Sexual Selection in Primates: New and Comparative Perspectives / Edition 1

by Peter M. Kappeler, Carel P. van Schaik

Overview

Successful reproduction is not always a cooperative affair, but rather a competition between males, with females having the final "say." Throughout there is conflict regarding when, with whom and how often mating should occur. This volume provides the first comprehensive summary of the various forms of sexual communication and behavior and the consequences of the interaction between the sexes.

Product Details

ISBN-13:	9780521537384
Publisher:	Cambridge University Press
Publication date:	05/13/2004
Edition description:	New Edition
Pages:	300
Product dimensions:	7.48(w) x 9.72(h) x 0.67(d)

About the Author

PETER KAPPELER is Head of the Department of Behaviour and Ecology in the Deutsches Primatenzentrum in Göttingen, Germany.

CAREL VAN SCHAIK is a Professor in the Department of Biological Anthropology and Anatomy at Duke University, North Carolina.

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Part I
Introduction

1 • Sexual selection in primates: review and preview

PETER M. KAPPELER
Department of Behaviour and Ecology German Primate Centre Göttingen, Germany

CAREL P. VAN SCHAIK
Department of Biological Anthropology and Anatomy Duke University Durham, NC, USA

INTRODUCTION

Sexual selection theory has provided a successful framework for studying sex differences in behaviour, morphology, development and reproductive strategies, as well as the resulting mating systems (Campbell, 1972; Emlen & Oring, 1977; Bradbury & Andersson, 1987; Andersson, 1994). Humans and other primates have played an important stimulating role in the original development of the second pillar of modern evolutionary theory (Darwin, 1871; Clutton-Brock, this volume), and primates were the subjects of the first scientific paper devoted to sexual selection (Darwin, 1876). After languishing for nearly a century, sexual selection theory was re-discovered by evolutionary biologists and students of animal behaviour, who made it one of the most active fields of organismal biology by refining the theoretical framework and testing it with many new empirical data, mainly from insects and birds (Andersson, 1994). Studies of sexual selection in primates, in contrast, were not resumed with the same general enthusiasm and vigour, but there were notable exceptions (e.g. Crook, 1972; Clutton-Brock et al., 1977; Harvey et al., 1978; Hrdy, 1979; Smuts & Smuts, 1993; van Schaik et al., 1999; van Schaik, 2000a). The first aim of this chapter is to provide an introductory summary of the main concepts and mechanisms of sexual selection theory in a way that highlights these contributions and questions of general interest from primatology, and to introduce the subsequent chapters of this volume.

A second aim of this chapter, and this volume in general, is to encourage integration of studies of sexual selection in primates with related work on other taxa and in other disciplines, including evolutionary theory (see also Maestripieri & Kappeler, 2002). Students of primates have addressed numerous specific questions about aspects of sexual selection, but the salient results and general conclusions emerging from these studies have not been systematically synthesised for more than 15 years (see Hrdy & Whitten, 1987; Smuts, 1987a, b). Moreover, recent studies of human sexual behaviour have addressed new, evolutionary questions (Buss, 1994; Thornhill & Gangestad, 1996), but the resulting new discipline of evolutionary psychology has remained largely isolated from primatology, even though comparative evidence from non-human primates, in particular, could advance the study and interpretation of human sexual strategies. Finally, observational and experimental studies of aspects of sexual selection in other mammals continue to provide an important comparative basis for characterising taxon-specific reproductive strategies and constraints that need to be more fully integrated into future research on primates and humans. We therefore hope that the chapters in this book stimulate exchange of new developments in theoretical, human, primate and mammalian sexual selection studies and will foster discussion among these largely separated sub-disciplines.

SELECTION IN RELATION TO SEX

Having developed the theory of evolution by natural selection (Darwin, 1859), Charles Darwin realised that a number of traits, mostly sexually dimorphic ornaments and armaments, did not seem to promote survival or were not primarily involved in the production of offspring. He suggested that these secondary sexual traits confer an advantage with respect to acquiring mates (Darwin, 1871), by intimidating rivals and/or by attracting mates, and he developed a theory of selection in relation to sex that was linked to natural selection. Primates show abundant evidence of such dimorphism (recently summarised by Dixson, 1998) in maternal investment; growth and developmental patterns; body and canine size; scent glands and scent-marking behaviour; vocalisations and various visual ornaments such as manes, flanges, coloured skin and fur; as well as interspecific variation in traits such as relative testes size and penile morphology, and the presence of sexual swellings. All these sex differences suggest that the traits involved evolved under the influence of sexual selection. The same is true for a host of sex differences in behavioural, physiological and even ecological and life-history characteristics (Dixson, 1998; van Schaik et al., 1999; Kappeler et al., 2003), including adaptive adjustment of birth sex ratios (Clutton-Brock & Iason, 1986; Dittus, 1998; but see Silk & Brown, this volume), a body of theory to which primate studies have contributed importantly (Clark, 1978; Silk, 1984; van Schaik & Hrdy, 1991; Brown, 2001).

