I can't remember a time when I wasn't interested in social behaviour, and I chose a biology degree course where animal behaviour was a key component. Sussex University was an exciting place to be as an undergraduate in the early 1970s when sociobiology was coming to the fore, and I was lucky enough to have John Maynard Smith as my personal tutor. John's enthusiasm for applying evolutionary principles to animal behaviour was an inspiration that I still value today. When I started doing a PhD on moorhens Gallinula chloropus the working title for my thesis was ‘the function of winter flocking in moorhens’ – why animals live in groups was a key issue in the 1970s. It was whilst watching flocks that I noticed birds fighting in front of potential mates. Moorhens cannot be sexed in the field so it was not immediately clear whether it was males fighting for females or vice versa, and I can remember still my surprise and delight when I came back home and looked up the birds' numbers and sizes to discover that it was the smaller females fighting in front of males. It became clear that they were fighting for access to a particular male, and I started to wonder what it was about this male that was worth fighting for.

Research on wild primates was still a relatively new endeavour in the USA when I entered graduate school in 1970. Courses on primate behaviour were primarily taught in anthropology departments. I was drawn to the field because Japanese researchers had reported that adult male monkeys sometimes killed infants in a species of South Asian monkey known as the Hanuman langur Semnopithecus entellus, and I wanted to find out why. The summer after my first year in graduate school I went to Mount Abu, in Rajasthan, with this question in mind. At the time I had no special interest in female behaviour, which frankly struck me as boring.

According to the only available article on the subject, entitled ‘The female primate’, ‘Her primary focus, a role which occupies more than 70 percent of her life, is motherhood … A female raises one infant after another for her entire adult life … Dominance interaction is usually minimal’ (Jay 1963). This narrow view of female natures was the result of a combination of factors, including Victorian social biases left over from Darwin's day, the fact that earlier observations had focused on captive animals, often consisting of mothers caged individually with their young, and evolutionary theory itself. As then formulated, Darwin's remarkably original and quite powerful theory of sexual selection left out many sources of variation affecting the differential reproductive success of females.

Overview

In sexually reproducing species, individual fitness is ultimately determined by social interactions over mating and fertilisation among rival members of the same sex and between prospective partners. Variation in the competitive ability to secure reproductive opportunities generates sexual selection, which promotes traits that confer a reproductive advantage in intrasexual competition through combat, scramble, courtship or manipulation, and which may benefit or harm members of the opposite sex. The ensuing intra- and intersexual coevolutionary dynamics often drag phenotypes away from naturally selected optima, producing the spectacular exaggeration that has captured the interest of generations of biologists. In this chapter, we first illustrate how the evolution of differential gametic investment by males and females (anisogamy) sets the scene for sexually dimorphic strategies and, ultimately, determines the intensity of evolutionary conflict between the sexes. In particular, we focus on intra- and interlocus sexual conflicts and their profound but poorly understood repercussions for intersexual coevolution. Second, we outline the principles of sexual selection theory, focusing on their implications for the evolution of sexual behaviour. Finally, we conclude by identifying future directions for the evolutionary analysis of sexual behaviour.

Introduction: sexual behaviour as a social trait

The lifetime reproductive success, or fitness, of an individual is measured by the representation of its genes in the gene pool of the next generation. In sexually reproducing species, individual fitness reflects the number of zygotes produced by an individual over its lifetime, and – indirectly – the ability of these zygotes to develop and reproduce.

Overview

Pair bonds and parental behaviour are among the most variable social traits. To understand how and why these traits are so variable, we investigate three issues in this chapter. First, we present an overview of recent work on molecular and neural aspects of pair bonds and parental care using microtine rodents as model organisms. We focus on two neuropeptides, oxytocin and vasopressin, and show that although both molecules are found in both sexes, oxytocin plays a more prominent role in regulating parenting and pair bonding in females, whereas vasopressin serves this role in males. Variation in the expression of oxytocin and vasopressin receptors appears to contribute to species and individual differences in social behaviour. These studies also show that although oxytocin and vasopressin function in distinct brain regions, they act within the same neural circuit. Therefore, females and males appear to accomplish behavioural changes in pair bonding and parental care by altering the responsiveness of the same neural circuit. Second, studies of pair bonds and parental care in natural populations have revealed that these traits are often tied together. Cost–benefit analyses of both traits in a game-theoretic framework provide novel insights into how diverse pair bonding and parental care may have evolved. Recent work emphasises the role of social environment in influencing pair bonding and care. Finally, we point out that currently there is a schism between proximate and ultimate approaches to understanding pair bonding and parental care.

