Up to this point, we have concentrated on social learning and its consequences in nuclear and extended families, where information is transferred between mates, between biological or adoptive parents and their offspring, between helpers and those they help, and among sibs. We now want to widen our discussion to see what goes on in those species of birds and mammals that are highly social, living in more or less permanent groups composed of both related and unrelated individuals. Our aim in this chapter is not to carry out an extensive review of the social group-life of birds and mammals. Rather, we want to look at some aspects of behaviour and psychology that throw light on the formation and maintenance of group traditions, and see how these group traditions themselves influence, directly or indirectly, the evolutionary development of social behaviour. We shall show how the various psychological mechanisms that serve to organise and co-ordinate the activities of a group depend on a constant flow of information among its members. This flow of information is mediated through social learning and maintained by frequent social interactions.

Before starting this discussion, we want to take a close look at the real-life intricacies of a group-living social mammal. So, imagine a cloudless day in January, in the Kalahari desert of south-west Africa, where we are watching the activities of meerkats, the social mongooses that live in small groups on the dry, open plain along the Nossob river.

According to the Bible, the Lord commanded Moses to tell his people ‘Thou shalt love thy neighbour as thyself.’ Regrettably, most of us fall short of this high moral standard: the interests of friends and neighbours are usually not as close to our heart as our own interests. Although human beings often co-operate with each other, strikingly altruistic acts are far from being the rule. When we do encounter them, we tend to regard them with surprise, admiration and sometimes even with contempt, indicating that these acts are seen as something exceptional. Impressively altruistic acts, especially those that are not directed towards close relatives, are often thought of as biologically ‘unnatural’ – the result of ideals imposed on us by custom, law or God, or else the unfortunate outcome of some miscalculation. Biologists have therefore been extremely puzzled by the observation that many birds, mammals and even insects perform what seem like acts of self-sacrifice. They take risks by warning others of lurking predators; they fight, sometimes to the death, to protect other individuals; and they take upon themselves the onerous chore of caring for the young of others. In several hundred species of birds and mammals, from bee-eaters and kingfishers to jays and woodpeckers, from voles and mongooses to bats and marmosets, parents are helped to rear their offspring by other individuals who seem to surrender, at least temporarily, their own reproductive rights and opportunities, and become ‘helpers’.

The mother-mouse portrayed in the previous chapter worked hard to rear her offspring, providing them with all the essentials: with food and warmth, with information and with security. As a typical mammalian single mother, she was not assisted in her labours, and hence did not enjoy the increased reproductive success that the help of another individual, such as her mate, might bring. But in some species of mammals and most birds, the mother is not the only caregiver; frequently the father participates in parental care and contributes to the offspring's ‘education’. Paternal involvement is not without complications, however, and sometimes there are conflicts between the parents over who should care for the youngsters, how much care should be given and for how long. Mates may also disagree over copulation frequency, fidelity and the level of commitment to the relationship. Indeed, our everyday experience of the relationships between human mates, as well as observations of monogamous birds and mammals, testify to frequent disagreements. The great Scandinavian playwright August Strindberg, one of the most bitter and eloquent writers on the struggle between the sexes, described the conflict between human males and females as being as old as sex itself and fundamentally insoluble. But what does this ancient conflict mean for biologists? Can we interpret family disputes as a reflection of conflicting evolutionary interests? How is the regular and often spectacular co-operation between mates achieved?

As with the relationships between mates, the focus of most evolutionary studies of the relationships between parents and their offspring and between siblings is conflict. This is not really surprising. Human beings have always been fascinated with family conflicts, as our myths, literature and gossip show. The Old Testament is a rich testimony to the centrality of conflicts in our lives: think about the bloody dispute between Cain and Abel, which culminated in the murder of Abel and the stigmatisation of the human race; think about Rebecca's maternal manipulation of the rivalry between Jacob and Esau over status; think about the story of Joseph and his brothers. But family conflicts are not limited to humans. Animal life is also full of sibling rivalry and parental attempts to control their unruly children. The interests of siblings often clash, and frequently those of parents and offspring seem not to coincide. As we know all too well, the joys of family life are marred by many problems.

