Various models have been proposed to explain how patterns of cooperative (between conspecifics) and mutualistic (between different species) interaction can arise and can be maintained. Game theoretical approaches, which began with the application of the Prisoners’ Dilemma paradigm, proved very stimulating, but it has become clear that they fall short in accommodating the complexities of the majority of real-life interactions. Various assumptions and implications of these models are not realistic. Thus cooperative and mutualistic interactions do not often occur in dyadic isolation, but mostly take place in a setting where there are many potential players. This implies that partner choice should be an essential element in models of cooperation. Moreover, the ratio of supply and demand for the commodities that the different parties seek to acquire may vary. Depending on this ratio, there may be competition between potential ‘buyers’ and ‘sellers’. Last but not least, there can be communication between the parties, leading to a process of bartering. These are characteristics which we normally associate with a ‘market’.

Ronald Noë was one of the first to realise the limitations of the game theoretic models which were current when he conducted his studies on coalition formation in savannah baboons. In the first chapter of Part II he reviews the different models which have been proposed and argues that a market approach offers a most appropriate perspective for understanding systems of cooperative and mutualistic interaction.

In the following chapters both theoretical considerations and supportive empirical evidence are presented to show that a market model offers the appropriate framework for studying such exchange systems.

Introduction

Males of many species are typified by exaggerated secondary sexual traits and courtship displays (Darwin 1871; Andersson 1994). These sexual signals are highly variable amongst closely related species and appear to change very quickly in evolutionary time (Iwasa & Pomiankowski 1995). Two classic examples of exaggeration and diversity in sexual characters are the cichlid fish species flocks of the African Great Lakes (Fryer & Iles 1980) and the birds of paradise found in south-east Asia (Coates 1990).

In this chapter we will consider how female mating preferences cause the evolution of exaggeration and diversity in male sexual displays. As recognised by Fisher (1930) this requires an understanding of how female sexual preferences evolve. Two main hypotheses have dominated thinking on this question, Fisher's runaway and the handicap process. These ideas concern the benefits of mate choice. Fisher's runaway assumes that females select mates with exaggerated ornaments because they are attractive. Choosy females benefit as their male offspring inherit genes for attraction. The handicap process assumes that the degree of exaggeration reveals male quality. In this case, choosy females benefit directly because higher-quality males make better fathers or indirectly because quality is inherited by their offspring. These are not the only forces affecting the evolution of mate choice. For example, inbreeding avoidance and species recognition can be important. However, Fisher's runaway and the handicap process seem the best candidates for explaining exaggeration and diversity.

The evolution of female preferences for male sexual ornaments has been treated in a number of ways, using major gene, quantitative genetic and game theory models. In the following sections we will summarise our work using quantitative genetic models.

Choice as a selective force

Selection, the driving force of evolution, is the process by which varieties that are better adapted to their environment increase in frequency relative to less well-adapted forms over the generations. The ‘environment’ is often perceived as a relatively passive mould into which the organism fits more or less well. Often enough, however, organisms literally select among other organisms and by their choice alter the relative fitness of the individuals among which they choose. Cheetahs, for example, may select the weakest individual in a group of Thomson gazelles (Caro 1986) and peahens may prefer peacocks with large, elaborate trains (Petrie et al. 1991).

Systems such as the peacock's mating system, in which the members of one class of organisms benefit from being chosen by members of another class, have properties similar to human markets on which goods or services are exchanged. These properties are:

1. • Commodities are exchanged between individuals that differ in the degree of control over these commodities.

2. • Trading partners are chosen from a number of potential partners. On average the interaction with a chosen partner yields a higher ‘profit’ than an interaction with a random partner, i.e. a fitness gain in evolutionary terms.

3. • There is competition among the members of the chosen class to be the most attractive partner. This competition by ‘outbidding’ causes an increase in the value of the commodity offered and hence its production costs. In evolutionary terms: stronger competition forces organisms to accept less favourable fitness effects from interactions.

4. • Supply and demand determine the bartering value of commodities exchanged.

5. • Commodities on offer can be advertised. As in commercial advertisements there is a potential for false information.

Living in a group is a cooperative strategy. Animals live in groups only if groups yield a net advantage compared to living solitarily. Group living inherently implies competition, however: one's worst rivals in the competition over food or mates are the conspecifics with the same needs and desires. The same is true for human social networks: common interests often go hand in hand with conflicts over the partitioning of utilities or duties. Thus both humans and non-humans are frequently caught in ‘social dilemmas’ and face similar problems: to find the optimal balance between contribution and exploitation and to keep cheaters and free-riders in check. Animals use strategies shaped by selection in the course of evolution when they deal with these challenges. Humans have the alternative option of using their cognitive capacities to plan their strategies rationally.

