitness, females may increase the fit- basis of female discrimination may be related ness of their progeny by selectively choosing to variation in the chance that dispersing to mate with partners whose genotypes are individuals will encounter close relatives. For dissimilar to their own, and some studies sug- example, in rodents where both are gests that they do so, although the way in relatively sedentary and females mature at an which individuals are able to recognize their early age, females typically avoid mating with own genotype is still uncertain. For example, close relatives, whether or not they are famil- house mice living in semi-natural enclosures iar with them (Dewsbury 1988; Ferkin 1990). produce offspring that are more heterozy- In such cases, discrimination may be based gous at the MHC locus than would be ex- on odors. In house mice Mus musculus,as pected by chance (Carroll and Potts 2007). well as some voles, females are able to dis- Much of this excess appears to be a conse- criminate between odors from siblings and quence of extra-territorial matings by fe- odors from unrelated individuals, and avoid males, thus suggesting that females favor mating with siblings (Gilder and Slater 1978; matings with genetically dissimilar partners. Gavish et al. 1984; Winn and Vestal 1986; Similarly, in grey seals Halichoerus grypus, the Bolhuis et al. 1988; Krackow and Matuschak genotypes of maternal half-siblings also are 1991). Individuals commonly use cues de- more diverse than would be expected by rived either from their own phenotype or chance (Amos et al. 2001). from the phenotype of parents or littermates Some of the best evidence of disassocia- to form a template that is subsequently tive mating is provided by studies of the used in comparisons with other individ- effects of the MHC genotype on mate uals (Beauchamp et al. 1988). choice in rodents (Carroll and Potts 2007; While outbreeding generally increases Solomon and Keane 2007). Individuals the fecundity of females and the fitness of that are heterozygous at the MHC locus their offspring, it can also have costs if it commonly show higher fitness than ho- disrupts co-adapted complexes, in mozygotes, and MHC homozygous geno- which case some studies suggest that indi- types are rarer and heterozygous ones viduals avoid breeding both with close rel- more common than would be expected by atives and with entirely unrelated partners chance in several vertebrates, thus suggest- (Bateson 1983). It is not yet clear how com- ing that females mate selectively with males mon trends of this kind are. Studies of that have different MHC genotypes from captive white-footed mice Peromyscus leuco- their own (Potts et al. 1991; Hedrick and pus have shown that females mate prefer- Black 1997; Ober et al. 1997; Paterson and entially with cousins, but studies of several Pemberton 1997; Jordan and Bruford 1998; other rodents have found no effects of this Penn and Potts 1999). Experiments with fish, kind (Solomon and Keane 2007). mice, and humans show that females can detect MHC-related odors and are attracted heterozygosity, genetic to individuals with genotypes dissimilar from dissimilarity, and compatibility their own (Potts et al. 1991; Milinski and In many organisms, including several Wedekind 2001; Carroll et al. 2002; Penn mammals, there is evidence that female 2002; Milinski 2003; Roberts and Gosling mating preferences are related to genetic 2003), in some cases favoring partners carry- parameters in males. The degree of male ing specific MHC alleles that complement ornamentation in several birds and some their own genotype (Egid and Brown 1989; mammals is correlated with levels of het- Wedekind and Fu¨ri 1997). MHC-based odor erozygosity at particular loci, and, in several preferences may also be involved in kin rec- species, females show a preference for more ognition and in the avoidance of close in- March 2009 FEMALE MATE CHOICE IN MAMMALS 13 breeding (Yamazaki et al. 1988; Penn and sus compatibility in mates may also vary Potts 1999). For example, cross-fostering ex- between individuals. For instance, in spe- periments show that female mice avoid mat- cies where pair-bonds are enforced by fe- ing with individuals carrying the MHC genes male aggression, dominant females may of the family in which they are reared rather choose (and monopolize) highly orna- than with individuals carrying their own mented males, while subordinate females MHC genes (Penn and Potts 1998a). may be forced to choose among less highly MHC-based preferences may be most ornamented males on the basis of compati- highly developed in species in which fe- bility (Mays and Hill 2004). males choose between males using olfac- tory cues. For example, MHC-related mate previous mating success choice may be highly developed in fish and One tactic that females might use in select- mammals because of their advanced olfac- ing mates is to copy the mating choices of tory capabilities (Mays and Hill 2004). An- other females. Studies of several social ani- other possibility is that MHC-based mate mals suggest that breeding females com- choice initially evolved as a mechanism to monly copy each other’s choice of mates and allow individuals to identify and avoid mat- may gain indirect benefits by doing so (Du- ing with close kin. If so, MHC-related pref- gatkin 1992). However, a recurrent problem erences might be expected to be weak or is that female mammals commonly copy absent in species where one sex habitually each other’s movements for reasons uncon- disperses at adolescence and the chance nected to mating preferences, and so evi- that dispersers