Introduction

The family Cheirogaleidae is arguably the most interesting group of primates alive today. Within this single clade, hypothesized to have originated approximately 25–30 Mya, we find the world's smallest living primate (genus Microcebus), one species that went “missing” for more than three decades (genus Allocebus), the only known obligate hibernator within the primates (genus Cheirogaleus), the only primate species that preys upon other members of its phylogenetic family (genus Mirza), and also, a taxonomic system that has exploded within the past two decades. This taxonomic explosion has been decidedly lopsided, however. Whereas the genus Allocebus has remained monotypic, containing the single species A. trichotis since its original description in 1875 (Günther 1875), the genus Microcebus (mouse lemurs) has gone from a two species system as recently as 1993 to one that that now contains more than 20 recognized species. This apparent skew in species-level diversity cries out for further exploration. Is it an artifact of organismal and geographic sampling bias, with certain species and ecosystems preferentially sampled, or is it based in biology, with some branches of the cheirogaleid tree (namely, the mouse lemurs) intrinsically more prone to evolutionary divergence? An exploration of these themes and questions is our goal in this chapter.

The first genus-level phylogeny of the cheirogaleid lemurs was published by Rumpler et al. (1994) and has remained virtually unchanged in the subsequent decades. Using karyotype data and restriction fragment analysis, the authors found strong support for the phylogeny illustrated in Figure 1.1. Notably, Rumpler and Albignac (1972) had long before discovered that the karyotype of Phaner (2n = 46) is quite distinct from that of the other four genera (2n = 66), leading those authors to propose a two-subfamily taxonomy of the Cheirogaleidae, the monotypic Phanerinae (including only the genus Phaner) and the Cheirogaleinae (comprising the four remaining genera). More recent molecular phylogenetic analyses have sampled more densely at the species level and have yielded fresh insights into interspecific relationships within the various genera, while leaving the “skeleton” of the phylogeny unchanged.

Introduction

The current geographic distribution of primates is confined largely to tropical and subtropical regions, where they have colonized a variety of habitats. The majority of primate taxa inhabit tropical forests with little annual fluctuation in environmental conditions. Some species, however, live in habitats characterized by pronounced seasonal fluctuations in climate and or resource availability. These primates tend to live at relatively high latitudes or altitudes, or both. Primates in such seasonal habitats provide an opportunity to identify behavioral and physiological adaptations that enable them to cope with fluctuating environmental conditions. Furthermore, it is interesting to ask whether and how schedules of growth and reproduction are adapted to maximize individual reproductive success under such seasonal conditions, because they may have to be traded off against maintenance requirements during the lean part of the year.

Primates living in seasonal environments exhibit a number of specific behavioral, ecological, and physiological adaptations. For example, during the climatically and or energetically most stressful time of year, they may reduce energy expenditure, e.g. by reducing overall activity, and many have scheduled periods of growth and infant weaning to coincide with seasons of relative abundance. Behavioral and physiological mechanisms of thermoregulation play especially important roles in maintaining homeostasis in seasonally stressed primates. These mechanisms are importantly influenced by circadian activity patterns because diurnal and nocturnal animals are exposed to fundamentally different constraints and options in this respect.

Anybody following the literature in behavioural and evolutionary biology has noticed that sexual selection studies have dominated the journals in this field more than any other single topic for the last decade or so. Why has sexual selection been such a sexy topic? First, this boom coincides with important methodological innovations. The invention of DNA-fingerprinting, for example, has led to the development of new tools for the measurement of reproductive success and the outcome of mate choice. Similarly, the development of new comparative methods has stimulated numerous tests of evolutionary hypotheses that address key predictions of sexual selection theory. Second, theoretical advances of the theory itself have been astounding. There are at least three areas where new ideas have generated disproportional interest and significant new insights. They concern sexual conflict, sperm competition and the study of various indicators of good genes in the context of mate choice.

Sexual conflict has been recognised as an arena of intense intersexual coevolution driven by the fundamental genetic conflict between males and females. Many adaptations of both sexes are now being recognised as a result of an intersexual arms race. Using many examples from the primate literature, Smuts and Smuts (1993) identified sexual coercion as a behavioural mechanism employed by males to resolve the conflict between the sexes to their advantage. Sexual coercion continues to be one area of investigation where primatologists make important general contributions, especially with respect to the multiple pervasive effects of the risk of infanticide on behaviour and physiology, but other aspects of sexual conflict have remained virtually unexplored in primates.

INTRODUCTION

Females of several species of Old World monkeys and apes exhibit enlarged perineal swellings that include the skin of the anogenital region and rump (see Fig. 5.1). Swellings are normally produced by adult females undergoing ovarian activity and they have stimulated evolutionary biologists since Darwin (1876) to think about their adaptive value and the evolutionary mechanisms responsible for their origin and maintenance. Given the association between sexual swellings and mating activity, it seems likely that some aspect of sexual selection is responsible for the evolution of this exaggerated trait. However, even today the functional significance of exaggerated swellings, as well as the processes responsible for their evolution, remain controversial (Dixson, 1983, 1998; Pagel, 1994, 1995; Radwan, 1995; Wiley & Poston, 1996; Nunn, 1999a; Stallmann & Froehlich, 2000; Domb & Pagel, 2001; Nunn et al., 2001; Domb & Pagel, 2002; Zinner et al., 2002; Snowdon, this volume).

