Primate Reciprocity and Its Cognitive Requirements

ArticleinEvolutionary Anthropology Issues News and Reviews 19(4):130 - 135 · July 2010with 209 Reads
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Abstract
Humans can engage in relatively indiscriminate altruistic behaviors such as donating money to charities, giving blood, and volunteering to review scientific papers. They also live in societies characterized by examples of cooperation of unmatched complexity, such as organized armies, the cooperative building of infrastructures such as roads and railways, and tax-paying, among others. (We exclude, of course, the “anonymous” societies of some social insects in which the animals themselves are not aware of the cooperative roles they play.) The emphasis on these unique aspects of our behavior1 has sometimes distracted scientists from paying attention to the more common aspects of our daily lives, which share characteristics with those of our fellow primates. We invite friends for dinner, console others after a loss, intervene in ongoing fights, and even groom others.2–4 These small acts of altruism, which constitute a large part of our daily social life, tend to resemble those of nonhuman primates.

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  • Chapter
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    A biologist studying the behavior of a species, when confronted with a seemingly costly behavior that is highly persistent in that species, would certainly entertain as her null hypothesis that this behavior is adaptive, and that the psychological mechanisms underlying it were therefore adaptations put in place by some form of natural selection. The aim of this chapter is to develop the outline of such an adaptive hypothesis (Alexander 1987) for the evolution in humans of our moral psychology, the moral emotions of which it consists, and the moral behaviors it produces. Briefly, we will propose that moral emotions are the subjective side of the proximate rules (motivations) that regulate human cooperation, which in turn is an evolutionarily novel adaptation to enable the uniquely derived lifestyle of human foragers, which requires generosity and sharing due to extreme mutual interdependence.
  • Chapter
    Reciprocal altruism provides one evolutionary explanation for cooperation, and extensive research has been conducted to discern when reciprocity occurs and the underlying proximate mechanisms. de Waal and colleagues have proposed three levels of reciprocity. Symmetry-based reciprocity is noncontingent and based on symmetries in existing relationships. Attitudinal reciprocity is contingent and based on an increased positive affective state due to recent interactions. Calculated reciprocity requires the cognitive ability to track favors given and received and has thus far only been seen in great apes (including humans). Long-term relationship structure may also play an important role in reciprocity, which may at least partly explain the relative lack of evidence for reciprocity from laboratory-based studies compared with field studies. Future studies need improved methodologies to better assess the roles of partner choice and long-term relationships in order to better discern the role that reciprocity plays in primate interactions.
  • Article
    Full-text available
    The exchange of services such as allo-grooming, allo-preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within-dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long-term positive correlation between services exchanged in animals, results for short-term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short-term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non-human primates may be little affected by recent single events. We suggest that long-term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short-term contingent events.
  • Article
    Full-text available
    Though competition and cooperation are often considered opposing forces in an arms race driving natural selection, many animals, including humans, cooperate in order to mitigate competition with others. Understanding others' psychological states, such as seeing and knowing, others' goals and intentions, and coordinating actions are all important for complex cooperation—as well as for predicting behavior in order to take advantage of others through tactical deception, a form of competition. We outline evidence of primates' understanding of how others perceive the world, and then consider how the evidence from both deception and cooperation fits this framework to give us a more complete understanding of the evolution of complex social cognition in primates. In experimental food competitions, primates flexibly manipulate group-mates' behavior to tactically deceive them. Deception can infiltrate cooperative interactions, such as when one takes an unfair share of meat after a coordinated hunt. In order to counter competition of this sort, primates maintain cooperation through partner choice, partner control, and third party punishment. Yet humans appear to stand alone in their ability to understand others' beliefs, which allows us not only to deceive others with the explicit intent to create a false belief, but it also allows us to put ourselves in others' shoes to determine when cheaters need to be punished, even if we are not directly disadvantaged by the cheater.
  • Article
    Full-text available
    Reciprocity (or ―reciprocal altruism‖) was once considered an important and widespread evolutionary explanation for cooperation, yet many reviews now conclude that it is rare or absent outside of humans. Here, I show that nonhuman reciprocity seems rare mainly because its meaning has changed over time. The original broad concept of reciprocity is well supported by evidence, but subsequent divergent uses of the term have relied on various translations of the strategy ‗tit-for-tat‘ in the repeated Prisoner‘s Dilemma game. This model has resulted in four problematic approaches to defining and testing reciprocity. Authors that deny evidence of nonhuman reciprocity tend to (1) assume that it requires sophisticated cognition, (2) focus exclusively on short-term contingency with a single partner, (3) require paradoxical evidence for a temporary lifetime fitness cost, and (4) assume that responses to investments are fixed. While these restrictions basically define reciprocity out of existence, evidence shows that fungi, plants, fish, birds, rats, and primates enforce mutual benefit by contingently altering their cooperative investments based on the cooperative returns, just as predicted by the original reciprocity theory.