Whereas Darwin's conceptual distinction between natural and sexual selection continues to be appreciated, more recent analyses and arguments summarised by Clutton-Brock (this volume) support the consideration of sexual selection as a form of natural selection that acts differently on the two sexes. This perspective leads to an emphasis on studying causes and consequences of sex-specific effects of selection. Why selection operates differentially on males and females has traditionally been related to fundamental aspects of their reproductive physiology and biology. As reviewed in detail by Gowaty (this volume), traditional sex roles, characterised by discriminating females and competitive males, were theoretically based on an elaboration of the consequences of anisogamy (Williams, 1966; Parker, 1979; Bulmer & Parker, 2002) and gained initial empirical support through a simple experiment with fruit flies (Bateman, 1948). Robert Trivers (1972) subsequently decoupled sex roles from gamete size and linked them instead to relative parental investment. In the end, variation in sex roles was convincingly linked to sex differences in potential reproductive rates (Clutton-Brock & Parker, 1992).

Sexual selection can be dissected into distinct components. Right from the start, Darwin identified mate choice (intersexual selection) and competition for mating partners (intrasexual selection) as driving forces behind adaptations in response to sexual selection (Bradbury & Andersson, 1987; Kirkpatrick, 1987; Andersson, 1994; Andersson & Iwasa, 1996; Cunningham & Birkhead, 1998; Kokko et al., 2002; see Clutton-Brock, this volume, for a historical perspective). However, it took until the 1970s for a third major component to be recognised: mating or intersexual conflict (Parker, 1979). This conflict varies from disagreement over the identity of mates or the frequency of mating to the chemical composition of seminal fluids. The outcome of this conflict may vary widely, producing stable equilibria in which one sex has the advantage, or complex arms races between the sexes (e.g. Hammerstein & Parker, 1987; Johnstone & Keller, 2000). We will return to these mechanisms with an emphasis on primate examples below.

Despite these theoretical clarifications, it is difficult in practice to demonstrate that sexual selection was responsible for the presence of a trait. For that, precise quantification and documentation of inter-individual variation, their effects on conspecifics, as well as their relation to variation in reproductive success is still required (see Snowdon, this volume).

COMPETITION FOR MATES

Fitness of male primates is generally limited by access to receptive females, and males compete among themselves either to exclude rivals from access to females altogether, or to mate more often and/or at the right time (Kappeler, 1999). As a result, several genetic studies have shown that male primates generally exhibit greater variance in reproductive success than females (e.g. de Ruiter et al., 1994; Gerloff et al., 1999; Launhardt et al., 2001; Soltis et al., 2001; Vigilant et al., 2001), even though some of the variance among males is reduced when the entire lifespan is considered ( Altmann et al., 1996; van Noordwijk & van Schaik, this volume). Determinants and consequences of variation in male monopolisation potential and variation in competitive mechanisms employed under different circumstances are therefore central questions for a better understanding of male reproductive strategies.

The evolutionary impact of mating competition among primate males on their morphology, life history, physiology and behaviour has been recognised for a long time (Schultz, 1938), although it took until the 1970s for comparative evidence to emerge (Crook & Gartlan, 1966; Crook, 1972; Clutton-Brock et al., 1977; Harvey et al., 1978; Alexander et al., 1979; Short, 1979; Harcourt et al., 1981; Harvey & Harcourt, 1984; Clutton-Brock, 1985). Several of the examples of systematic and predicted relationships between mating systems and morphological and behavioural correlates were first documented in primates and have become classic textbook examples (e.g. Krebs & Davies, 1992).

Sexual dimorphism in body and canine size, in particular, have fascinated primatologists for a long time because detailed data for a large number of species showed a rich variation, including some of the most spectacular cases found among mammals, such as mandrills, orangutans and gorillas (Short, 1979; Rodman & Mitani, 1987; Weckerly, 1998; Setchell et al., 2001). Morphological differences between human males and females, as well as their development over evolutionary times, have likewise occupied generations of anthropologists (e.g. Ghesquiere et al., 1985; Plavcan & van Schaik, 1997). It has long been evident that body and canine size are good indicators of the intensity of male-male competition, but only recently are we actually beginning to explain most of the variance, especially among polygynous species (Plavcan, 2001, this volume; Lindenfors, 2002). Studies of primate sexual dimorphism have also stimulated similar work in other mammals (Alexander et al., 1979; Gittleman & van Valkenburgh, 1997; Weckerly, 1998; Lindenfors et al., 2002). A second recent development in studies of primate sexual dimorphism has been a focus on developmental questions (Leigh, 1995; Leigh & Shea, 1995; Leigh & Terranova, 1998; Smith & Leigh, 1998; Pereira & Leigh, 2003) that has been extended to other aspects of sexual selection by Setchell and Lee (this volume; see also Badyaev, 2002).