Overview

Given the vast topic of group living, this chapter highlights research areas into group living that continue to attract considerable attention or represent new developments. By these criteria, three topics stood out to us: the selfish herd, social networks and collective behaviour. The selfish herd is the idea that aggregation of prey animals can occur simply through the selfish actions of individuals positioning themselves so as to reduce their risk of attack. This idea is very much at the core of why animals live in groups, and the theory has been influential for a considerable period. The idea of the selfish herd is simple but subtle, and we decided to discuss it carefully, since textbook discussions on this concept often ignore four aspects of complexity: more complex and realistic geometries than are normally considered; the underlying behavioural rules that might lead to selfish herd effects; the predicted outcome of such rules in terms of properties of the group; and the interaction of selfish herd effects with other selective pressures on group size, shape and composition.

The second emerging field we choose is the application of social network analysis (a conceptual and statistical tool from the social sciences) to animal groups and populations. Although this topic is not completely new, recent developments represent an exponential increase in new tools for studying social networks that makes network analysis a powerful method to understand social organisation.

Science is about theories and tests of theories, but it is not nearly as dry or as mechanical as that may seem to imply, especially in behavioural ecology. A life in science is also about career choices made, luck, interesting experiences and even fun. Here is a selection from my own career in studying social selection.

Wisest educational choice. Grad school at the University of Michigan. They had a policy of admitting the best students they could, and giving them time to find their advisors and research programme. I found Richard Alexander, though my first real interaction with him was when he thought I might have cribbed ideas for an essay I wrote for his class. Fortunately, as a good scientist, he could change his mind.

Luckiest educational choice. Grad school at the University of Michigan. Though I knew Alexander would be there, I did not know what an inspiring teacher he was. Nor did I know that he would be arranging semester-long visits, in my first three fall semesters at Michigan, by John Maynard Smith, Bill Hamilton and George Williams.

Favourite paper in grad school. Trivers' 1974 paper on parent–offspring conflict turned kin selection on its head by showing that it could describe conflict among relatives. Dick Alexander didn't think it could be true, but he changed his mind there too. This idea, when applied to social insects (first in Trivers & Hare 1976), made them much more interesting.

Overview

The study of social behaviour, often called sociobiology, is entering a new phase. A growing focus on mechanisms has enriched the older, evolutionary, perspective of sociobiology. The chapters in this book provide an overview of some of the most influential examples of research adopting the multifaceted approaches used to understand social evolution. There are top-down examinations of the way selection influences behaviour and, therefore, its neural and genetic structure, and bottom-up examinations of the genetic, hormonal or neurobiological substrates of behaviour. We therefore have a detailed understanding of the social, ecological, physiological, neurological, hormonal and genetic factors leading to complex social behaviour, but little integration. Picking apart the components and influences on behaviour is a reductionist approach, and although this has provided considerable insights we argue that it is now time for a synthetic perspective. We argue that a complementary perspective that unifies the particulate knowledge we have gained is now possible, and in keeping with current fashion we label this a systems biology approach to studying behavioural complexity. In reality, this is not new but a re-emphasis of the original synthetic view of sociobiology. Systems biology is simply a focus on interactions among components, and it works towards developing a predictive framework for resulting emergent properties of a system. Systems biology depends on a detailed understanding of the component parts to a system, and we believe this will be increasingly available for social behaviour, given the availability of new and less expensive approaches to gaining mechanistic information.

Which comes first – passion for the scientific question or passion for the organism? For most biologists I think it's the former, but for me it was the latter. I became smitten with honey bees at the age of 18 and have never looked back.

Once immersed in study, the question did come: how can a honey bee, with a brain the size of a grass seed, create a collective organisation in which all tasks are divided efficiently but flexibly among as many as 50 000 individuals? Honey bee division of labour is a spectacular example of social behaviour; trying to understand its mechanisms and evolution has motivated most of the research in my laboratory over the years and also has led periodically to rewarding expeditions into new scientific terrains.

After starting with behavioural and endocrine analyses as a graduate student at Cornell University with Roger Morse, my postdoctoral studies with Robert Page at Ohio State University demonstrated for the first time heritable influences on division of labour (Robinson & Page 1988). Then mechanistic studies in my own lab at the University of Illinois revealed striking differences in brain chemistry and brain structure between bees performing different jobs, raising the possibility that these changes were orchestrated by changes in brain gene expression (Withers et al. 1993). To enhance our ability to discover insights into the mechanisms and evolution of this form of social behaviour, I decided in the mid 1990s to initiate a molecular component to our research programme.

