INTRODUCTION

Animal societies derive from the social relationships that exist among its members (Hinde, 1983). Behavioural ecologists have traditionally focused on the core relationships defining a mating system as a means toward understanding the role of ecology in the evolution of sociality (e.g. Jarman, 1974; Bradbury & Vehrencamp, 1977). Typically, these core relationships emerge from the operation of both natural and sexual selection and how they differently affect the behaviour of females and males (Rubenstein, 1986; van Schaik, 1989). However, emphasis on mating systems has tended to marginalise the importance to social evolution of interactions and relationships that extend beyond the basic breeding unit. This is even true for the small subset of species with multi-level societies, where breeding units and other social subgroups are themselves organised into more complex social groups within a population. By examining how natural and sexual selection operate within multi-level societies, however, a more complete understanding of the function and evolution of sociality emerges than would by investigating the dynamics of mating systems alone (e.g. Dunbar, 1988).

Although the societies of many primate species are multi-levelled, the relative simplicity of societies of plains zebras (Equus burchelli) where only two tiers exist – the core breeding units and the herds they often comprise – can provide insights into the rules that give form to multi-level societies. In this chapter we begin by highlighting the environmental and sociosexual factors that shape zebra mating systems and herd dynamics.

INTRODUCTION

Sexual dimorphism in anthropoid primates is commonly viewed as a product of sexual selection (Clutton-Brock et al., 1977; Harvey et al., 1978; Gaulin & Sailer, 1984; Clutton-Brock, 1985; Milton, 1985; Rodman & Mitani, 1987; Kay et al., 1988; Ely & Kurland, 1989; Greenfield, 1992a, b; Plavcan & van Schaik, 1992, 1994, 1997; Ford, 1994; Martin et al., 1994; Mitani et al., 1996b; Lindenfors & Tullberg, 1998; Plavcan, 1999, 2001; Barton, 2000; Lindenfors, 2002a; Mitani et al., 2002). Yet dimorphism in anthropoids is highly variable, and is expressed not as a single character, but rather to different degrees in different traits. This naturally raises the question of whether this variation is owing to variation in the strength of sexual selection, phylogenetic effects or the action of other selective factors on the dimorphic characters. While numerous papers have examined the causes and correlates of dimorphism in anthropoids, the relative contribution of sexual selection and other factors to variation in dimorphism remains unclear.

Part of this problem lies in the way that both dimorphism and sexual selection are measured. Both of these variables are estimated with error, not only in a simple statistical sense, but also in the assumptions that are used to justify measures as appropriate for analysis. Some of these biases are obvious, while others are not. Thus, if dimorphism is poorly correlated with an estimate of sexual selection, we can legitimately ask whether dimorphism is affected by factors other than sexual selection, or whether our measures fail to capture variation in either sexual selection or the targets of sexual selection.

The past 30 years have seen a sea change in the study of sexual selection in primates. With few exceptions–such as Goodall's work on chimpanzees and DeVore's on baboons–the earlier work usually consisted only of descriptive field studies giving such crude social and ecological parameters as group size, age and sex composition, preferred food species, and whether reproduction was annual or not. The literature was often dull and justified only by the phylogenetic closeness of the species studied to ourselves.

Now we have studies of male paternity using DNA analysis, experimental analyses of the attractiveness of female swellings, comparative work on sexual dimorphism in size across various primates characterised for intensity of sexual selection, comparative studies of the primary sex ratio in primates and studies of sperm competition as well. On the theoretical side, we have passed well beyond the initial model linking sex differences in variance in reproductive success to sex differences in parental investment. We now have theory regarding reproductive skew, sex-antagonistic genes and sex-antagonistic selection, female choice biased toward daughters, and extra-pair and sperm competition as major variables in sexual selection. This is the new world that the present volume introduces us to. What follows is one person's selective summary, meant to highlight the key findings. Much is left out, of course, and there are certainly some important results that I have overlooked.

Knowledge of common morphological terms is necessary when carrying out an assessment of the face. Figs. 4.1 to 4.5 illustrate these facial surface anatomical terms. There has been a long history of research into quantifying the relationship between the skeletal structure of the skull and the overlying soft tissues of the face, with the express purpose of facilitating facial reconstruction. Gerasimov (1971) was convinced that there was a clear correlation between the relief of the skull and the surface of the soft stratum. He claimed that this could be illustrated by the asymmetry of the skull, which is also exhibited in the asymmetry of the face. He clarified this with a photographic study of faces to create totally right-sided and left-sided faces from an original face. He took a frontal-view photograph of a subject and split the photograph on a line that dissected the glabella and the philtrum. He then created two faces by mirror imaging each side and attaching it to its mirror image: one made up of two right sides and one of two left sides. He found for every subject two distinct faces were created: a ‘fine’ face and a ‘rough’ face. He suggested that asymmetry is a basic element of individuality and that since the asymmetry is natural, any reconstruction of the soft tissues will define the character of this asymmetry and secure similarity to the actual face (see Fig. 4.6).

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.

No two faces are alike, not even those of identical twins. Each face is unique. The human face is one of the most important social tools. An enormous variety of communication signals are produced using the face and it governs the expression of emotion, interest, desire and attention. We use our faces to attract, repel, scare, soothe and entertain. The face suggests details such as age, gender, culture, health and ethnic group. It is usually the first part of the body that we notice and the only part that we address. We are each capable of perceiving the smallest variation between faces and it is this ability that allows us to carry out personal recognition and identification. As adults we recognise and differentiate hundreds of faces of our family, friends, colleagues, famous people etc. This is illustrated by our ability to distinguish eventually the faces of identical twins (see Fig. 1.1). Even though the faces of identical twins are remarkably similar and they share the same genetic profile, their faces are in fact slightly different and people who know identical twins very well can distinguish them from one another.