Partly as a result of this additional focus on ontogeny, there has been increasing recognition of the fact that sexual selection does not only target adult males in the context of mating competition. Rather, the entire life history of males, including their morphological and physiological development, as well as their timing of transfers into other groups, has apparently been shaped by sexual selection ( Alberts & Altmann, 1995a, b). Setchell and Lee (this volume) summarise and evaluate the effects of intrasexual selection during various phases of the ontogeny of male primates (see also Pereira & Leigh, 2003), whereas Utami and van Hooff (this volume) discuss the enigmatic special case of bimaturism in orangutans. Along the same lines, van Noordwijk and van Schaik (this volume) focus on behavioural decisions by male primates related to the way they can achieve high reproductive success, showing that multiple aspects of their career choices, from the risk taken in rank acquisition to the nature and timing of transfer decisions, have been shaped by intrasexual selection. Convergent processes and outcomes in an independent taxon are described by Rubenstein and Hack (this volume) in their analysis of zebra stallions' behavioural and evolutionary responses to trade-offs created by natural and sexual selection.

THE MALE PERSPECTIVE OF COMPETITIVE SCENARIOS

The nature of competition among primate males is determined by the monopolisability of females, which in turn is determined by various female features: their spatial distribution, the size of their groups and the degree of synchrony of their receptive periods (Mitani et al., 1996a; Nunn, 1999; Kappeler, 2000; see also Emlen & Oring, 1977; Jarman, 1983; Ims, 1988, 1990; Clutton-Brock, 1989; Carranza et al., 1995; Creel & Macdonald, 1995; Michener & McLean, 1996). How many members of the same and opposite sex live together is both a determinant and outcome of sexual strategies, in particular those of males (Kappeler & van Schaik, 2002), but also, indirectly, those of females, whose behaviours affect the parameters of male-male competition (Wiley & Poston, 1996; Gowaty, 1997).

From the males' perspective, the most basic question is whether females are dispersed in space, or not. Whenever reproductively active females are not associated with each other, males must make a strategic decision about dispersal and ranging behaviour (Dunbar, 2000). Depending on the males' decision, two fundamentally different types of social organisations can be distinguished: males either also range independently, often trying to encompass ranges of several females within their home range, or they associate permanently with either a single female or a group of spatially clumped females (van Schaik & Kappeler, 1997, 2003).

Given a particular spatial distribution of females and the males' decision to associate with them or not, three hierarchical levels of intermale competition can be distinguished (Kappeler, 1999; Setchell & Kappeler, 2004). First and foremost, males ought to be concerned with gaining access to as many receptive females as possible, while at the same time preventing rivals from doing so. Complete monopolisation of several females should always be the most successful male reproductive strategy and, thus, the top male priority. Second, if complete monopolisation is not possible, a male should try to maximise his number of copulations, while keeping the number of copulations by rivals at a minimum. Finally, if males cannot skew the number of copulations in their favour, they may rely on various mechanisms of post-copulatory selection to maximise their chances of fertilisation with just one or a few copulations. At each level of competition, mechanisms of both scramble and contest competition can be employed and combined.

MECHANISMS OF MATING COMPETITION

Primate males employ a number of mechanisms before, during and even after mating to out-compete their rivals in the race for fertilisations (summarised in Dixson, 1998; Setchell & Kappeler, 2004). Apart from the timing in relation to mating (before, during, after), the distinction between contest (or interference) and scramble (or exploitation) mechanisms is useful to characterise competitive mechanisms. Along this spectrum, the use of physical force, aggression and threat gives way to indirect mechanisms not requiring physical contact, such as effective mate searching and sperm competition. Below, we briefly characterise the best-known mechanisms in primates (see also Setchell & Kappeler, 2004 for a more detailed discussion).

Receiving and sending signals

First, in species in which males are not permanently associated with females, males need to find receptive females. Males with increased endurance and improved abilities to detect female acoustic and olfactory signals from long range should have an advantage over others. However, the sensory sensitivities and capabilities of solitary primates, for which this ability is most important, remain virtually unstudied (cf. Schwagmeyer & Woonter, 1986; Ims, 1990; Schwagmeyer et al., 1998).