will encounter close relatives dence that females follow each other does is low (Penn and Potts 1999). This could not necessarily indicate that they are copying explain why there is no evidence of disasso- each other’s choice of mating partners (Clut- ciative mating for the MHC genotype in Soay ton-Brock and McComb 1993). For example, sheep Ovis aries, where male competition ap- in several ungulate species in which males pears to determine the identity of mating defend mating territories, females com- partners (Paterson and Pemberton 1997; monly follow each other between territories, Pemberton 2004). collecting with particular males (Clutton- Evidence that individuals favor geneti- Brock et al. 1993). Although this could occur cally dissimilar mates raises the question of as a result of estrous females copying each how these preferences interact with selec- other’s mating preferences, an alternative tion for good genes (Colegrave et al. 2002; possibility is that females are safer from pred- Mays and Hill 2004). One possibility is that ators or harassing males when they are in there is a hierarchy of cues used in mating larger groups (McComb and Clutton-Brock preferences. For example, individuals may 1994; Nefdt and Thirgood 1997). In red make an initial choice on the basis of deer, estrous females suffer less harassment “good genes” and then use compatibility from males when they gather together in criteria to select a mate from among ac- larger groups (Carranza and Valencia 1999), ceptable males. Experiments with mice while, in elephant seals, dependent pups are provide some evidence for hierarchies of less likely to be injured or killed if their this kind (Roberts and Gosling 2003): fe- mothers join larger harems (McMahon and males prefer males who scent mark fre- Bradshaw 2004). If females are indeed copy- quently—a trait that is associated both with ing each other’s mating preferences, their androgen levels and dominance and may tendency to join males with larger harems be an indicator of genetic quality—but, should be specific to females in estrus. Also, when there is little variation in the scent individuals in larger harems might be more marking rate, they show a preference for likely to mate with harem holders per unit males with MHC genotypes unlike their time of spent in their harems than females own (Roberts and Gosling 2003). Some with less popular males. As predicted, ex- studies have suggested that the relative im- periments with captive fallow deer that com- portance of selection for good genes ver- pared the responses of estrous and anestrous 14 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 females to mature males with and without Most studies of mate-choice copying as- females found that the attraction of females sume that females monitor and copy each to males associated with other females only other’s movements, but another possibility occurred in estrous females (McComb and is that males signal the fact that they have Clutton-Brock 1994). However, estrous fe- mated recently and females respond to males showed no preference for males that these signals. Experiments with rats show they had seen mating over those that had not that females offered a choice between a mated, and, in free-ranging populations of male that had copulated recently and one fallow deer, females in large harems are no that had not done so consistently preferred more likely to mate per unit of time than the male that had recently copulated those in small harems (Clutton-Brock and (Galef et al. 2008). In contrast, when trials McComb 1993; Clutton-Brock et al. 1993, were repeated using females that had no 1996). While this suggests that estrous fe- sense of smell, females showed no prefer- males tend to aggregate, it does not sup- ence for either male. port the suggestion that they copy each other’s choice of mates. partner number and post-copulatory In a number of mammals where females mate choice live in matrilineal groups, related females In mammals where males and females are commonly breed with the same male (Clut- closely bonded, including both socially mo- ton-Brock 1982; Pemberton et al. 1992). For nogamous and polygynous species, females example, in greater horseshoe bats Rhinolo- rarely mate with more than one male per phus ferrumequinun, related females often visit season (Brotherton et al. 1997; Clutton- the same mating partners (Rossiter et al. Brock and Isvaran 2006). For example, in 2005). It is sometimes suggested that these both red deer, which form harems, and fal- trends are a consequence of female prefer- low deer, which mate on resource territories ences to mate with the same male as their or leks, females have short estrus periods and relatives in order to increase coefficients of usually copulate only once or twice per sea- relatedness within social groups, thereby re- son, usually with a single partner (Clutton- ducing competition and increasing the po- Brock et al. 1982, 1988a,b). In contrast, in tential for kin-selected cooperation (Rossiter other mammalian groups, including mono- et al. 2005). However, a more likely expla- tocous species, such as topi (Bro-Jørgensen nation is that related females copy each 2002), and polytocous ones, such as North other’s movements and gain direct ben- American red squirrels Tamiasciurus hudsoni- efits by doing so. cus (Berteaux and Boutin 2000), females Some studies of humans also suggest commonly mate with multiple partners, of- that women may copy each other’s choice ten in rapid succession (see Jolly 1966; - of partners. For example, a recent experi- sall and Nash 1973; Bertram 1976; Tutin