In this chapter, we explore the role of sexual selection in the evolution of exaggerated sexual swellings. Because sexual swellings are associated with mating behaviour and competition among males for access to females, sexual selection has figured prominently among hypotheses for this exaggerated trait. Hypotheses have incorporated the two primary components of sexual selection, sometimes within the same explanation. For example, the best-male hypothesis (Clutton-Brock & Harvey, 1976) states that swellings stimulate male–male competition, improving the ability of females to identify and mate with the highest-quality males.

In recent years, our understanding of the theoretical basis for sexual selection has increased.

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.

INTRODUCTION

Post-copulatory sexual selection comprises two processes: sperm competition and cryptic female choice (Birkhead & Møller, 1998). Sperm competition is the inevitable consequence of females copulating with and being inseminated by more than one male during a single reproductive cycle: the sperm of different males compete to fertilise the female's ova. Cryptic female choice can similarly occur only when females are inseminated by more than one male, but – so far, at least – it does not appear to be inevitable. The evolutionary significance of these two processes has become apparent only since the 1970s; before that it was assumed that females in many taxa typically copulated with only a single male during any reproductive cycle. Recognition of the ubiquity of these post-copulatory mechanisms of sexual selection has created new opportunities to study the dynamic interactions between the sexes, which are being fuelled by the fundamental conflict between males and females over the maximisation of their reproductive success at yet additional frontiers (e.g. Johnstone & Keller, 2000). Furthermore, consideration of post-copulatory mechanisms can inform analyses and interpretation of pre-copulatory reproductive strategies of both sexes (Parker, 1970, 1984). In this chapter, we review mechanisms and consequences of post-copulatory sexual selection in two groups of animals for which some of the most detailed behavioural data exist, and which differ fundamentally in reproductive physiology and their modal social and mating systems: birds and primates.

INTRODUCTION

Empathy probably guides most hypotheses about social Behaviour (Hrdy, 1986), or at least the amount of attention given to particular problems. For several decades now, behavioural biologists have been fascinated with sexual monogamy, or its absence, in both birds and mammals. However, the question of the evolution of social monogamy has also been a topic of sustained interest (e.g., Kleiman, 1977; Barlow, 1988; Komers & Brotherton, 1997; Fuentes, 2000). Unfortunately, despite this interest, a comprehensive model of the evolution of social monogamy, at least among mammals, has so far eluded us, quite possibly because there are both multiple pathways leading up to it, and multiple benefits favouring its maintenance in different lineages. There is, accordingly, little hope for a simple unitary model for the evolution of social monogamy.

In this chapter, we examine the evolution of social monogamy in one mammalian lineage: primates. Primates are a very suitable group for a study of the evolution of social monogamy. Pairs are remarkably common among them (Kleiman, 1977; Müller & Thalmann, 2000), and range from dispersed to associated, and from variable to uniform. In the following paragraphs we outline our approach to this question.

Our focus is on the evolution of pairs as a social system, i.e., the associations and social interactions among individual animals. The social system encompasses the social organization (its size, composition, and spatiotemporal cohesion), the mating system, and social structure (patterning of social interactions and relationships among members of the social unit) (Kappeler & van Schaik, 2002).

INTRODUCTION

Current socio-ecological theory assumes that social systems are the result of adaptations, and thus subject to evolutionary modification by selection (Crook & Gartlan, 1966; Emlen & Oring, 1977; Wrangham, 1987; Ims, 1988). Social systems are not direct targets of selection, however, because they represent the outcome of individual behavioral interactions and strategies (Hinde, 1976). The underlying behavior of individuals towards conspecifics is thought to be largely shaped by ecological factors, such as the distribution of risks and resources in the environment (Wrangham, 1980; van Schaik & van Hooff, 1983; Terborgh & Janson, 1986; van Schaik, 1989), as well as the resulting social boundary conditions (Janson, 1986; van Schaik, 1996). Behavior constitutes, therefore, the crucial interface between individuals and their environment (Terborgh, 1992). Individuals decide at the behavioral level whether they lead a solitary life or form permanent groups, and which group size and composition is optimal under a given set of ecological conditions. An animal's behavioral decisions at this level are therefore a target of selection where convergences among distantly related taxa as a result of similar selection pressures can be expected.

Among mammals, primates exhibit an extraordinary level of diversity in social systems (Smuts et al., 1987), rivaled perhaps only by that found among marsupials and carnivores (Gittleman, 1989; Strahan, 1995). They display all fundamental types of mammalian grouping patterns (Clutton-Brock, 1989) and show a variety of bonding patterns, especially in gregarious taxa (van Schaik, 1989). Thus, the evolution of convergences is not principally constrained by primate-specific traits.

For the purpose of an analysis of convergence in social systems, the living primates can be divided into four major groups with potentially important variation in taxonomic diversity.