The next task is to marshal the evidence, largely from naturalistic studies of wild chimpanzee groups, of how the egalitarian mutual dependence system operates within chimpanzee society. Anthropological understandings regarding the workings of human foraging societies are used to structure this discussion.

An egalitarian society is one in which all members are considered to be of equal intrinsic worth and are entitled to equal access to, and share of, the goods, rights and privileges of their society. Within the structure of such societies, individuals have a high degree of autonomy. Hence power relationships do not exist in societies that are egalitarian in form, nor do inequalities of possessions, prestige and status. The immediate-return foraging system is intensely egalitarian. Indeed, Woodburn (1982:432) emphasizes very strongly that no other system found among humans ‘permits so great an emphasis on equality.’

People who live as foragers are highly ‘individualized;’ they are not equal in the sense of being the same as each other (Service 1966:83). The unspecialized nature of foraging societies means that all adults participate much more fully in every aspect of the society than do members of more complex social systems. Members are accepted as they are, for what they are, in their natural variety, Service emphasizes.

Similarities in overt behavioral manifestations of humans and chimpanzees do not necessarily imply that the phenomenon derives from the same underlying mechanisms. However, the following analysis proceeds on the assumption that, if certain positive behaviors and relationships are intrinsic to foraging humans, they are equally imperative to chimpanzees who follow the same foraging system.

General anthropological understandings

This part of the book is a brief summary of anthropological understandings regarding the social behavior and organization of foragers, gatherer–hunters, who lived by the most simple full form of human organization, the immediate-return system, at the time they were studied. More detailed data from the field studies of these groups are inserted throughout the text, wherever they illuminate aspects of the social behavior and organization of chimpanzees.

Anthropologists consider the ancient foraging (gathering–hunting) way of life as the most successful and longitudinal adaptation humans have ever achieved. Indeed, until the advent of the age of agriculture, approximately 10,000 years ago, all peoples everywhere on earth lived by a foraging mode (Murdock 1968). Today, foraging societies have all but vanished. There remain only a few, small, scattered groups, in environments climatically so inhospitable as not to be much desired by agriculturists or industrialists, and even these areas are being preempted rapidly (see figure 4).

There is a general agreement among anthropologists that all foraging peoples live in small groups, and follow a nomadic pattern known as fission and fusion. Another point on which there was, until recently, complete agreement is that, whatever the foraging construct is, it ‘is not a corporation of persons who are bound together by the necessity of maintaining property’ (Lee and DeVore 1968:8).

There is considerable diversity among foraging models. Some anthropologists suggest lineage models, local groups which are organized around central members of a single lineage, and some who affiliate through marriage alliances.

Foraging theory: when, and when not, to defend territory

The degree of exclusive use of a territory varies widely among animal species, from almost total control to sharing significant portions of the area and its resources with outsiders (Myers, Connors and Pitelka 1981). Animals do not usually defend a territory, excluding others, unless the benefits of so doing exceed the costs. In this section, the behavior of the wild chimpanzees, and the provisioned Gombe and Mahale groups, will be considered in terms of foraging theory (costs and net benefits), frustration, and competition theories.

Customarily, the term foraging is used to refer to behavior associated with searching for, obtaining and consuming wild foods. Foraging strategy refers to the way in which foraging animals achieve a particular goal. Animals that adopt the most successful strategy forage ‘optimally’ and are favored by natural selection (Krebs 1981). The goal and criterion of success might be to obtain as much food as possible or to minimize the time spent foraging each day in order to ‘bank’ time and energy for other activities, such as seeking mates, reproduction, resting, grooming, antipredator behavior and so on. Foraging strategy is often viewed in terms of the tactical ‘decisions’ that animals make, as to which food items to seek and when, where and how to do so. As Krebs (1981) puts it, in terms of fitness the foremost question is: what tactics should an animal adopt that will be most effective toward reaching its goal?

Every so often there appears a work of synthesis which is so original and creative that it clarifies and systematizes a whole field of observation or knowledge that had hitherto been adventitious and chaotic. Such were the works of Rudolf Virchow, whose Cellular-Pathologie (1858) not only founded the science of pathology, but constituted the fundamental contribution to the rise of modern medicine, as was also Claude Bernard's Introduction à l'étude de la Médecine Experimentale (1865), which put physiology on a firm scientific basis as well as the founding of regulatory biology and its relation to human health. What these books, each in its own way, did for the growth and development of medicine and human health, I am convinced that Mrs Power's admirable book will do for the growth and development of our better understanding of the dynamics of social life not only among chimpanzees, but for all primates, including humans. For what the author has done is to make a microscopic examination of the fieldwork of numerous independent investigators who have studied chimpanzees under natural or artificial conditions. With great acumen she has seen that even under natural conditions, the conditions may not be as ‘natural’ as most investigators and their interpreters and readers may have thought, and that various factors under such conditions have led to a variety of inferences which have in fact been erroneous. Mrs Power's analysis of these factors for the first time really makes it possible to train future students of animal behavior, and more particularly of primate behavior, including humans, in the delicate methodology of fieldwork.

