Selection in Relation to Sex in Primates

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This chapter summarizes the main concepts of modern sexual selection theory and examines the evidence for the operation of sexual selection in primates. Traditional classifications of mating systems suffer from the problem of not considering reproductive strategies of both males and females equally and are biased by a strong male perspective. Modern sexual selection theory encompasses the conflicting interests of males and females and the evolutionary consequences of all aspects of competition for mates. The chapter focuses on causes, mechanisms, and consequences of sexual selection. In addition, the chapter accounts for the relevance of primates to sexual selection and relevance of sexual selection to primates; and summarizes a great variety of mating systems that exist in primates. The reproductive success of a male primate is limited by the number of females he can fertilize. The main scenarios from the males' perspective and females' perspective of sexual strategies are outlined. Male primates compete for access to females and their gametes; however, they also show mate choice and parental care for infants and this improves their reproductive success. However, female choice for male quality may be less important than female counter-strategies against male coercion, infanticide in particular. Female primate behavior tends to increase the number of males mated with. Female reproductive strategies can act in tandem with male strategies. However, female strategies may also be in opposition to male-male competition. By using a comparative and theory-oriented approach to examine and integrate recent developments in primate sexual selection studies, the chapter draws some general conclusions about sexual selection in primates, identifies reasons why primates were neglected in particular areas of sexual selection research, and stimulates future research on all aspects of sexual selection in primates.

Introduction

Essentially neglected for 100 years after the publication of “The Descent of Man and Selection in Relation to Sex” (Darwin, 1871), sexual selection is now one of the most active fields in evolutionary biology, with a vast literature devoted to empirical and theoretical research (Andersson, 1994). However, although Darwin addressed the question of sexual dimorphism, secondary sexual characteristics, and weapons in primates, and later published a paper entitled “Sexual Selection in Relation to Monkeys” (Darwin 1871, Darwin 1876), studies of non-human primates continue to be under-represented in this field. This is especially true for investigations of the diversity of sexually selected behavioral strategies and tactics. Whereas primatologists have described and analyzed anatomical differences between the sexes in great detail (see Dixson, 1998a for a recent review), other targets of sexual selection remain relatively poorly studied, especially in comparison with other taxa (e.g., insects, birds, amphibia, and fish; Johnstone 1995, Johnstone 2000, Andersson 1996, Ryan 1998, Paul 2002). Moreover, although several reviews have covered aspects of sexual selection in primates (Hrdy 1987, Smuts 1987, Small 1989, Keddy-Hector 1992, Smuts 1993, van Schaik 1999, van Schaik 2000a, Paul 2002), the existing body of relevant primate data has largely remained un-synthesized in recent years. Some behavioral aspects of sexual selection are perhaps better studied in human primates (Thornhill 1996, Buss 1994, Buss 1999), but evolutionary psychology, the discipline mostly concerned with evolutionary studies of human sexual behavior, is largely isolated from mainstream primatology.

We aim to begin filling these gaps by reviewing research on the causes and consequences of reproductive competition, mate selection, and inter-sexual conflict in primates and teasing apart specific adaptations and tactics from the perspective of both sexes. We begin our review with a brief summary of the main concepts of sexual selection theory. We then examine the relevance of sexual selection to primates and the relevance of primate studies to studies of sexual selection. Next, by using a comparative and theory-oriented approach to examine the reproductive strategies of male and female primates, we hope to draw some general conclusions about sexual selection in primates and to stimulate future research on all aspects of sexual selection in primates.

Section snippets

Causes, Mechanisms, and Consequences of Sexual Selection

Sexual selection arises from “the advantages that certain individuals have over others of the same sex and species, in exclusive relation to reproduction” (Darwin, 1871). Darwin developed the theory of sexual selection to explain the evolution of conspicuous male traits such as bright colors, long tails, and antlers. Such traits pose a risk to a male's survival; however, Darwin suggested that this cost was outweighed by an advantage in fighting other males or attracting females, and a higher

Relevance of Primates to Sexual Selection

Given the extensive data available concerning sexual selection in other taxa, why do we need a review like this chapter or entire books (Kappeler 2003, Jones 2003) on sexual selection in primates? Primates are not obvious candidates for the experimental approach required to test sexual selection hypotheses. Ethical issues and their slow life-history limit the possibilities for study (Janson 2000, Stearns 2003). Long-term studies are essential, and small sample sizes make it difficult to obtain

Relevance of Sexual Selection to Primates

What evidence do we have for the operation of sexual selection in primates? As in other mammals, the costs of internal fertilization, gestation, and lactation are especially high for female primates (Altmann 1980, Oftedal 1984, Gittleman 1987, Clutton-Brock 1989, Clutton-Brock 1989, Lee 1991, Lee 1996). As a result, some form of polygyny is expected in most species (Clutton-Brock 1989, Dunbar 1995). The great variety of mating systems that exist in primates has been reviewed elsewhere (

The Male Perspective: The “Copulatory Imperative”

The reproductive success of a male primate is limited by the number of females he can fertilize, selecting for a “copulatory imperative” (Ghiselin, 1974). The primary type and intensity of competition between males is determined by the monopolizability of females, which in turn is determined by their spatial distribution, the absolute number of females in group-living species, and the degree of synchrony of their receptive periods (Mitani 1996a, Mitani 1996b, Nunn 1999b, Kappeler 2000a). In the

The Female Perspective: Biasing and Confusing Paternity

Because of their relatively slow life-histories, female primates invest heavily in a limited number of offspring. Consequently, to maximize their reproductive success, females are expected to benefit from conceiving with the best male, gaining good genes and (in some species) various male services. However, while females may want to bias paternity in favor of a particular male with a preferred phenotype or genotype, or both, there is an emerging consensus that female primates mate polyandrously

Conflict Between the Sexes

Male and female reproductive strategies are intimately linked in primates. They are also inherently in conflict as the interests of males and female diverge. Sexual conflict can be seen as an arms race where the evolution of strategies in one sex leads to counter-strategies from the other, which in turn lead to counter-counter-strategies in the first (Parker, 1979; Clutton-Brock and Parker, 1995). This intraspecific red queen phenomenon is well illustrated by the evolution of male infanticide

Conclusions and Future Directions

Studies of sexual selection in primates have long been dominated by examination of male contest competition over copulatory access to females, an emphasis that has tended to eclipse the wide diversity of sexually selected strategies and tactics that occur in both sexes of this order. Underlying this diversity is the extent to which males are able to monopolize females, which is dependent on the dispersal and grouping patterns of female primates, in turn driven by the distribution, abundance,

Summary

The causes, mechanisms, and consequences of mate choice and competition for mates are currently among the most intensively discussed topics in evolutionary biology. However, primates are notably under-represented in this debate. In this review, we briefly summarize the main concepts of modern sexual selection theory and examine the evidence for the operation of sexual selection in primates. Traditional classifications of mating systems suffer from the problem of not considering reproductive

Acknowledgements

We thank Carel van Schaik, Claudia Fichtel, and Alan Dixson for numerous stimulating discussions of sexual selection in primates, Marc Naguib for the invitation to contribute this paper, Eckhard Heymann for pointing out some callitrichid references, and Charles Snowdon, Marc Naguib, Peter Slater, and an anonymous reviewer for their constructive comments on an earlier version of this manuscript.

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