Although learning is an essential part of the ambivalent and intricate interactions between parents and their offspring, evolutionary interpretations of these interactions have failed to take into account the limitations and possibilities that learning introduces into the relationship. In this chapter, we will try to show how incorporating learning into the evolutionary scheme provides additional and alternative explanations of many aspects of parent–offspring relationships.

Any discussion of evolution must assume something about heredity, so ideas about evolution and notions of heredity are intimately linked. From the outline of our views given in the previous chapter, it will be clear that we believe that something is wrong with the assumptions about heredity that underlie a lot of present-day evolutionary thinking. In this chapter, therefore, we are going to take a closer look at the hereditary basis of behaviour, focusing on its genetic basis. What does it mean to say that genes determine behaviour? What is the difference between this assertion and the claim that patterns of behaviour have a genetic basis? To what extent do heritable differences in behaviour reflect genetic differences?

Often the easiest and most fruitful way of thinking about the evolution of behaviour is to have some actual animal behaviour in mind, so in this and most subsequent chapters we are going to ground our discussion on some observations of real animals in their natural habitat. This time we take ourselves at sunrise to an old olive orchard in the Judaean hills near Jerusalem.

In this chapter we are going to look at tradition, genes and learning all at once, as they interact during evolution. We have shown in previous chapters how, irrespective of any genetic change, social learning can lead to independent cultural evolution and promote speciation. When the role of the transmission of learnt information is recognised, interpretations of the evolution of many important behaviours are altered. However, for a more complete picture of what happens during behavioural evolution, we need to look at the type of genetic changes that occur during the evolution of the mechanisms of learning and the various forms of memory. We need to know what drives the evolution of learning, and in what kinds of environments it is likely to evolve. Learning is not a monolithic process, of course. For example, the development of bird song involves imprinting-like learning, trial-and-error learning and several types of social learning, all entwined. The same is true of the development of behaviours such as foraging, hunting, mobbing and even of nest building, the once classical illustration of an ‘instinct’. So how do these different types of learning evolve, and how does behavioural transmission across generations affect learning and other processes and characters? In what follows, we are going to argue that learning is an important agent of its own evolution – that the evolution of learning is, to a large extent, self-propelled.

Introduction

In most species of the animal world, fathers contribute relatively little to the well-being and provisioning of their young, often no more than their genes (for exceptions, see, e.g., Ridley 1978; Trivers 1985; Clutton-Brock 1991). This is especially true for mammals, where internal fertilization, long gestation and lactation predispose mothers to care for their offspring alone. Since only females lactate, males can contribute relatively little to rearing of young. Due to internal fertilization paternity is never certain. Moreover, during the long periods of gestation males have ample time to desert the impregnated female in order to increase their reproductive success by seeking additional fertilizations with other females. Not surprisingly then, paternal care is found in only a small minority (less than 5%) of all mammalian species (Kleiman 1977; Clutton-Brock 1991; Woodroffe & Vincent 1994). Compared to most other mammalian taxa, however, primates are characterized by a surprisingly high level of male–infant affiliation or “male care”: Nearly 40% of all primate genera have been reported as exhibiting “direct male parental care” (carrying, retrieving, protecting, provisioning, grooming and/or huddling with young) – the highest percentage for any individual mammalian order (Kleiman & Malcolm 1981).

While there are reasons to remain skeptical about whether all of these observations are correctly classified as “male care” (e.g., Hrdy 1976; Packer 1980), or whether male care is really widespread among all of the species mentioned (Maestripieri 1998), this high level of male–infant affiliation is unexpected and, more importantly, does not seem to be well understood.

Introduction

The aim of this chapter is to evaluate the evidence for the sexual selection hypothesis for infanticide by male primates, in relation to other hypotheses for this phenomenon. The sexual selection hypothesis emerges largely vindicated. The second part of the chapter then sets the stage for the rest of this book by summarizing observed behavior during episodes of infanticide, the evidence for the decision rules used by males, and the effects of social organization on rates of infanticide by males, and by pointing out some of the remaining difficulties with the hypothesis in its present form.