Second, because of the inherent risks of overt fighting, there is selection for displays and signals during male encounters. Visual signals emanating from body and canine size may play a role in this context, as well as the coloured skins, manes and capes of hair, cheek flanges and other facial adornments found in males of many primate species ( Dixson, 1998; Snowdon, this volume). However, in contrast to birds ( Andersson, 1986; Zuk et al., 1990; Zuk, 1991; M⊘ller & Pomiankowski, 1993), there is very little evidence demonstrating that the comparatively rare sexually-dimorphic ornaments of primates are actually condition-dependent (but see Setchell & Dixson, 2001b; see also West & Packer, 2002) or that male rivals even attend to these signals (but see Gerald, 2001). Moreover, no studies to date have systematically investigated female preference for male ornaments in non-human primates, which is a potential additional or alternative function of these visual signals.

Sexually dimorphic acoustic signals, such as loud calls, could also function in repelling and deterring non-resident rivals or in aiding species recognition and influencing female mating decisions, but there has been very little support for these hypotheses in recent reviews and comparative tests (Wich & Nunn, 2002; Snowdon, this volume). Furthermore, there is some evidence to suggest that the transfer of olfactory signals among primate males has been shaped by sexual selection. Males often have more and bigger scent glands than females and they also mark and investigate scents more often (Dixson, 1998; Heymann, 1998). In some primates, the frequency, quality and effect on the receiver of male signals have been shown to be status-dependent (Kappeler, 1990c, 1998; Fornasieri & Roeder, 1992; Perret, 1992; Kraus et al., 1999; Maggioncalda et al., 1999), but much more compara- tive and experimental work is required to illuminate the function of pheromones in intrasexual selection further.

Physical prowess and dominance

Whenever males fight for access to receptive females, sexual selection theory predicts that characters contributing to physical superiority, such as large body size and/or weaponry will be favoured (Darwin, 1871). Most polygynous primates are indeed sexually dimorphic in body size and weaponry because selection for physical superiority is more intense among males, presumably because they compete for non-shareable benefits directly linked to fitness (van Schaik, 1996), even though selection for such traits is not limited to males (Plavcan et al., 1995). The resulting sexual dimorphism in body and canine size has been analysed mostly among species (but see Bercovitch, 1989), using mating system classification (Clutton-Brock et al., 1977; Kappeler, 1990a, 1996; Lindenfors & Tullberg, 1998), operational sex ratio (Mitani et al., 1996b) or behavioural competition levels (Kay et al., 1988; Plavcan & van Schaik, 1992; Plavcan, 2001) to determine the relative contribution of intrasexual selection vis-à-vis other ecological factors and evolutionary by-products and developmental mechanisms (reviewed in Plavcan, 2001, this volume; Pereira & Leigh, 2003; Setchell & Lee, this volume).

Dominance, which is typically based on physical superiority, is an important behavioural mechanism used by male primates to obtain access to receptive females (Packer, 1979; Samuels et al., 1984; Shively & Smith, 1985; Bercovitch, 1988). The priority-of-access model, which postulates that the dominance hierarchy functions as a queue and that the number of simultaneously fertile females determines male access, provides a theoretical framework for the analysis of dominance effects (Altmann, 1962). This mechanism of reproductive competition is often manifested as mate guarding or consortships. In species where consortships occur, most copulations take place during this time, thus increasing the consorting male's probability of mating, in addition to providing an opportunity for preventing rivals from doing so. High-ranking males are often more successful in forming consortships (Bercovitch, 1991; Cowlishaw & Dunbar, 1991), but some females consort with several males in succession (Hrdy & Whitten, 1987; Hrdy, 2000), indicating that females can affect the competitive regime for males both directly and indirectly.

There has been much debate over the relationships among dominance, mating and reproductive success in male primates (Cowlishaw & Dunbar, 1991; de Ruiter & van Hooff, 1993). The genetic measures of reproductive skew among males needed to examine the crucial relationship between mating success and reproductive success are gradually becoming available (e.g. Pope, 1990; de Ruiter et al., 1992; Altmann et al., 1996; Launhardt et al., 2001). The priority-of-access model, which incorporates the effects of indirect female choice (Wiley & Poston, 1996), provides the basic expectation for reproductive skew among males. Deviations from it are due to the success of alternative mating tactics, sperm competition and female mating preferences (M⊘ller & Ninni, 1998; Petrie & Kempenaers, 1998; Johnstone et al., 1999; Engh et al., 2002). Future studies should strive to determine the relative contributions of these processes in primates.