ment has shown that women give higher 1979; Cords et al. 1986; Packer et al. 1991; ratings to photographs of men paired with Pereira and Weiss 1991; East et al. 2003; Wil- smiling female profiles than to photo- son et al. 2004). In some species, up to 90% graphs of these same men paired with the of litters show multiple paternity, as in the profiles of the same women who, rather yellow-toothed cavy Galea flavidens (Hohoff than smiling, are instead wearing neutral et al. 2003). Intraspecific variation in partner expressions (Jones et al. 2007). These pair- number is also common: in one population ings have the opposite effect on male sub- of thirteen-lined ground squirrels Spermophi- jects, suggesting that female approval af- lus tridecemlineatus, the frequency of multiple fects the attraction of males to other paternity within litters ranged from 0–50% women. Whether this reflects a mating between years (Schwagmeyer and Brown preference is not yet known, and other 1983; Schwagmeyer and Parker 1987). studies indicate that women do not find In some species, females make no obvi- “attached” men more attractive than “un- ous attempt to instigate multiple mating; attached” ones (Uller and Johansson 2003). rather, it appears to be a consequence of March 2009 FEMALE MATE CHOICE IN MAMMALS 15 competition between males. In Soay sheep, an apparatus that prevented harassment or for example, estrous females commonly monopolization of females showed that mate with large numbers of males, but they 90% of mating females actively solicited show little evidence of active mate choice copulations with more than one male, and and often attempt to avoid pursuing males that females preferred heavier males and (Wilson et al. 2004). Similarly, female thir- those that courted more frequently (Ho- teen-lined ground squirrels show little evi- hoff et al. 2003). dence of active female preferences for mat- Mating with multiple partners often has ing with particular males (Schwagmeyer substantial costs, including the energy costs 1984), and most females copulate with all of locating suitable partners, the risk of ha- males that locate and attempt to mate with rassment or punishment by dominant males, them (Schwagmeyer 1984, 1986; Schwagm- the risks of acquiring sexually transmissible eyer and Woontner 1985). In some groups of diseases, reduced control of paternity, and mammals, interspecific differences in the increased competition between offspring number of males that females usually mate born either in the same or successive litters, with is thought to be a consequence of con- yet it presumably has substantial benefits as trasts in the capacity of males to defend fe- well (Schwagmeyer 1984; Ridley 1988; Wolff males. For instance, in many sea lions, males and Macdonald 2004). One common sug- are territorial, mating is rarely interrupted, gestion is that mating with multiple partners and, as in red deer, females typically mate may reduce the risk of mating with a tempo- with a single male (Gentry and Kooyman rarily or permanently infertile partner. Stud- 1886; Cassini 1999). In contrast, in seal spe- ies of artificial insemination in domestic cies, such as elephant seals, males vary in mammals show that the use of sperm from dominance but do not defend territories, more than one male can increase the prob- copulations are frequently interrupted, and ability of conception (Hess et al. 1954; Beatty females commonly mate with several part- 1960), and, in some natural populations of ners. birds and mammals, mating with multiple In other mammals, females appear to go males appears to be a response to previous out of their way to invite or pursue matings with more than one partner. For example, breeding failure (Ens et al. 1993). For exam- in ring-tailed lemurs Lemur catta and blue ple, in rock wallabies Petrogale assimilis, which monkeys Cercopithecus mitis, estrous females form monogamous pairs, some females often solicit mating from several partners breed both with resident males and with ex- from outside their group in the course of a tra-group males (Spencer et al. 1998). These single day (Jolly 1966; Cords et al. 1986). females are more likely to breed with males Similarly, female brown capuchin monkeys other than their mate if their previous off- Cebus apella, as well as females in several spring failed to survive to emergence from baboon and macaque species that live in the pouch. However, not all studies show multi-male groups, commonly make active that multiple mating increases fecundity, attempts to mate with several different and, in some rodents, females that mate with males (Taub 1980; Janson 1984). Even in multiple partners show reduced rates of con- these situations, it can be difficult to be ception (Schwagmeyer 1986). For example, sure that females are not coerced into mat- female deermice Peromyscus maniculatus and ing with multiple partners, but some stud- Djungarian hamsters Phodopus sungorus sun- ies are able to exclude this possibility. For gorus that mate with multiple partners are example, in yellow-toothed cavies, estrous less likely to become pregnant than those females race between males, making it that mate with a single partner (Dewsbury difficult for single males to monopolize and Baumgardner 1981; Dewsbury 1982a; them (Rood and Weir 1970; Rood 1972; Wynne-Edwards and Lisk 1984), perhaps be- Schwarz-Weig and Sachser 1996). Experi- cause the risk of male infanticide increases ments in which receptive females were al- when multiple males have access to a fe- lowed to choose between different males in male’s territory and because it is beneficial to 16 