Critics have repeatedly pointed out that the evidence for infanticide in primates is often circumstantial at best, and that researchers may have jumped to conclusions on the basis of premature extrapolation from snippets of observations (Boggess 1979, 1984; Bartlett et al. 1993; Sussman et al. 1995). This makes it difficult to critically evaluate the hypothesis that a male committing infanticide will on average gain reproductively by doing so. Of course, it has made it equally difficult to evaluate other hypotheses. In this chapter, I therefore evaluate the sexual selection hypothesis for infanticide by males in non-human primates by a careful review of the most appropriate sources of evidence: directly observed cases in wild primates.

The conditions in which male infanticide are expected to raise the male's fitness have been reviewed extensively before (Hausfater & Hrdy 1984).

Introduction

The chapters in this volume point to four major conclusions. First, infanticide by males in many kinds of animal is most reasonably interpreted as a reproductive strategy, although not every observed case fits neatly all the criteria specified by this hypothesis (van Schaik, Chapter 2; Palombit et al., Chapter 6; Blumstein, Chapter 8; Veiga, Chapter 9). As further evidence accumulates, the patterns appear to reinforce the sexual selection hypothesis (e.g., Borries et al. 1999b) rather than non-adaptive interpretations (see Sommer, Chapter 1). Second, there are predictable correlates of infanticide risk among primates and other mammal species, including life history factors such as long infant dependency relative to gestation, large litter size, altriciality and social factors such as the loss of protectors, in particular the rate of breeding male replacement (van Schaik, Chapters 2 and 3; Borries & Koenig, Chapter 5; Blumstein, Chapter 8; van Noordwijk & van Schaik, Chapter 14; Nunn & van Schaik, Chapter 16). Third, females in species with infanticide by males are not just passive recipients of male aggression, but have developed a broad array of behavioral and physiological strategies to reduce infanticide risk. These traits are a major focus of this volume and will be developed more fully later.

A fourth conclusion to emerge is that females may also kill infants, in some species more frequently than do males (Blumstein, Chapter 8; Veiga, Chapter 9; Digby, Chapter 17; Voland & Stephan, Chapter 18).

Introduction

It is now widely accepted that infanticide by males has affected important features of primate social organization by selecting for various social counterstrategies of females (Hrdy 1979; Smuts & Smuts 1993; van Schaik 1996; Treves & Chapman 1996; see various chapters in this book). One of these possible female counterstrategies is female secondary transfer (Marsh 1979b; Sterck 1997; Sterck & Korstjens, Chapter 13). Female transfer decisions are expected to be strongly influenced by the identity of the male with whom a female associates. Secondary transfer is expected only where female relationships are relatively weak because it means the break-up of associations and coalitions, at least temporarily. Hence, given the predominance of female philopatry in primates, only a small number of species is expected to show this behavior. Thomas's langurs (Presbytis thomasi) are one of the few species known to show female secondary transfer related to infanticide avoidance. Females leave when infants have died or when they are old and independent enough to be left behind (Sterck 1997; Steenbeek 1999a). This makes the Thomas's langur an excellent choice for investigating the possible influence of infanticide on social relationships, since in species like this female choice in relation to male characteristics and strategies will be most manifest.

Species with regular female secondary transfer are of particular interest, because where the group contains only a single male, female emigration may terminate a group's lifespan.

Introduction

The sexual selection hypothesis for the selective advantages of infanticide by males requires that certain conditions be met. Provided the male is able to locate the infant, in order to derive reproductive benefits from infanticide he must be able to kill it with limited costs, the female must resume ovarian cycling earlier or produce more offspring than she would do otherwise, and he must gain mating access to the female when she resumes cycling (Hrdy 1979; van Schaik, Chapter 2). Whether or not these conditions are met depends on life style and life history. Life style variables are the location of the infants relative to the female, the presence or absence of hiding places for infants, and the degree of predictability of female spatial position in territories. Life history variables include the degree of infant precociality, and hence their ability to escape from attacking males, and the speed of female reproduction, i.e., their ability to be pregnant and lactating at the same time.