Inhibition and alternative tactics

In several primates, subordinate males show signs of partial physiological suppression of sexual function, characterised by reduced body mass and condition; reduced testis size; smaller, less active scent glands; reduced development of secondary sexual traits; decreased levels of circulating testosterone, growth hormone and luteinising hormone; lower frequencies of sexual and olfactory behaviours, or any combination thereof (Schilling et al., 1984; Perret, 1992; Kraus et al., 1999; Maggioncalda et al., 1999, 2000; Setchell & Dixson, 2001a; Utami & van Hooff, this volume). This phenomenon can be interpreted as an adaptation of the subordinate (see Gross, 1996): inhibition allows him to remain in the presence of dominant males, thereby avoiding aggression and the costs of high testosterone for a period (Utami et al., 2002; Setchell, 2003). Similarly, juvenile males may prolong growth and delay maturation to achieve larger size and competitive ability upon entering the mating arena (Alberts & Altmann, 1995b). Because testes are typically already spermatogenic in maturing males, they may obtain a few low-risk sneaky copulations while in this phase (e.g. Berard et al., 1994). On the other hand, because inhibited males may suffer a disadvantage in sperm competition and because they are less attractive to females (e.g. van Hooff & Utami, this volume), the inhibition may reflect pressures exerted by the dominant male(s). More information on primates in nature, as well as other mammals (e.g. Arnold & Dittami, 1997), is needed to determine the relative importance of self-imposed inhibition and dominant-imposed suppression. One possibility is that where stress is a major mechanism, we are dealing with true suppression imposed by the dominant (see Sapolsky, 1985; von Holst, 1998), whereas in the absence of stress the inhibition may reflect an adaptation on the part of the subordinate.

At least four behavioural mechanisms of alternative mating strategies have been recognised. First, males in poor physical condition or social position can form coalitions to force a superior male to relinquish a receptive female (Bercovitch, 1988; Noë & Sluijter, 1990), whereas dominant males may need to form coalitions to improve their effectiveness at mate guarding in the presence of too many rivals (Watts, 1998). Second, adult males living in all-male bands throughout the year can raid groups containing multiple females and a single resident male during the brief mating season. By doing so, they may avoid the costs of being around dominants for most of the year (Borries, 2000; Cords, 2000). The presence of such all-male groups may have profound effects on social organisation (see Rubenstein & Hack, this volume). Third, young, less powerful males may associate with a fully developed male and the group of females associated with him, thereby obtaining occasional mating opportunities and prospects of succession, at reduced costs of female defence to the dominant (Pope, 1990; Robbins, 1999; Watts, 2000). Finally, by forming friendships with particular females, some males obtain access to at least one female at little risk of aggression from dominant males (Smuts, 1985). Despite these many diverse examples, it is likely that not all alternative mating tactics of male primates have been discovered yet (cf. Koprowski, 1993; Stockley et al., 1994; Gemmell et al., 2001), and we clearly need detailed long-term studies to understand their stability and genetic payoffs.

Copulatory and post-copulatory mechanisms

Once a male has successfully gained access to a receptive female, variable aspects of copulation may influence his reproductive success. First, copulation frequency is much higher in promiscuous than in monandrous species, both reflecting and creating different intensities of sperm competition ( Dixson, 1998). Second, copulatory patterns - including variation in intromission and ejaculatory patterns, number of thrusts before ejaculation, length of intromission, duration of copulation, and the need for single or multiple intromissions prior to ejaculation - exhibit similar variation among species that appear to correlate with broad mating system categories (Dixson, 1998). Because most primates are notoriously promiscuous, presumably as a result of several female benefits and trade-offs (Gangestad & Thornhill, this volume; van Schaik et al., this volume), sperm competition among primates is widespread and intense (Birkhead & Kappeler, this volume), constituting a powerful and ubiquitous mechanism of mating competition. With the exception of testes size (Harcourt & Gardiner, 1994; Harcourt et al., 1995; Harcourt, 1996; Kappeler, 1997a), however, physiological and morphological determinants and correlates of success in sperm competition in primates are still relatively poorly known (Dixson, 1998; Birkhead & Kappeler, this volume). To what extent individual variation in primate testes size is positively correlated with competitive potential (rank, body size) on the one hand, and mating and reproductive success on the other hand, independent of potentially confounding co-variables, also remains largely unresolved by the existing interspecific studies (but see Bercovitch, 1989). As with studies of sexual dimorphism, studies of variation in testes size among primates have inspired and influenced similar investigations in other mammals (Kenagy & Trombulak, 1986; Dewsbury & Pierce, 1989; M⊘ller, 1989; M⊘ller & Birkhead, 1989; Heske & Ostfeld, 1990; Rose et al., 1997; Gomendio et al., 1998; Hosken, 1998).

Even after fertilisation has been achieved, male reproductive competition can continue with two additional mechanisms at the intersection of male-male competition and intersexual conflict. First, females may terminate investment in the developing foetus in the presence of a new dominant male. This 'Bruce effect', which is well known in rodents (Schwagmeyer, 1979; Mahady & Wolff, 2002), is advantageous for the male inducing it, because it will create a mating opportunity in the near future, so that it was originally considered a product of male-male competition (Trivers, 1972). However, whenever the risk of infanticide or the loss of paternal care following birth are high (Labov, 1981), resorption or abortion is primarily adaptive from the female perspective so that it may ultimately represent more of a female reproductive strategy. Despite the difficulties of detecting the early termination of reproduction, there is some evidence that it may occur among primates under the right circumstances (Pereira, 1983; see also Forbes, 1997).