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 females to avoid conception (Dewsbury variation in female mate choice and 1982a). partner number In other cases, mating with multiple Although most studies of female mate partners may increase the survival of foe- choice have investigated whether there are tuses to term or the survival of young. For consistent female preferences for particu- example, in captive yellow-toothed cavies, lar characteristics in males, the benefits females that are allowed to mate with mul- and costs of particular choices are likely to tiple partners have fewer still-births and vary in space and time. This might be ex- successfully wean significantly more of pected to lead to variation in sampling tac- their pups (Keil and Sachser 1998). Since tics, mating preferences, and degree of the same males were used to fertilize single choosiness, and there is increasing evidence versus multiple mating females in this ex- that this is indeed the case (Zeh and Zeh periment, and young were suckled by mul- 1996; Widemo and Saether 1999; Fawcett tiple females (Ku¨nkele and Hoeck 1995), and Johnstone 2003). Studies of birds show this effect was unlikely to be a consequence that the strength and, in some cases, the of differences in male quality or of differ- direction of female mating preferences can ences in parental care, and the most likely vary widely (Chaine and Lyon 2008), and explanation is that sperm competition weeded out qualitatively inferior several studies indicate that the strength of (Sivinski 1984; Keil and Sachser 1998). In female mating preferences varies in mam- other cases, mating with multiple males may mals as well. For example, in mice, prefer- increase the survival of juveniles by increas- ences for MHC-dissimilar males that can be ing the amount of care and protection they detected in estrous females disappear when receive from males (Goldizen 1987) and re- females are not in estrus (Egid and Brown ducing the risks of infanticide (Hrdy 1981). 1989). Several studies of humans also suggest In Japanese macaques Macaca fuscata, males that MHC-related odor preferences as well as are eight times more likely to attack infants if female preferences for in males they have not previously mated with their vary with the stage of the reproductive cycle mothers, and infants born to females that or the hormonal status of subjects (Jordan mate with multiple males attract less aggres- and Bruford 1998; Penton-Voak et al. 1999). sion (Soltis et al. 2000). Similarly, among The probability that females will mate some rodents in which male infanticide is with multiple partners also changes through- common, controlled experiments show that out the reproductive cycle in some species. resident males are less likely to attack neo- In several monkey species, for example, fe- nates if they have previously had sexual ex- males initiate more frequently perience with the mother (vom Saal 1984; around the time of ovulation than they do Ebensperger 1998a,b). A final possibility is during other times of the cycle, and sexual that mating with multiple males contributes behavior declines considerably during the lu- to the genetic quality of offspring, either by teal phase (Manson 2006). In female chim- increasing the chance that a female will panzees Pan troglodytes, individuals com- breed with a higher quality male (trading- monly copulate with multiple males during up) or by increasing competition between the early stages of the estrus cycle but are sperm in the female reproductive tract more likely to copulate repeatedly with high- (Schwagmeyer 1984; Eberhard 1996). How- ranking males during the later stages, when ever, empirical evidence that mating with conception is most likely (Matsumoto-Oda multiple partners improves the quality of a 1999). However, changes in the probability female’s offspring is not yet available for that females will conceive are also likely to mammals. affect the behavior of males, and it is often March 2009 FEMALE MATE CHOICE IN MAMMALS 17 difficult to be sure that changes in the num- several studies have demonstrated, the ber of partners are a consequence of female chance that particular males will attract the decisions rather than male coercion. attention of females does not necessarily re- flect the probability that they will indeed Discussion mate with them, and mating frequency is not As Darwin described, intrasexual competi- always closely related to the probability of tion is widespread in mammals, and it is com- successful fertilization (Dewsbury 1982a). monly associated with strong selection favor- Moreover, as the costs and benefits of mate ing the development of traits that enhance choice in captive animals may differ from competitive success in males, who commonly those that are important in natural popula- use their greater size and strength to con- tions, there is a danger that the extent of strain female mate choice or to coerce fe- mate choice and the basis of female prefer- males into mating with them (Clutton-Brock ences in captive animals under controlled and Parker 1995). The prevalence of intra- conditions differ from the usual situation in sexual competition and coercive tactics in natural populations. males and the structure of mammalian The limitations of existing studies on fe- breeding systems complicate attempts to male mate choice in mammals have implica- demonstrate that female mating preferences tions for future research. In birds, controlled have an important influence on male mating experiments involving the modification of success. In particular, the common tendency male signals in natural