In the first chapter of Part I Elinor Ostrom, who has her roots in the social sciences, reviews the vast body of empirical as well as theoretical knowledge on the behaviour of humans caught in social dilemmas. She finds that humans tend to behave more cooperatively in social dilemmas than theory would predict. Charles Nunn and Rebecca Lewis look at social dilemmas with the eyes of evolutionary biologists. In this field the emphasis has traditionally been on dyadic interactions. Nunn and Lewis therefore first show how dyadic game theoretical models can be developed into the n-player models that are more meaningful to the study of social dilemmas.

Introduction

The interaction between ‘cleaners’ and their ‘clients’ is one of the most amazing interspecific interactions one can witness on coral reefs. Cleaners are small fish and shrimps that inspect the body surface and the inside of the gill chambers and mouth of larger fish, the clients, in search for ectoparasites and dead or infected tissue (Eibl-Eibesfeldt 1955; Randall 1955; Limbaugh et al. 1961, reviews: Feder 1966; Losey 1987; Losey et al. 1999). Cleaning seems to be ubiquitous in aquatic systems, and many fish species are known to be facultative cleaners as juveniles (review by Wirtz 1998). The highest degree of specialisation is found in coral reefs, where a few members of the Labridae and Gobiidae families evolved into highly specialised cleaners which feed almost exclusively on material they remove from clients (Losey et al. 1999). Most work has been done on the two cleaner wrasses Labroides dimidiatus and L. phthyrophagus (Losey et al. 1999). These cleaners live in small territories, the so-called cleaning stations. Clients actively visit these cleaning stations and often use special postures to signal their wish to be inspected (Randall 1958; Losey 1971). Clients visit cleaners several times a day, some up to an estimated 144 times a day for a total of 30 min. (Grutter 1995).

Since the 1950s, scientists tried to solve the puzzle of this apparent mutualism. After early descriptive work, the question of the impact of cleaning on client fitness was tackled. Experiments in which cleaners were removed from relatively small coral reef heads (‘patch reefs’) which are isolated by sand from other reef areas, yielded inconclusive results concerning changes in fish densities and parasite loads (Limbaugh 1961; Youngbluth 1968; Losey 1972; Gorlick et al. 1987; Grutter 1997a).

The despotic society model

In 1932 an English zoologist, the later Sir Solly Zuckerman, published a book entitled The Social Life of Monkeys and Apes. It was based to a large extent on his studies of the social behaviour and relationships in a colony of hamadryas baboons (Papio hamadryas) in the London Zoo. This book would influence the scientific view on animal societies for a long time to come. Zuckerman painted a rather grim picture of this baboon society. He emphasised its despotic character. Despotic dominance relationships were maintained by severe, sometimes lethal, aggression and bullying, and were expressed in sexual violence and raping. Sexual drive was supposed to form the main cohesion factor. Sexual presenting, typically a female solicitation behaviour, but also used by subordinate males, was supposed to function as a submissive means to avert violence and the tensions of conflict. We now recognise this picture as a caricature. The situation was caused by the unnatural, and – one might say – even pathological condition of this colony. The hamadryas baboons had been collected from the wild and had been put together in the zoo, without due regard for the natural growth and for the history and maturation of their social relationships.

The complexity of natural social organisation

The hamadryas baboon has a rather peculiar social organisation, unlike that of many other primates (Kummer 1957, 1968). In the wild these baboons live in large groups with a multilayered structure. The basic units are formed by harems, in which, as a rule, a single adult male herds a few females and their offspring. In the barren desert environment in which this species lives, these harems are the basic foraging units.

Introduction

It is now almost three decades since sperm competition was defined in terms of competition between the ejaculates of two or more males for a given set of eggs (Parker 1970). That article reviewed the evidence in insects and suggested a variety of ways in which the selective pressure of sperm competition may shape a range of adaptations across behavioural, physiological and morphological levels. Sperm competition is now accepted as a discipline in its own right, and currently attracts considerable interest. In addition to a host of papers, there exist four books on the subject (Smith 1984; Birkhead & Møller 1992, 1998; Baker & Bellis 1995) and others are in preparation.

Interest has focused on both empirical and theoretical aspects of sperm competition, and our own contribution has mainly related to the formulation of a prospective theoretical basis. We wish in this chapter to summarise the current theoretical models and their predictions on one specific aspect of this work: the economics of sperm allocation by males in relation to the information available to them. We stress that our concept of ‘information’ is a broad one. We include information in the form of cues correlating with the risk or intensity of sperm competition, perceived by a given male at the time of mating, and also include ‘information’ in the sense of a ‘self-knowledge’ (an adaptive response in relation to a given male's personal circumstances or state). In order to do this we compare predicted sperm allocation patterns in the absence of information with those predicted under specific information regimes.