In this chapter, I examine whether infanticide by males is concentrated in species with the expected female life history. Infanticide by males is most advantageous where lactation is long relative to gestation. In such species, postpartum mating and early pregnancy are impossible because this would produce two sets of young of different ages, different needs and different competitive power for access to milk.

Introduction

The killing of dependent young individuals by conspecifics, what ecologists have called infanticide, has been viewed as one extreme and dramatic consequence of selection favoring those behaviors that promote the direct fitness of perpetrators (e.g., Hamilton 1964a,b). However, the evolutionary scenarios of this behavior may differ considerably depending on the identity of the perpetrators. It has been proposed that infanticide by non-kin is fundamentally different from infanticide by kin, which emphasizes the fact that the latter involves the sacrificing of shared genes for some presumed compensating benefits to the perpetrator's inclusive fitness (O'Connor 1978; Mock 1984). This infanticide by kin can be further subdivided into parental infanticide, i.e., the killing of young is committed by their own parents, and siblicide, the term used when the killing is carried out by full or half-siblings. The incidence of siblicide in taxa other than birds is, however, practically unknown (see Mock 1984). Four functional hypotheses have been proposed by Hrdy (1979) to explain the different types of pay-offs that may accrue to infanticidal individuals. In other words, infanticide should have evolved in the following contexts: (1) the exploitation of the infant, mainly as a food source; (2) resource competition, either with the infant or with its parents; (3) parental manipulation, wherein the parents interrupt their investment in the offspring to maximize their reproductive success; and (4) sexual selection, wherein infanticide increases the success of killers in intrasexual competition for mates.

Introduction

The topic of infanticide has been a staple theorem of sociobiology ever since this discipline – the study of social behavior from an evolutionary perspective – was born two and a half decades ago (Wilson 1975). The killing of conspecific young is still hotly debated. Does it occur at all, does it reflect an adaptation, a pathology or even a political agenda? Infanticide – observed among such varied taxa as birds, rodents, carnivores, pinnipeds and primates (Hausfater & Hrdy 1984; Parmigiani & vom Saal 1994) – therefore remains a litmus test upon which the validity of a sociobiological interpretation of behavior depends. I attempt to trace some intellectual roots of the controversy: those of defenders of adaptationist explanations, those of critics from within the paradigm of evolutionary biology, and those of critics who operate from other paradigms such as the social sciences. My ultimate aim is to defend the adaptationist interpretation as a valid and fruitful approach, while acknowledging that its narrative is anchored in a time-dependent framework of interpretation.

Cute and brute

People are fascinated by animals, not least because people are, in their own right, animals who can empathize with similar organisms. The average viewer of a natural history documentary will feel good if a monkey mother cuddles her newborn: “It's so cute.” But different emotions flare up if, over television dinner, wild chimpanzees eat an infant of their own kind: “It's so brute.”

Introduction

Sex-biased dispersal

Dispersal is a common feature of bird and mammal societies. Philopatry, however, is generally assumed to be the most advantageous situation, because it assures knowledge of the home range and offers better opportunities for cooperation with relatives. Several benefits of foregoing these advantages have been proposed (better mating opportunities, including inbreeding avoidance; reduction of within-group competition; coercion) (Greenwood 1980; Pusey & Packer 1987a; Moore 1993). The balance between the costs and benefits of dispersal obviously differs between the sexes, because dispersal is often highly sex biased. Most bird species show a female bias in dispersal, whereas most mammal species show a male bias (Greenwood 1980; Dobson & Jones 1985; Liberg & Schantz 1985). The best explanation proposed so far for such a strong sex bias is inbreeding avoidance.

In mammals it is generally assumed that the costs of dispersal are higher for females than for males, because loss of a range or allies affects female reproductive success more than male reproductive success, explaining the prevalence of male-biased dispersal (Waser et al., 1986; Pusey & Packer 1987a; Clutton-Brock 1989a). Female dispersal, however, is found in some mammal species and a considerable number of primate species (Moore 1984; Clutton-Brock 1989a; Strier 1994).

Costs and benefits of dispersal

Different costs and benefits of female philopatry and dispersal can be distinguished. Females in gregarious animals such as diurnal primates can remain in their natal range or in their natal group.