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.

Introduction

In many species, the process of mate finding begins with advertising. As such, advertising is an opening bid that is often made in the absence of any information about the quality (and sometimes even the identity) of potential mates. These bids will, however, often reflect a trade-off between the individual's assessment of its own preferences and its experience of what the marketplace in general has to offer. This is as true of human beings as it is of other species (Grammer 1989). In humans, bids of this kind are often contingent on the advertiser's perception of his/her own bargaining hand; in consequence, the level of demands that an advertiser makes may vary according to what he/she has to offer (Waynforth & Dunbar 1995).

Advertisements in personal columns provide one outlet where human mate choice criteria are explicitly elaborated. Analyses of the content of such advertisements have consistently shown that the words used in these advertisements reflect a small number of key dimensions that have strong evolutionary valency (Kenrick & Keefe 1992; Wiederman 1993; Greenlees & McGrew 1994; Waynforth & Dunbar 1995; Bereczkei et al. 1997). All these studies concur that the single most important criteria by which men assess the mate quality of women is age (or, as a surrogate of this, physical attractiveness), while women tend to emphasise a wider range of criteria, including wealth/status and commitment (Borgerhof Mulder 1988a; Buss 1989; Voland & Engel 1990; Kenrick & Keefe 1992; Waynforth & Dunbar 1995; for a review of the more general literature, see Grammer 1989). Age in women is significant because it is a direct correlate of both fertility and future reproductive potential (Fisher's reproductive value).

Mating usually involves a bilateral decision of two individuals to accept each other as partners. However, depending on the species and on socio-ecological circumstances, females can differ strongly from males in how choosy they are and what principles govern their choice. In many animal species females are far more choosy than males. Evolutionary explanations of this phenomenon are typically based on the idea that competition for access to mates is stronger in males than in females. This asymmetry seems to be induced by differences in reproductive potential and, ultimately, by differences between eggs and sperm (anisogamy). Now, whenever there is strong choosiness in one sex, it pays the other sex to advertise desired properties and hide the undesired ones. Assuming that different advertisements are indeed compared by potential mating partners, the success of an advertisement will depend on how one's own signal compares to that of the competitors.

This competitive situation creates a mating market where individuals have different market values because they differ in their signalling potential. The higher an individual's market value, the larger its scope for being choosy itself. Therefore, Pawl-owski and Dunbar study the heterosexual human mating market and explore how sensitive individuals are to their own market value. By analysing written advertisements they demonstrate a positive correlation between market value and aspiration level. They also show that, with an interesting exception, advertisers behave as if they know the choice criteria of the opposite sex. This is an important requirement for the mating scene to operate as a market.

The constraints of life force every organism to behave economically. The study of economic behaviour is therefore not limited to ‘economics’. Scientific disciplines that concentrate on other aspects of human behaviour, such as psychology, sociology and anthropology, have to pay close attention to the economic decisions that drive human behaviour. The same is true for biological disciplines in which strategic options of individual organisms play a central role, notably ethology, behavioural ecology and evolutionary ecology. In order to determine in how far a behavioural strategy is ‘economical’, it has to be compared to some ideal norm: the strategy that would yield maximum payoff. In economics this norm is set by the strategy of a hypothetical ‘super-rational’ individual. For most of us the term ‘super-rational’ has a connotation of ‘very intelligent’; a strategy achieved by the use of superior cognitive capacities. Evolutionary biologists have realised, however, that even the dimmest of organisms, such as fungi and flatworms, often use ‘super-rational strategies’, because a process of selection running over a vast number of generations can shape the behaviour of every species to near perfection, as long as the circumstances in which it lives change slow enough compared to the rate of evolution. There lies the common ground between biology and economics: while Adam Smith's human producers and consumers are driven by the ‘invisible hand’ of self-interest, Charles Darwin's living organisms are driven by the selection for maximising individual fitness.

The present volume gives a number of examples of the common grounds on which economics, biology and the social sciences meet.

Introduction

Social dilemmas and the resulting problems of collective action are at the core of the study of how humans behave in interdependent situations. After an era of gloomy predictions based on the initial study of Prisoner's Dilemma (PD) games and the theory of collective ‘inaction’ (Olson 1965), recent theoretical work has made important breakthroughs for understanding human behaviour with guardedly more optimistic predictions. It is now theoretically well established that when individuals, modelled as fully rational actors, interact in an indefinitely repeated social dilemma situation, a PD game for example, it is possible for them to achieve optimal or near optimal outcomes and avoid the dominant strategies of one-shot and finitely repeated games that yield non-optimal outcomes (Aumann 1981; Fudenberg & Maskin 1986). Recent work in evolutionary game theory (Güth & Kliemt 1995; Sethi & Somanathan 1996) also identifies conditions under which cooperative behaviour backed by norms can be stable against invasion by narrow, self-interested strategies. It is also possible for individuals in social dilemma situations to do as badly round after round as is predicted for a one-shot or a finitely repeated series of situations. All potential outcomes between that produced by the dominant strategy and strategies leading to optimality are also possible equilibria. Empirical studies conducted in experimental laboratories (Ledyard 1995) and field settings (Bromley et al. 1992; Ostrom et al. 1994) provide evidence that more cooperation is achieved in social dilemma situations than the predicted zero level in one-shot or finitely repeated settings. Empirical studies of animal communities show both that the collective action problem exists in these settings and that multiple strategies are frequently found in these settings including full cooperators, conditional cooperators, full free-riders (see Nunn & Lewis this volume; and Nunn 2000).