Second, males may interfere with the reproductive success of rivals, while at the same time improving their own, by committing sexually selected infanticide. The evidence in support of this hypothesis has recently been summarised (van Schaik & Janson, 2000) and is overwhelming. Briefly, males in dozens of primate species have now been observed to kill unrelated dependent infants, leading to a faster resumption of the affected mother's reproductive activity, thereby creating additional mating opportunities for the male (Hrdy, 1979; van Schaik, 2000a). Due to their particular life history characteristics, primates may be especially vulnerable to infanticide (van Schaik & Kappeler, 1997), but the same principles have been demonstrated in other mammalian lineages (van Noordwijk & van Schaik, 2000; van Schaik, 2000b). This strong selective force on male and female reproductive success has shaped many other aspects of primate reproductive physiology and social behaviour (van Schaik & Janson, 2000; van Schaik et al., this volume).

MATE CHOICE

Mate choice by females has been the aspect of Darwin's original theory initially meeting the most scepticism. Since the 1970s, however, female choice has been one of the most intensively and productively studied topics in evolutionary biology (e.g. Searcy, 1979; O'Donald, 1980; Andersson, 1982; Kirkpatrick, 1982; summarised in Andersson, 1994). Whereas the sophistication of theoretical models is as yet not matched by equally sophisticated empirical evidence, we now have a good idea about the underlying behavioural and genetic mechanisms, as well as the benefits females may derive from careful choice of their mates (e.g. Hamilton & Zuk, 1982; Zuk, 1991; Johnstone, 1995; Gibson & Langen, 1996; M⊘ller, 1997, 2000).

In some cases, females obtain direct, material benefits from choosing a particular male that have positive effects on their fecundity (Thornhill & Alcock, 1983). More commonly, however, females obtain indirect benefits in the form of advantages accruing to their offspring, because they choose males of the right species (Panhuis et al., 2001), reduce the effects of inbreeding by discriminating against closely related males (Perrin & Mazalov, 2000), or prefer mates with genotypes that maximise offspring heterozygosity (McCracken & Bradbury, 1977). Phenotypic indicators of male quality that are preferred by females can be colourful patches, length of tails, symmetry of structures, aspects of male calls, and age or the morphological correlates thereof (Andersson, 1986; McComb, 1991; M⊘ller, 1992; Swaddle & Cuthill, 1994; Gangestad & Thornhill, 1998; this volume; Widemo & Saether, 1999; Waynforth, 2001). Nonetheless, some doubt persists as to whether the currently most popular models provide a complete explanation, for instance because the presence of some pre-existing female preferences may reflect sensory exploitation by males (Ryan & Keddy-Hector, 1992; Endler & Basolo, 1998; Ryan, 1998), thus prompting additional modelling (see e.g. Kokko et al., 2002).

FEMALE CHOICE IN PRIMATES

As in other mammals, fitness of female primates is limited by access to resources and the quality of parental care (Trivers, 1972; Emlen & Oring, 1977). Because primates have relatively slow life histories and each female may only produce a few single young during her reproductive career (Lee, 1996; Ross, 1998), female primates are expected to select their mates carefully. The potential importance of female choice for female fitness is further accentuated by the fact that males in most primate species provide little or no direct infant care. However, apart from the active avoidance of inbreeding (Grob et al., 1998), there is surprisingly little evidence for female choice in primates, either in terms of the exclusive selection of particular mates or the consequences of such persistent choices on male phenotypes (Small, 1989; Keddy-Hector, 1992). Here we examine some of the possible reasons for this, from the demographic context, to mating behaviour, to post-mating discrimination.

Living in permanent social units with long-term membership - a near-universal feature of primates - imposes potential demographic constraints on choice. Thus, species living in pairs are predisposed towards monandry, although recent behavioural and genetic studies revealed that extra-pair copulations are possible, sometimes common, and often initiated by female primates (Palombit, 1994; Fietz et al., 2000; Sommer & Reichard, 2000). Hence, females may in fact often select or reject mates despite demographic or social constraints. Females may also exercise choice by affecting the composition of their social units. Transfer between social units is present in some species (e.g. Sterck & Korstjens, 2000), but is likely to be an expensive alternative option relative to the fitness benefits obtained by unconstrained female choice of mates. Females of some species are known to exert influence on the success of male immigration attempts (e.g. Smuts, 1987a) or may not accept a male who has taken over the social unit they live in (e.g. Dunbar, 1984), but it is not clear how widespread these choices are. However, social units in which females have mating access to multiple males are remarkably common among primates (van Schaik, 2000b).