Overview

Human social behaviour is wonderfully complex, and influenced by manifold effects including genetic, environmental and cultural factors (Chapter 15). Here we focus on one aspect of human social behaviour: social cognition. Human social cognition, or the ability to process social information thus influencing human social behaviour, is a broad and complex concept, as yet not defined unambiguously. The aim of this chapter is to introduce the basic neural processes underlying human social cognition, and the genetic and molecular influences that may shape behavioural variation between individuals. To this end, we describe the neural circuits in the brain underlying social cognition, particularly with reference to self-knowledge and the concept of theory of mind – the ability to think about things from the perspective of another. Cellular aspects of social cognition, although still unclear, are explored in relation to the putative role of mirror neurons. The neurobiology of attachment underlying social relationships aids the discussion of the molecular underpinnings of social cognition with particular reference to neuropeptides: oxytocin and vasopressin. Oxytocin and vasopressin are nonapeptides that have been increasingly identified as playing a pivotal role in social cognition. Animal studies have highlighted the role of these peptides in social roles as diverse as parenting behaviour, social recognition and affiliative behaviours (Chapter 11). Here we discuss the evidence implicating these neuropeptides in humans. Moreover, it is increasingly recognised in animal studies that the processes of social cognition are supported by reward circuitry, underpinned by the dopaminergic neurotransmitter system in the brain.

OVERVIEW

Sociobiology has come a long way. We now have a solid base of evolutionary theory supported by a myriad of empirical tests. It is perhaps less appreciated, however, that first discussions of social behaviour and evolution in Darwin's day drew upon single-celled organisms. Since then, microbes have received short shrift, and their full spectrum of sociality has only recently come to light. Almost everything that a microorganism does has social consequences; simply dividing can consume another's resources. Microbes also secrete a wide range of products that affect others, including digestive enzymes, toxins, molecules for communication and DNA that allows genes to mix both within and among species. Many species do all of this in surface-attached communities, known as biofilms, in which the diversity of species and interactions reaches bewildering heights. Grouping can even involve differentiation and development, as in the spectacular multicellular escape responses of slime moulds and myxobacteria. Like any society, however, microbes face conflict, and most groups will involve instances of both cooperation and competition among their members. And, as in any society, microbial conflicts are mediated by three key processes: constraints on rebellion, coercion that enforces compliance, and kinship whereby cells direct altruistic aid towards clone-mates.

Reciprocity is the secret of our success, even though two unrelated individuals sometimes find it difficult to cooperate. They may mutually reciprocate help, if they know they will meet again. However, there is always the temptation not to return the help to the donor. Using a strategy such as Tit-for-Tat (see Chapter 4) can minimise the risk of being the sucker in the end, but there is no guarantee. To achieve cooperation seems hopeless when groups of three or more unrelated individuals need to cooperate in order to maintain a common resource: the resource is usually overused and collapses, as do fish populations as a consequence of over-fishing, and the global climate as a consequence of unrestricted use of fossil energy. The latter is regarded as the greatest challenge to humankind. The tragedy of the commons, as Hardin (1968) called this kind of social dilemma (see Chapter 6), appears inevitable – free access to a public resource brings ruin to all.

The so-called Public Goods game has been invented as a paradigm to study tragedy of the commons situations experimentally. For example, a group of four volunteers is asked to supply one euro each to a public pool, which is then doubled and redistributed among the four players irrespective of whether they have contributed. If all contribute, each has a net gain of one euro. However, a single defector has a net gain of 1.50 euro whereas each of the three contributors gains only 50 cents. Why should you cooperate?

Overview

Tinbergen (1963) proposed that in order to understand behaviour it is necessary to discover not only its adaptive function and phylogenetic history (now often referred to as ultimate causation) but also its development and physiology (proximate causation). In recent years there has been increasing appreciation of the importance of pursuing these four aims not only separately but also in an integrated manner that allows them to inform each other. Hormonal and neural mechanisms are best understood in an ecological and evolutionary context. An appreciation of how they work is essential both for understanding the ecology and evolution of behaviour, and for linking genes to behaviour. This chapter will discuss hormonal and neural bases of social behaviour, emphasising basic principles, recent trends and questions for the future, with a more extended discussion of bird song as a prime example of a social behaviour that has inspired a substantial body of integrative research. Special attention will be given to learned song and the songbird neural song system that underlies the learning, production and perception of song. As a neural system that is anatomically well defined, dedicated to an important category of social behaviour, and hormonally influenced, the song system is uniquely valuable for elucidating general principles of the mechanisms of social behaviour.