Traditionally, the final section of a scientific monograph is the one in which the author goes beyond interpreting the data to speculate on a range of implications that she or he thinks is recognizable in the data. The following proposals start from a basis of evidence and theory, but go beyond into the realm of logical possibility. The reason for doing so is to stimulate further discussion and to suggest possible new approaches for further research.

The adaptive value of aggressive behavior: a possibility

The theme of this study is that a system of mutual dependence involving positive behavior, egalitarianism, individual autonomy, and the noninterference form of mutualism (NIM) is the adapted mode of organization of chimpanzees under normal environmental circumstances. It is also argued that this benign, loosely structured form of social order of chimpanzees can change rapidly to encompass negative, society-destroying behavior and a rigidly structured dominance hierarchy.

It is now known that equal potentials for aggressive or peaceful responses are both part of the genetic constitution of all animals; there is no genetic coding that inevitably results in either aggression or peacefulness, only a set of genetic attributes ultimately for self-defense ‘that can be expressed as aggressiveness under particular sets of conditions’ (Dubos 1973:86). It follows that also part of this set of genetic attributes are those that act to maintain peace, under differing conditions. The ultimate goal of the entire set is survivial of the species.

The principles and patterns, behaviors, interactions and relationships that structure a mutual dependence system require more explanation and substantiation than they have received to this point. Accordingly, in this part of the book, evidence from naturalistic studies of chimpanzees and from field studies of the six human groups who, when studied, lived by an immediate-return foraging system, are used to develop further the model of the basic mutual dependence system as it is among chimpanzees.

In reading the rest of this volume, three earlier mentioned points must be kept in mind. First, it is now generally agreed that chimpanzees share the same range of emotions, and similar mental processes, with humans, though they are technically greatly inferior.

Second, the mutual dependence system as outlined is a model, and a preliminary one at that: a first attempt to understand the adapted social structure of chimpanzees from a new perspective. In reality, chimpanzee social groups will vary from the model. Chimpanzee social behavior, like that of humans, is extremely plastic. Differing ecological conditions will affect local behavior and local traditions. For example, Sugiyama and Koman (1979) found that in the wild group that they studied for 6 months in the vicinity of Bossou, Guinea, one particular male leader, ‘Bafu’, made repeated attempts to keep the entire Bossou group together, going back and forth making barking calls as they traveled, apparently trying to keep together the forerunners and those lagging. This is leader behaviour quite different from that of the model.

Introduction

Despite more than 30 years of study of free-living chimpanzees in their African habitat, there is no firm agreement as to the social organization of this species. Both ‘naturalistic’ (unobtrusive) and ‘provisioning’ (artificially feeding) methods of field study have been used, with sharply differing results. Independent field researchers, using various naturalistic methods report – quite separately but with striking unanimity – peaceful, open groups of nonaggressive chimpanzees without signs of any dominance hierarchy, enforced territoriality or single leaders.

At the long-established, permanent centers for the study of free chimpanzees in Gombe and Mahale National Parks, Tanzania, artificial feeding methods have been used. Researchers at both centers – also quite separately – report many strongly similar aspects of behavior and social organization of the provisioned apes that are opposite to reports from naturalistic studies. The artificially fed Gombe and Mahale apes are extremely aggressive, dominance seeking, directly competitive and fiercely territorial.

Habituating the apes to the presence of humans through provisioning facilitates excellent, lengthy observation opportunities, an intimate knowledge of the chimpanzees as interacting individuals, and a large pool of data. Naturalistic studies do not have these advantages. Consequently, not only are our current understandings of chimpanzee social behavior and organization based very largely on the Gombe and Mahale studies but also there is a tendency to assume that the noncontinuous naturalistic studies yield few or no data on the social behavior and organization of chimpanzees. Washburn (1980:258) expresses the view of many when he asserts that ‘the beginning of reliable studies’ on the natural behavior of chimpanzees may be marked by ‘Jane Goodall's (1968) long-continued investigations’ (my emphasis).

In this section of the book the behavior and social organization of wild chimpanzees, as reported by those using naturalistic methods of field study, are compared with the same phenomena as they are reported among the Gombe and Mahale chimpanzees. The reader is warned that the way the evidence of negative social change is gathered together and presented here gives a very one-sided picture of the Gombe situation. Positive (friendly, supportive) interactions have not ceased. (They may even have increased as a result of the need for greater reassurance and consolation). There was not unremitting turmoil, but sporadic eruptions, with intervals of peaceful behavior. This comparison is begun by reference to an early insight of Kortlandt, as it structures the adapted egalitarian system of chimpanzees.