Within the demographic constraints imposed upon them by the nature of their social organisation, primate females show a striking tendency toward active promiscuity (Hrdy & Whitten, 1987; Hrdy, 2000; Paul, 2002) and employ still poorly studied mechanisms and criteria to choose mates, if they exercise any direct choice at all. In species with substantial direct male care, through female mate choice - or more precisely in this case, choice of polyandry - females may obtain important direct benefits (Goldizen & Terborgh, 1986; Goldizen, 1987). It is possible that the fitness benefits in terms of infanticide avoidance and protection by likely fathers (see van Schaik et al., this volume) outweigh any genetic benefits gained from choosing particularly attractive males in other social settings. Promiscuity is found in spite of the serious risks of disease transmission (Nunn & Altizer, this volume) and the tendency among mammalian males, prominently displayed by male primates, of trying to curtail the behavioural freedom of females to exert mate choice (see Gowaty, this volume) - an expression of mating conflict (see below).

Their reproductive physiology provides female primates with several mechanisms and levels of control to affect the number and identity of available mates (Wiley & Poston, 1996). First, seasonal reproduction, usually dictated by environmental factors, provides a necessary, albeit insufficient, condition for the synchronisation of cycles among several associated females. The more females are receptive at or during the same time, the smaller is the ability of a single dominant male to monopolise access to all of them (Emlen & Oring, 1977; Dunbar, 2000; Eberle & Kappeler, 2002). As a result, females may increase their opportunities to choose additional mates. Second, females can apparently vary the length of their follicular phase within certain limits, which has the same consequences for male monopolisation potential and female choice (van Schaik et al., 1999). Third, females in different species either advertise or conceal ovulation (Burley, 1979; Andelman, 1987; Sillén-Tullberg & M⊘ller, 1993; Converse et al., 1995; van Schaik et al., 1999; Heistermann et al., 2001), in effect manipulating males. By clearly advertising receptive periods, females can incite male-male competition without bearing the costs of prolonged and/or repeated matings (e.g. Hoelzel et al., 1999). By concealing ovulation, females reduce male monopolisation potential and increase the pool of potential mates because no male can restrict his mating effort to a particular time. The sexual swellings of some Old World monkeys and apes may fulfil both functions simultaneously. Increasing sexual swellings advertise the approach of a receptive period, but they do not allow pinpointing of the exact date of ovulation (see Nunn et al., 2001; Zinner et al., this volume). There is some evidence that these signals can also be used strategically (Zinner & Deschner, 2000).

An important behavioural mechanism of female choice is mating cooperation. With the possible exception of orangutans (Galdikas, 1985a, b; Schuermann & van Hooff, 1986; Fox, 2002; Utami et al., 2002), mating in primates requires active female cooperation. By simply walking away or sitting down, females can prevent matings at a particular time or by a particular male, albeit at some potential cost. Lunging or cuffing in response to the advances of males is an effective mechanism in many species without pronounced sexual dimorphism. Active solicitations and presentations towards particular males are common forms of positive female choice in other species (Janson, 1984, 1986). Lemurs constitute a particularly interesting case because lemur females have more freedom to choose than other primate females as they match males in size and weaponry (Kappeler, 1990a, 1991, 1996; Richard, 1992; Plavcan et al., 1995) and dominate them socially in all contexts (Kappeler, 1990b, 1993; Pereira et al., 1990; Kubzdela et al., 1992). Interestingly, polyandrous matings are nevertheless the rule among non-pair-living lemurs (Jolly, 1967; Richard, 1974; Sauther, 1991; Overdorff, 1998; Ostner & Kappeler, 1999; Radespiel et al., 2001), even though females do have and exhibit certain preferences (Pereira & Weiss, 1991). Bonobos present a similar, puzzling case (Wrangham, 1993; Parish, 1994). Future research will have to determine whether factors other than infanticide avoidance (Hrdy, 2000; Jolly et al., 2000), perhaps also proximate ones (de Waal, 1987; Hrdy, 1995), can explain the sexual behaviour of these species.

Active promiscuity will move the arena of mate choice to the post-mating period. Cryptic female choice (Eberhard, 1996) will tend to produce a discrepancy between mating and siring success. It is an adaptation to situations where females cannot keep males from mating or have other reasons to mate with multiple males (Gowaty, 1997; Tregenza & Wedell, 2000; Zeh & Zeh, 2001). Mechanisms of cryptic choice in primates remain largely unknown, but selective orgasm is one promising possibility deserving more investigation (see Birkhead & Kappeler, this volume).

VARIANT SEX ROLES AND SEXUAL CONFLICT

Whenever one sex has become the limiting factor for the reproductive success of the other sex, the latter will compete for access, and the former will exert choice. As discussed above, in many animals, and especially among mammals, females are the limiting factor for males, who therefore compete for access, allowing the females to exert their choice. However, this neat dichotomy is sometimes upset by cases of females competing for access to mates, or males exerting mate choice, as well as by a ubiquitous conflict of interest between the sexes (Gowaty, 1997, and this volume). We now address these complications.