populations have for females to be attracted to particular sites, played an important role in studies of mate combined with male competition for pre- choice (Andersson 1982, 1994), and male ferred mating territories, means that neither signals have been successfully manipulated variation in male mating success nor corre- under natural conditions in a number of lations between male mating success and mammals (Brotherton 1994; West and male phenotype provide reliable indications Packer 2002; Brotherton and Komers 2003; of the importance of female choice. These Charlton et al. 2007). Since modifying visual problems are well-illustrated by recent stud- signals often presents major logistic prob- ies of lek-breeding mammals that were ini- lems in mammals, experiments involving the tially thought to offer opportunities to assess manipulation of olfactory and auditory sig- female mating preferences uncontaminated nals used by males to attract females are now by the effects of male competition. However, a priority. Future studies might sensibly focus detailed studies of mammalian leks suggest on species, such as some diurnal rodents that male competition for particular territo- (Huck et al. 1986; Schradin and Pillay 2004; ries, as well as individual differences in the Schradin 2005a,b; Solomon and Keane capacity of males to exclude marauders and 2007), in which individuals can both be eas- retain females in their territory, probably has ily maintained in captivity and observed in an important influence on male success, and the wild, allowing controlled experiments on even evidence that females are more likely to female choices under captive conditions to mate with particular males per unit time be integrated with experimental and obser- spent on their territories is not necessarily an vational approaches in natural populations. indication of strong mating preferences. The As yet, there is no clear indication that most convincing evidence for female mate female mate choice is either less important choice in mammals comes from studies of or is less likely to be maintained by indirect captive mammals—mostly rodents—carried benefits in mammals than in birds. Empirical out under controlled conditions where the research suggests that the male characteris- effects of male competition can be excluded tics favored by female mammals cover much and where it is possible to demonstrate that the same range as in birds. These include females are attracted to particular categories female preferences for males likely to be of males (Gosling et al. 2000; Gosling and successful in competitive interactions, indi- Roberts 2001a,b). However, even experi- viduals with condition-related displays or ments of this kind have their limitations. As secondary sexual characters, unrelated or 18 THE QUARTERLY REVIEW OF BIOLOGY Volume 84 genetically compatible partners, and, in partner has yet to be investigated, but trends some species, the preference for mating with of this kind might be expected (Sheldon multiple partners. Some female preferences, 2000). such as those for mating with dominant part- The perception that female mate choice ners, appear likely to be maintained by direct is less highly developed and that it less fitness benefits. Others, such as preferences commonly involves preferences for male for genetically dissimilar partners, appear characteristics associated with genetic qual- likely to be maintained by heritable benefits ity in mammals than in birds has probably to their offspring. In many cases, benefits of arisen partly because of differences in the both kinds are likely to be involved. How- relative importance of visual and olfactory ever, it seems likely that there may be quali- signaling modalities in the two groups. The tative differences between birds and mam- evolution in many birds of elaborate plum- mals in the basis upon which females select age that is more highly developed in males mating partners. As a result of the preva- suggests the importance of mate choice lence of coercive tactics in male mammals and indicates the cues that females are and their potentially high costs to females likely to use in choosing mates, whereas (Smuts and Smuts 1993; Clutton-Brock and the elaboration of male olfactory signaling Parker 1995), female mammals may show stronger preferences than female birds for in mammals is less obvious to human ob- mating partners capable of providing ade- servers. Both the complexity of olfactory quate protection against other males, which signals and the extent of sexual dimor- may help to explain why they commonly se- phism in signal structure have still been lect for more competitive partners or indi- rather sparsely explored (Roberts and Gos- viduals with high testosterone levels. Con- ling 2003), and it is possible that in some versely, since male contributions to rearing mammals, males produce olfactory signals offspring are typically larger in birds than that match the elaboration and complexity mammals, female birds may more com- of the peacock’s tail (Petrie et al. 1991) monly favor partners that are likely to invest or the sedge warbler’s song (Catchpole heavily in parental care and may be less likely 1980). to select competitive partners if they are likely to contribute less to parental care. acknowledgments Whether female mammals, like female birds, We are grateful to Maurice Gosling, Marc Hauser, commonly adjust their level of parental in- Marion Petrie, James Thomson, Richard Wrangham, vestment in relation to the quality of their and two anonymous referees for their comments.

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