Kortlandt's hypothesis

Kortlandt's startling hypothesis is based on his 1960 observations of wild chimpanzee groups, made largely when they came to feed on pawpaw fruit growing on an abandoned edge of a plantation at Bossou, New Guinea. It was to his own very great surprise, Kortlandt (1962:132) comments, that he realized that ‘the chief social distinction’ in wild chimpanzee groups ‘is between childless and childrearing adults rather than between males and females.’ While this is an enormously important insight, it was met with a resounding silence by the academic community, presumably because this vital understanding does not fit within the then-unchallenged dominance paradigm.

Most of the early observers categorized chimpanzee groups into four types of subgroup, usually mixed groups (males, females and young) mother groups (females and young), all male, and lone male groups (Goodall 1965a; Reynolds and Reynolds 1965; Sugiyama 1972; Ghiglieri 1984).

In the absence of adult conspecifics, newly-hatched chicks will approach a wide range of bright or moving objects. After a period of exposure to such an object they form a social attachment to it. When they are close to the object the chicks emit soft calls, and if it moves away they will follow it. If subsequently exposed to a new object the chicks will run away emitting distress calls. From these observations it may be inferred that chicks learn about some of the visual characteristics of the first object to which they are exposed. This process is referred to as filial imprinting, and has been studied most intensively in precocial birds such as domestic chicks, ducklings, and goslings (Spalding, 1873; Heinroth, 1911; Lorenz, 1935, 1937; Bateson, 1966). Similar processes may also occur in mammals, but evidence for this is harder to obtain due to their comparative lack of mobility shortly after birth. This chapter will concentrate on the neural and behavioural analysis of filial imprinting in the domestic chick, a species which readily imprints on to a wide range of visual objects.

Imprinting can be reliably reproduced in the laboratory in the following way. Chicks are dark-reared until being exposed to a conspicuous object such as a rotating, illuminated red box, for a period of time, normally several hours. From between two hours to several days later, chicks are given a choice between the object to which they were exposed and a novel object. The extent to which the chick approaches each of the two objects is compared and a preference score calculated.

Since Hamilton's oft-cited prediction regarding the unequal distribution of behaviour among genetically related (kin) and unrelated conspecifics (nonkin) (Hamilton, 1964), the phenomenon of kin recognition has been repeatedly documented among a diverse assortment of animal species (Colgan, 1983; Fletcher & Michener, 1987; this volume). As in other maturing fields of inquiry, attention has shifted from description and documentation of recognition systems to a search for the ‘mechanisms’ supporting kin recognition. This search has produced a canonical list that typically comprises four classes of mechanisms: (1) spatial distribution, (2) familiarity, (3) phenotype matching, and (4) recognition alleles. These hypotheses have been offered as explanations of the dynamic control of recognition, but generally contain reference to the developmental means by which recognition cues come to exert their effects (Hepper, 1986; Fletcher, 1987). Thus, the ontogeny of kin recognition has, explicitly or implicitly, become one of the central foci of debate in this relatively young field.

In nature, among species bearing multiple offspring in a single clutch or litter (including most mammals), a necessary concomitant to reproduction is the association of mother with offspring and of littermate siblings with one another. Therefore, some degree of prior experience with related conspecifics is virtually inevitable. A common experimental design intended to isolate effects of prior experience involves cross-fostering of some offspring to unrelated litters shortly after birth. However, even if performed within moments of birth, cross-fostering cannot separate genetic factors from experiences of siblings that share the same prenatal environment (cf. Ressler, 1962).

Co-operation can be defined as any mutually beneficial interaction between two or more individuals. By this standard definition, many, probably most, birds and mammals exhibit co-operation in one or more contexts. Cooperation can range from a simple apparently incidental group effect, such as the simultaneous mobbing of an owl by individuals of two species of songbirds, to complex mutual dependence, such as the rotating sentinel systems of some group-living animals (e.g. McGowan, 1987). Virtually all researchers recognize co-operation when they see it and its widespread occurrence is not a matter of controversy (Axelrod & Hamilton, 1981).

The phenomenon of co-operative behaviour is a fascinating one, for several reasons. First, co-operation is a universal human trait and the vast majority of interactions among individual humans are co-operative to a greater or lesser degree. Thus, it is easy for people to empathize with the cooperative behaviours they observe in animals.