COMPETITIVE FEMALES

Female-female mating competition for sexual access to mates has so far mostly been observed in artificial or rare situations (summarised in Nunn et al., 2001; but see Gowaty, this volume). It is not to be confused with various other phenomena that may superficially resemble it. Thus, the active role taken by females in soliciting matings (Hrdy, 1981; Hrdy & Whitten, 1987; van Schaik et al., 1999) does not necessarily reflect competition for access to mates (see below). Likewise, examples of inhibition of female ovarian activity in the presence of a dominant female in various callitrichids (Abbott, 1989) is generally thought to reflect female competition for access to helpers, rather than mates. Finally, females may compete over social access to dominant males, as in gorillas (Watts, 1992, 2000), but again there is no evidence for females competing for sexual access as well (Robbins, 1999).

If females actually compete for access to males, we expect them also to show the features that go with it: enlarged armaments or special ornaments where this competition is intense. Relatively increased female canine size is indeed associated with increased intensity and frequency of competition among females (Plavcan et al., 1995), which can have lethal effects (McGraw et al., 2002), but this interspecific effect is due to competition for resources and not for mates. Moreover, reversed sexual dimorphism, with females being larger or heavier than males, has also been documented in a few primate species, notably among lemurs (Kappeler, 1991; Wright, 1995; Schmid & Kappeler, 1998; Richard et al., 2002) and some New World monkeys (Ford, 1994), but again there is no evidence for escalated female competition in the context of mating in these taxa (Richard, 1987; Kappeler, 1993; Jolly, 1998).

Special female ornaments are expected where they enhance their owners being chosen by males. Pagel (1994) offered such an indicator explanation for female sexual swellings, and a recent field study of baboons presented the first support for this hypothesis (Domb & Pagel, 2001). However, Zinner et al. (2002, and this volume) conclude that the evidence for female competition for access to mates is weak. Moreover, their re-analysis and interpretation of the baboon data indicate that they actually offer more support for the idea that swellings indicate proximity to ovulation. Scent gland size and/or use in callitrichids may represent another potential example (Heymann, 1998), but these taxa typically contain only a single reproductive female. Thus, as theoretically expected, given their much higher parental investment and particularly slow reproductive rates, there is very little evidence for female-female competition in primates as of yet. However, incidental observations of females preferentially attacking oestrous females (Wasser, 1983) or harassing matings of other females (e.g. Linn et al., 1995) are nonetheless puzzling and require an explanation.

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Table of Contents

List of contributors; Foreword Robert L. Trivers; Preface; Part I. Introduction: 1. Sexual selection in primates: review and selective preview Peter M. Kappeler and Carel P. van Schaik; 2. What is sexual selection? Tim H. Clutton-Brock; 3. Sex roles, contests for the control of reproduction and sexual selection Patricia Adair Gowaty; Part II. Sexual Signals: Substrates and Function: 4. Sexual selection and communication Charles T. Snowdon; 5. Sexual selection and exaggerated sexual swellings of female primates Dietmar P. Zinner, Charles L. Nunn, Carel P. van Schaik and Peter M. Kappeler; 6. Female multiple mating and genetic benefits in humans: investigations of design Steven W. Gangestad and Randy Thornhill; Part III. Sexual Selection in Action: 7. Sexual selection, behaviour and sexually transmitted diseases Charles L. Nunn and Sonia M. Altizer; 8. Mating conflict in primates: infanticide, sexual harassment and female sexuality Carel P. van Schaik, Gauri R. Pradhan and Maria A. van Noordwijk; 9. Post-copulatory sexual selection in birds and primates Tim R. Birkhead and Peter M. Kappeler; Part IV. Development and Consequences: 10. Development and sexual selection in primates Joanna M. Setchell and Phyllis C. Lee ; 11. Alternative male reproductive strategies: male bimaturism in orangutans Suci Atmoko Utami and Jan A. R. A. M. van Hooff; 12. Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions Maria A. van Noordwijk and Carel P. van Schaik; 13. Sexual selection, measures of sexual selection and sexual dimorphism in primates J. Michael Plavcan; 14. Sex ratios in primate groups Joan B. Silk and Gillian R. Brown; 15. Natural and sexual selection and the evolution of multi-level societies: insights from zebras with comparisons to primates Daniel I. Rubenstein and Mace Hack; Index.

Editorial Reviews

"The book contains useful information for both novices and experts, with a good mix of theory and data. Anyone interested in either sexual selection or primates will find this volume useful, and it should be required reading for everyone interested in both topics." The Quarterly Review, Thore Bergman, Biology, University of Pennsylvania, Philadelphia, Pennsylvania

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