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.

Facial reconstruction is a process whereby the face of an individual is built onto the skull for the purpose of identification. The theory behind facial reconstruction is that in the same way that we all have unique faces, we all have unique skulls, and it is the small variations in the shape, form and proportions of the skull that lead to significant variations in our faces. When I first became involved in facial anthropology, I too had a great deal of difficulty believing that the amount of variation seen in the world's population of faces could also be exhibited in skulls. Even though we are all experts at facial recognition and identification, due to our innate ability to distinguish one face from another, we find it difficult to believe that the skull can provide a detailed map for the face. This must be, in part, due to our inability to distinguish one skull from another in the same way that we can distinguish one face from another. Uninitiated observers will not be able to demonstrate proportional and feature variation between skulls with ease. Since all skulls appear similar in shape and proportions to the inexperienced eye, it is assumed that the information provided by one skull must be virtually the same as that provided by another skull. However, the practised and experienced observer can demonstrate unlimited variation in shape, size, proportion and detail between skulls. I am now convinced: each skull is as individual as each face.

Introduction

Sexual selection is an important evolutionary force in mammalian species because of one simple fact – males are a glut on the market. From the females' point of view, there are more males than needed to meet their reproductive requirements. And from the males' point of view, there are not nearly enough females to go around to satisfy their reproductive potential. The relative abundance of males generates strong intrasexual competition among them.

The goals of this chapter are to explore the selective factors that influence the evolution of birth sex ratios, and to weigh the empirical evidence that primate females facultatively manipulate birth sex ratios to enhance their own fitness. We will begin by briefly enumerating some of the ways in which adult sex ratios influence the evolution of male and female life histories, morphology and reproductive strategies in primate groups. Then, we will explain how natural selection shapes the evolution of birth sex ratios, and consider the empirical evidence for adaptive manipulation of birth sex ratios in primate groups.

The reconstruction of children's faces has always been considered more problematic than adult facial reconstruction. There are many difficulties associated with juvenile remains, including more inaccurate sex and racial origin determination, the more emotive and sensitive nature of an investigation into the death of an unknown child, and the less defined skeletal details associated with underdeveloped skulls. Historically this field has not been separated from adult facial reconstruction, although the differences between adult and juvenile skulls are enormous. This may be a reflection of the small numbers of juvenile reconstructions produced relative to adult reconstructions, and it may be due to the paucity of juvenile research. Until 1963 there were no published juvenile facial tissue depth measurements, and anthropometrical studies have concentrated on facial growth patterns rather than facial standards. However, there has been a great deal of anthropological research into age and sex determination, and the growth of juvenile skulls.

Juvenile age determination

With the remains of preadolescent children there are three age estimates that can be used: the numbers of emerged teeth, calcification of the permanent mandibular first molar, and the schedule of calcification of the dentition as a whole. A consistent and predictable sequence has been determined for the formation, eruption and loss of primary dentition, and its replacement with secondary dentition. The rates have been calculated for children from many populations (Iscan & Helmer, 1993). All the deciduous dentition and the first permanent molars have begun to mineralise at birth.

The accuracy of the facial reconstruction method has been extensively debated over the years. One of the points of contention seems to be disagreement over who should carry out the facial reconstruction work itself. Should it be the artist, who uses more intuitive sculptural skills; or the scientist, who follows a preconceived method? Often scientists employed artists to carry out the sculptural work under their scientific supervision. Such work, however, did not escape criticism. As early as 1900, Merkel was assisted by Eichler, a sculptor, and together they carried out the reconstruction of an ancient Saxon. Eichler departed widely from the prescribed data and followed his own deductions concerning the development of muscles, as suggested by the lines and features of the skull. The aesthetically pleasing result could not be tested and therefore the departure from the data could not be defended. Alternatively, there have been many facial reconstructions that have been carried out with a very methodical and scientifically pure technique that have resulted in wooden, lifeless and clumsily sculpted faces that are crying out for the aesthetic and observed input of an artist. The contention is based around whether or not aesthetic appeal is a necessity when recognition or similarity to an individual is the only requirement. One theory proposed by George (1993) suggested that the face shape and proportions are the most important factors, and any added detail, which makes the face human, may detract from the features and overall impression of the face.

INTRODUCTION

Studies of sexual selection in primates or other animals tend to focus on outcomes – sexual dimorphism, differential mating and reproductive success for adult males and females. However, adult sex differences represent the end-points of complex and interrelated developmental processes, and arise from differences in behaviour and physiology between males and females. In most vertebrates, including primates, the sexes are nearly identical in size and shape during early development, and adult differences are thus the product of divergent growth strategies (Badyaev, 2002). Sex differences in growth and development arise as a result of the different roles played by the two sexes in reproduction and the corresponding determinants of reproductive success for males and females, which are intricately linked to social organisation and mating system (Kappeler & van Schaik, 2002). Evolution shapes processes throughout the lifecycle, and the mechanisms for partitioning resources among growth, reproduction and survival are, to a large part, established during development, while consequences may not be observed until the end of the lifespan. A developmental perspective is therefore fundamental to studies of the action of sexual selection (see also Pereira & Leigh, 2003).

For mammals in general, and primates in particular, past work on sexual selection and development has concentrated on the influence of growth on sexual dimorphism (e.g. ungulates: Jarman, 1983; Georgiadis, 1985; Clutton-Brock et al., 1992; seals: Trillmich, 1996; primates: Leigh, 1995; Pereira & Leigh, 2003) or growth and life-history traits such as rates of reproduction (e.g. Gordon, 1989; Pontier et al. , 1989; Lee & 2003).