Second, highly developed intra-group co-operation is often seen in species also characterized by high levels of inter-group competition. Our own species is the prime example of this relationship. Killing of conspecifics may be viewed as indicative of extreme intraspecific competition, and human warfare, the searching out and killing of male chimpanzees (Pan troglodytes) by groups of males (Goodall, 1986), the expulsion or killing of male prideholding lions, (Panthera leo) by invading coalitions of males (e.g. Packer & Pusey, 1982) and the running down and killing of a lone wolf (Canis lupis) by a pack (Mech, 1970), illustrate this relationship between co-operation and competition.

Introduction

Kinship underlies many facets of vertebrate sociality. Yet vertebrate societies rarely consist exclusively of kin. Typically, individuals interact both with kin and non-kin in numerous and often unpredictable contexts. Clear advantages accrue to those individuals that discriminate behaviourally among conspecifics based on their genetic relatedness. The ability to recognize relatives permits individuals (1) to favour their kin, thereby enhancing their inclusive fitness (Hamilton, 1964; Grafen, 1985), and (2) to avoid incest or even to choose an optimally related mate (Shields, 1982; Bateson, 1983), potentially increasing their own reproductive success. Possible benefits of kin discrimination are easily enumerated in birds and mammals (reviewed in Waldman, 1988), so their kin recognition abilities (e.g. Holmes & Sherman, 1982; Hepper, 1983; Beecher, 1988) should not be surprising. Less is known about the social life of fishes, amphibians, and reptiles, but they also may recognize their kin. Some fishes and larval amphibians, for example, recognize their siblings and preferentially school with them (e.g. Waldman, 1982b; O'Hara & Blaustein, 1985; Quinn & Busack, 1985; Van Havre & FitzGerald, 1988; Olsen, 1989). Similarly, iguana hatchlings associate in social groups with their siblings rather than with unrelated individuals (Werner et ah, 1987).

Mechanisms of kin recognition have been more thoroughly examined in amphibians than in other vertebrates. Indeed, information on the ontogeny and sensory bases of kin recognition comparable in detail to that known about social insects (e.g. Gamboa et aL, 1986; Hölldobler & Carlin, 1987; Michener & Smith, 1987) and some invertebrates (Linsenmair, 1987) is currently available only for larval amphibians. Warm-blooded vertebrates can be unwieldy as subjects for ontogenetic studies in the laboratory.

In practice, although not in theory, the subject of this chapter – the genetic determination of body scents that distinguish one individual from another individual of the same mammalian species – is fairly new. Systematic work on this topic was made possible by certain incidental observations made by animal technicians responsible for deriving and maintaining congenic mouse strains in a special facility for that purpose at Sloan Kettering Institute, in New York, USA.

Studies on the major histocompatibility complex (MHC)

In general, mice of an inbred strain are genetically identical to one another. Mice of an inbred congenic strain are likewise identical with one another and differ from a selected standard inbred strain only in the vicinity of a particular gene or gene complex. This discrete genetic difference between a pair of congenic strains, meaning a standard inbred strain and its congenic companion strain, is achieved by crossing two inbred strains and then serially back-crossing to the selected inbred parental strain for many generations with selection for an allelic genetic trait of interest, derived from the opposite parental strain, in each generation. Any difference that distinguishes a pair of congenic strains, provided that this is shown to be genetic by appropriate segregation tests, must be due to the selected gene or a gene in that vicinity, i.e. within the small segment of donor chromosome carried over together with the selected gene (Boyse, 1977; Foster et ai, 1981).

Introduction

Much evidence has now accumulated to demonstrate that individuals respond differentially to conspecifics according to their genetic relatedness (e.g. Hepper, 1986a; Fletcher & Michener, 1987; see also this book). Furthermore, this differential responding is not confined to one particular behaviour but is found in a diverse variety of situations and behaviours (see this book). This strongly suggests that individuals have some means which enable them to identify genetic relatedness. It is the aim of this chapter to explore how individuals recognize their kin. Previously (e.g. Hepper, 1986a; Porter, 1987; Waldman, 1988) this ability has been considered under the general rubric of the ‘mechanisms’ of kin recognition. This chapter will discuss factors which contribute to the individual recognizing its kin and will, by addressing these factors, enable the underlying basis of kin recognition to be elucidated. Although the chapter will concentrate on mammalian kin recognition it is hoped that the considerations presented will be applicable to other animal groups. I shall first discuss present approaches to mechanisms of kin recognition.

In Hamilton's seminal papers of 1964 (a,b), as well as demonstrating the fitness benefits to an individual of responding differentially to kin and nonkin, a number of ways were proposed by which individuals would be able to discriminate between kin and non-kin in social situations. From this discussion (Hamilton, 1964b) and that of others (e.g. Alexander, 1979; Bekoff, 1981; Hölldobler & Michener, 1980) four basic ‘mechanisms’ have been proposed to explain how individuals recognize their kin (Holmes & Sherman, 1983). These have become firmly rooted in the literature and I shall outline each briefly.