The mammalian strategy of internal gestation followed by lactation imposes severe constraints on what males can do in terms of parental investment. This asymmetry in the processes of reproduction results in male mammals placing disproportionate emphasis on mating strategies and less on parental care than is typical of most other taxa. Although male mammals can contribute indirectly to parental care (e.g. by defending a feeding territory for the females(s) or acting as an anti-predator defence), this only remains an option where females can gain a net benefit from associating with males relative to the foraging costs that additional animals must inevitably impose on them.

This asymmetry in reproductive biology has one important implication for mammalian social systems. In birds, it is not uncommon for males to arrive first on the breeding ground.Having partitioned the available space among themselves, they settle on their territories to await the arrival of the females who then choose among them. While a similar pattern can be observed in those mammals that adopt a lek mating system (notably some deer, antelope and pinnipeds), the reverse is probably more typical of many mammals (and most primates). In a classic experiment, Charles- Dominique (1977) released a number of dwarf galago (Galago demidorvii) into a forest in Gabon. He found that the population developed its own natural structure in a surprisingly ordered manner. First, the females established their ranges; once they had decided how to distribute themselves, the males then mapped themselves onto the female distribution.

Introduction

Economists think they know how humans ought to behave if only they were smart enough. Biologists have some knowledge of how animals actually do behave. It does not seem a feasible question to ask how animals ought to behave. Yet, there is a conceptual link between normative economic theory and its empirical biological counterpart. Darwinian evolution often creates animal traits that look to an observer as if the animal did care about the economist's advice. Therefore, economic analysis of animal behaviour has become a flourishing field of biological research in which games and markets play an important role. This chapter discusses fundamental concepts in human and animal economics. They are illustrated with examples from both disciplines. Furthermore, it is shown that the facts often do not meet theoretical expectations. Some hints are given as to why this may be so. Theory development in animal and human economics is far from being completed.

Evolutionary adaptation and bounded rationality: are animals better economists than humans?

Classical economic theory based most of its thoughts on the idea that decision makers are rational in the sense of maximising subjective expected utility. Savage (1954) axiomatised this Bayesian approach to decision making and Harsanyi & Selten (1988) explored it further in the game theoretic context of strategic interaction. However, the more the economic notion of rationality had been made precise, the less it seemed adequately to reflect properties of the real world. Rational decision makers are assumed to possess unlimited cognitive and computational power and to solve correctly every mathematical problem in zero time at no cost.

Introduction

Mutualistic interactions between species are diverse and widespread, and are becoming well documented empirically (Bronstein 1994b). The partners involved in mutualistic interactions range from bacteria to fungi to plants and animals. Early mathematical models of mutualisms predicted that they should be rare in nature (e.g.May 1973). Since then, modellers of mutualisms have focused on defining conditions and mechanisms that could account for the prevelance of mutualistic interactions in nature. Recently, mutualisms have been modelled as biological markets (Noë & Hammerstein 1994, 1995; Schwartz & Hoeksema 1998).

Mutualisms are characterised by complexity and variation, with multiple, varying individuals and species on both sides of the interaction, species engaged in multiple types of mutualism simultaneously, and costs and benefits of the interaction changing over time and space. Biological market models address this complexity in a number of ways, and as such may be appropriate for modelling many types of mutualistic interactions. The central mechanism of market models is that the price of trade is negotiated, with individuals choosing partners who are offering the best price. This partner-choice mechanism incorporates variation among potential partners in a mutualism, and recognizes that mutualisms operate in a complex community context.

Many mutualisms may be best seen as interactions in which individuals of one or both species exploit individuals of the other species, but that none the less result in net benefits to each of the individuals involved (Thompson 1982; 1994; Futuyma & Slatkin 1983; Janzen 1985; Herre & West 1997).

Periodically through the day – most obviously early in the morning and late in the afternoon – an individual member of a wild baboon group will approach another and begin to comb meticulously through its pelage with dextrous fingers or, equally likely, solicit such behaviour by lying down in front of the other animal. Such grooming, for other monkeys and apes, as well as baboons, is the defining act of sociality. Its dynamics are therefore likely both to reflect current ecological circumstances and to illuminate historical selection for attributes that enable successful performance in the social world. The broad question then, with which to begin, concerns the function of grooming.

To the observer, two things are immediately apparent. First, grooming clearly has hygienic value, since an animal also puts effort into grooming itself and because the grooming it receives from others is directed at those parts of its body that it cannot easily reach (Barton 1985). The targets of this grooming are ectoparasites, such as lice and their eggs (Saunders 1988; Tanaka & Takefushi 1993). The diligence and concentration that groomers apply to this task underscore the fact that grooming is more than just a pretext for tactile contact. Nevertheless, the second observation is that this physical contact is manifestly pleasurable for the recipient; it is, in fact, associated with the increased production of β-endorphins (Keverne et al. 1989). Presumably, this hedonistic benefit is a derived feature and serves, proximately, as the primary reinforcer sustaining participation. The analysis of function cannot, however, end here.