Parental care in birds and mammals is so familiar to all of us that it seems unlikely that it can hold any fresh surprises or offer any new insights. However, there are important aspects of parental care that are commonly overlooked when its role in evolution is discussed. Parental care is one of the major routes through which information is transferred across generations. It is largely through the effects of parental care that animal traditions become established. The information transmitted through parental care relates to all the aspects of life; some is used everyday, some only rarely. Information is transmitted through several different but usually interacting channels, and is essential for the survival and reproduction of the offspring. A look at some typical parental behaviour, that of the common domestic mouse, will show the remarkable range and importance of the information that is transmitted from parent to offspring.

To understand how traditions originate and how they evolve, we must first establish the relationship between learning, memory and social organisation. Not everything that is learnt becomes a habit, not every habit involves social interactions and not every social habit is transmitted across generations. We therefore need to know what learning entails, how patterns of behaviour are memorised and how they lead to the formation of traditions. Our purpose is not to describe the neural mechanisms of learning and memory, but rather to outline the psychological, ecological and social conditions that influence how behaviour patterns are generated, remembered and transmitted. ‘Learning’ and ‘remembering’ are not simple and unitary processes, however: different species rely to varying extents on several types of learning and memory. This affects the nature of the habits they develop, and whether or not and in what manner these habits form cultural traditions. To get a better understanding of the different types of learning and their consequences, we will return again to the Judaean hills and observe the behaviour of some of their inhabitants.

This book is about the way in which the evolution of birds and mammals is affected by social learning and by the traditions formed by social learning. From observation and experiment, we know that higher animals can acquire information from or through the behaviour of others, and through their own behaviour they can transmit this information to the next generation. Variations in such socially acquired and transmitted behaviour-influencing information cannot be under direct genetic control, since animals with very similar genes can have, and pass on, very different behaviours and traditions. There is clearly another inheritance system, a behavioural system of information transmission, which is superimposed on the genetic system. Some years ago we decided that the evolutionary consequences of this additional tier of variation and inheritance were worth exploring, and set out to see how our view of the evolution of higher animals is altered by incorporating non-genetic behavioural inheritance and the traditions that it produces. This book is the outcome of that endeavour.

We found that adding the behavioural system of information transmission has some radical implications for the current gene-centred view of evolution. For example, the classical distinctions between development and evolution become very blurred. An animal tradition is the product of a historical, evolutionary process, yet it can be formed and transmitted only if it is actively constructed during the behavioural development of individuals and groups.

If you ask a biologist to explain the evolution of the elaborate morning song of a great tit, the subtle food preferences of a domestic mouse, or the efficient hunting techniques of a pack of wolves, what sort of explanation will you get? The chances are you will be told that this type of behaviour can readily be explained by the conventional theory of natural selection acting on genetic differences between individuals. Ever since Darwin, the theory of natural selection has been applied to all sorts of biological problems, from the origin of life to the origin of language, and for most of this century it has been assumed that genetic differences between individuals underlie the variation on which natural selection acts. It is not surprising, therefore, that behavioural evolution is also seen as the outcome of the selection of genetic variations. But is this view correct? In this book we are going to argue that when applied to the behaviour of higher animals, conventional evolutionary theory is rarely adequate and is often misleading. Natural selection acting on genetic differences between individuals is not a sufficient explanation for the evolution of the behaviour of the great tit, the mouse or the wolf.

To understand why we are not satisfied with the current application of Darwin's theory to behaviour, we need to go back to basics. Darwin's theory depends on some fundamental properties of biological entities: on their ability to reproduce, on the differences between individuals and on the heritable nature of some of these differences.

In The Descent of Man and The Expression of the Emotions in Man and Animals, Darwin argues for evolutionary continuity between the minds of man and higher animals, stressing that higher animals share with us many complex mental capacities:

In one form or another, the continuity thesis is accepted by all evolutionary biologists. Even when a large mental gap between the minds of animals and man is recognised, the interpretation of this gap is based on the assumption that there is an underlying genetic and evolutionary continuity. However, notice how Darwin framed his statement: he did not claim that we are psychologically and cognitively simpler than we believe we are – that we are psychologically more like ‘lower’ animals. On the contrary, Darwin believed that ‘lower’ animals are more complex than is usually thought – that they are more similar to us, possessing more sophisticated capacities than we usually grant them.

In this book, we have followed Darwin's approach, emphasising the learning capacities of higher animals, particularly their ability to learn from others.

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.