Introduction

Models of cooperation in animal behaviour frequently address issues of cheating (also called defecting; reviewed in Dugatkin 1997). In the simplest case, cheaters gain more than cooperators because they obtain the benefits of another's action without paying the costs. Cooperation has been modelled extensively using two-player game theory models (especially the Prisoner's Dilemma; Axelrod 1984). However, these two-player models fail to capture the dynamics of cooperation in larger, polyadic social settings, which often require more complicated mathematical representations (n-player games; e.g. Joshi 1987; Boyd & Richerson 1988; Dugatkin 1990).

An empirical study by Heinsohn and Packer (1995) illustrates the difficulties of modelling cooperation in large social groups. These authors provide experimental evidence for cheating in lions by simulating territorial intrusions using playbacks. In their study, the perceived benefits of territorial defence were altered by playing back different numbers of roaring neighbours. The patterns of response suggest that female lions use one of four strategies: some females always participate (unconditional cooperators), others participate when they are most needed but not at other times (conditional cooperators), and some females never participate (unconditional laggards), or actually participate less when they are most needed (conditional laggards). Heinsohn and Packer (1995) examined whether some cooperative strategies commonly used in game theory might apply to lion cooperative territoriality (i.e. Tit-for-Tat and Pavlov; Axelrod & Hamilton 1981; Nowak & Sigmund 1993). However, these attempts were unsuccessful, probably because more complicated models are needed to represent the complex behavioural interactions expected with four strategies in a polyadic setting (Heinsohn & Packer 1995).

Threats to gorillas in the Virungas during the 20th century

Gorilla (Gorilla gorilla) populations are threatened throughout their range, primarily by human activities. As human populations increase in Africa the available room for gorillas is decreasing and gorillas are coming into contact with humans much more than they used to. Each of the three subspecies (see chapter 1 for discussion about possible changes in taxonomy), G. g .gorilla(population of about 110 000), G. g. graueri(population of about 17 000), and G .g. beringei(population of about 600) are threatened by slightly different factors that result from increasing human populations, and all gorilla populations are considered under IUCN criteria as either vulnerable or endangered (Harcourt, 1996). The major threats to gorillas can be categorized as: (1) habitat loss, modification, or fragmentation; (2) hunting or poaching; (3) disease transmission from humans; and (4) war or political unrest. The mountain gorillas in the Virungas have been exposed to each of these threats over the period during which western scientists have known about them.Despite the international publicity about these animals and despite their potential to earn foreign currency for the countries where they are found, mountain gorillas still face several of these threats. This chapter reviews the threats gorillas have faced in the Virungas over time and summarizes some of the research that has aimed to address these threats and provide information to park managers to better conserve the gorillas. We focus primarily on Rwanda and the Parc National des Volcans because the Karisoke Research Center, where most researchers have been based, is in this country.

Introduction

The importance of males to the survival of infants is argued to be a major force in the evolution of male-female association in primates (van Schaik, 1996; Palombit et al., 1997; Sterck et al., 1997; Palombit, 1999). Across taxa, however, the extent and nature of males“ interactions with immatures, especially infants, vary enormously, from intense, directed caregiving in some NewWorld monkeys like marmoset, tamarins, and titis (Wright, 1984; Goldizen, 1987), to mere tolerance with occasional affiliation as in many Old World monkeys (Whitten, 1987; Maestripieri, 1998). Differences across and within species have been linked to various functions of males interactions with infants: while in some cases they represent investment by males in related infants, usually offspring (e.g. Busse and Hamilton, 1981; Anderson, 1992), in others, males appear to be using infants as social tools, either in their competitive interactions with other males (Paul et al., 1996), or as means to gain mating access to infants-mothers (Smuts, 1985; Ferrari, 1992; van Schaik & Paul, 1996). To add to the complexity, several functions might apply in the same species. In baboons, for example, all three have been invoked to explain male-infant interactions (Packer, 1980; Smuts & Gubernick, 1992).

In considering the function of male-immature relationships researchers have examined the benefits that immmature animals gain from their associations with males. It has been argued that, for most polygynous primates, the primary contribution that males make to their offspring's fitness is protection from predators and/or infanticide by unrelated adult males (Dunbar, 1984; van Schaik, 1996; Palombit, 1999; van Schaik & Janson, 2000).