My interest in the evolution of diversity in microbial populations began more than 20 years ago. For the first 10 of those years I was oblivious to the fact that one of the most dramatic forms to emerge during the course of selection experiments, the so-named wrinkly spreader (WS) type, owed its success to cooperation among individual cells. Rather ashamedly, despite having recognised the novelty of what I had witnessed, it took me another 10 years to get round to publishing this work. Perhaps, however, an attempt to publish in the early 1990s, in the absence of studies that gave credibility to the microcosm experiments (see Chapter 13), would have met with limited success.

There was no eureka moment of realisation, although with hindsight there ought to have been. I was aware that WS genotypes formed cellular mats that grew at the air–liquid interface of broth-filled microcosms (Rainey & Travisano 1998). I was also aware that the ability to occupy the air–liquid interface was the secret of their evolutionary success (the broth phase rapidly become anaerobic due to microbial growth). Most tellingly, I was aware that the mats sank into the broth when they became old and heavy.

Overview

In this chapter we outline proximate processes that favour group formation and lead to the emergence of social structure in mammalian societies, particularly complex societies. We operationally define a mammalian society as complex if its social structure includes social coalitions, social alliances or social queues – well known from primates, elephants and cetaceans but also present in, for instance, some carnivores, bats, rodents and ungulates. We consider how social structure can lead to a disparity in the benefits and costs acquired by group members, and how this leads to conflicts of interest between them. We detail the social and reproductive tactics that individuals use when conflicts arise, and consider the fitness consequences associated with these tactics. We illustrate most key points using observational studies of free-ranging mammals, because experimental studies are rare, and we draw examples from a broad range of social systems and mammalian orders.

Introduction

How do complex societies emerge from a life in groups? Living in groups inevitably results in conflicts of interest between group members. The specific forms of these conflicts are likely to affect the strategies to cope with them. Not only will the details of these strategies shape the social relationships we can observe, they may be the consequences of evolutionary processes, and are likely to have resulted in the social complexity described for many mammalian societies.

When I began as a research student in 1973, the key to understanding mating systems was thought to be through a study of ecology. My bible was David Lack's recent book (1968), which showed how variation in bird mating systems could be linked to differences in the type, abundance and dispersion of resources, such as food and nest sites. Lack concluded that most bird species were monogamous because a male and female each maximised their reproductive success if they cooperated to rear a brood together. Two quotes from Lack's book convey the prevailing view of that time: a comparative approach was needed rather than experiments because ‘no one has yet found how to make a monogamous species polygynous’ (p. 8); ‘given that the marvellous adaptations of the brood parasites are a product of natural selection, it is … hard to concede that this same powerful force is likewise responsible for the dull, conventional habits of the monogamous song birds which raise their own young’ (p. 97).

Two changes heralded a revolution during the next decade. The first was a new idea, namely the recognition of sexual conflict in mating and parental care (Trivers 1972, Parker 1979). The second was a new technique, namely DNA profiles for assigning parentage with precision. A new idea and a new technique was an inspiring combination for a fresh look at bird mating systems.

Overview

Communication is at the core of understanding sociality as an interface between behaviours and phenotypes, and their evolutionary trajectories. Central to communication research is gaining an understanding of the information content of signals and the ecological, social and physiological factors that influence their format. It is clear that individuals which benefit from social exchange can critically influence what information is transmitted, how it is transmitted and whether it is scrambled to prevent eavesdropping. Less clear is how the physical channels through which signals are emitted and received might influence the extent to which they are prone to errors, dishonesty and manipulation. Here we show how sensory systems, perceptual physiology, cognitive decision rules and evolutionary trajectories produce the broad range of signalling modalities and contents that we see in nature. Our overview suggests that experimental evidence on the meaning, honesty and selective benefits of communication for signallers and receivers across invertebrates and vertebrates can provide a taxonomically broad but conceptually similar set of examples. This is not surprising, since studies across diverse lineages have demonstrated that the mechanism and function of communication systems both critically shape social behaviour and are being shaped by sociality. In particular, functional investigations of the sensory systems of vocal communication in songbirds, visual signals in trap-building predators, and chemical signalling in arthropods, have established clear examples of the limits to perception and discrimination of signal design.