  • Article
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    A large body of evidence suggests that female Old World monkeys maintain selective long-term grooming interactions with fitness benefits. The last two decades have produced evidence that the regulation of social interactions among primates can be, in part, explained by the Biological Markets theory, with grooming behaviour as the focus of these studies. Grooming facilitates bonding between individuals, constituting an essential part of the regulation of social relationships among female cercopithecids. In contrast to the well-studied baboons (Papio spp), knowledge about the nature of grooming interactions and their regulation is generally lacking for the large, terrestrial species of mandrills (Mandrillus sphinx). We used a combination of social network analysis tools and well-established methods for assessing partner diversity and reciprocity to characterise grooming networks, partner choice and patterns of trade (be groomed, give grooming) among females in a captive group of mandrills, both within and across two separate observation periods. Our results suggest that, even though the relatively stable conditions of captivity allowed the studied females to maintain selective grooming interactions across time, small scale demographic changes affected the grooming dynamics of the group in accordance with the expectations of the Biological Markets theory. In particular, the maturation and consequent integration of a high ranking female into the group's grooming network from one period to the next resulted in a more pronounced effect of rank on the regulation of grooming interactions. In addition, the influence of the maturation of a dependent infant on the grooming interactions of his mother were evident between periods. Our results also demonstrate that grooming networks are dynamic and that high ranking individuals are not necessarily the most central in grooming networks. Finally, we discuss the potential of social network analysis to identify cases of social exclusion and its consequences for captive management.
  • Article
    Biological Market Theory (BMT) has provided an elegant framework to study how commodities are exchanged among individuals. In primates, BMT predicts that individuals exchange grooming with other commodities based on the law of supply and demand. However, BMT still suffers some theoretical and methodological limitations. Our aim in this paper is to discuss some of these limitations, including the lack of consensus over the time frame in which exchanges take place, and over the commodities involved, the cognitive challenges imposed by biological markets (BMs), and the heterogeneity of methods used to test BMT across studies. In particular, we discuss (1) the importance of predetermining both the time frame over which exchanges take place and (2) the commodities that are exchanged in primate BMs, (3) the cognitive skills that primates need to navigate in a BM, and (4) other methodological issues arising when testing BMT. For each of these points, we propose an agenda with possible solutions and we show how the issues raised also apply to BMs in species other than primates.
  • Article
    Full-text available
    The explanations for a rapid dispersal of modern humans after 100,000 BP remain enigmatic. Populations of modern humans took new routes – crossing significant topographic and environmental barriers, including making major sea crossings, and moving into and through risky and difficult environments. Neither population increase nor ecological changes provide an adequate explanation for a pattern of rapid movement, including leaping into new regions (saltation events). Here it is argued that the structural dynamics of emotionally complex collaboration and in depth moral commitments generates regular expulsion events of founding populations. These expulsion events provide an explanation for the as yet elusive element to dispersal. Alongside cognitive and cultural complexity we should recognise the influence of emerging emotional complexity on significant behavioural changes in the Palaeolithic.
  • Chapter
    Is moral behavior unique to humans? Although moral behavior is primarily discussed in relation to humans, if a function of moral behavior is to promote social cohesion and harmony within a social group, there is no a priori reason not to expect a similar set of behaviors in other social species (Bonnie and de Waal 2004; Flack and de Waal 2000; Haidt 2003). Although this certainly does not mean that what we see in other species need be identical to humans’ behavior, there may be a suite of related behaviors that have evolved for the same purposes in other species. Of course, this idea is not new. In The Descent of Man and Selection in Relation to Sex (Darwin 1871/1981: 71–72), Darwin argued that sociality is innate, rather than created by humankind, and provided a framework for the development of morality in any species. The question is, then, from which precursor behaviors did morality evolve, and how can we study this in other species?
  • Article
    Nepotism and reciprocity are not mutually exclusive explanations for cooperation, because helping decisions can depend on both kinship cues and past reciprocal help. The importance of these two factors can therefore be difficult to disentangle using observational data. We developed a resampling procedure for inferring the statistical power to detect observational evidence of nepotism and reciprocity. We first applied this procedure to simulated data sets resulting from perfect reciprocity, where the probability and duration of helping events from individual A to B equalled that from B to A. We then assessed how the probability of detecting correlational evidence of reciprocity was influenced by (1) an increasing number of helping observations and (2) an increasing degree of simultaneous nepotism. Last, we applied the same analyses to empirical data on food sharing in common vampire bats, Desmodus rotundus, and allogrooming in mandrills, Mandrillus sphinx, and Japanese macaques, Macaca fuscata. We show that at smaller sample sizes, the effect of kinship was easier to detect and overestimated relative to the effect of reciprocal help. This bias in power was true in both empirical and simulated data, including when simulating perfect reciprocity and imperfect nepotism. We explain the causes and consequences of this difference in power for detecting the roles of kinship versus reciprocal help. When comparing the relative evidence for kin-biased help and reciprocal help, we suggest that researchers measure the relative reliability of both kinship bias and symmetry in the model by plotting the coefficients and their detection probability as a function of sampling effort. We provide R scripts to allow others to do this power analysis with their own data sets.
  • Article
    It is often (implicitly) assumed that the expectation of reciprocation motivates animal altruism, and thus that animals “plan” their social interactions. We tested this hypothesis by studying a captive group of mandrills (Mandrillus sphinx). In our focal group, the alpha male was more likely to provide agonistic support in the minutes after the receipt of grooming than in the absence of previous grooming. This offered other group members the possibility of manipulating the male’s support by grooming him before engaging in an aggression. We used survival analysis to test the hypothesis that the other group members systematically groomed the alpha male just before engaging in aggression, which would suggest that the expectation of reciprocation motivated their grooming. Contrary to the prediction of our hypothesis, we found that other group members did not groom the alpha male just before engaging in aggression, and thus did not benefit from increased support from the most effective ally. These results suggest that mandrills do not plan their social interactions and that the expectation of reciprocation does not motivate them to groom. KeywordsAggression–Grooming– Mandrillus sphinx –Proximate causation–Reciprocation
  • Article
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    Imagine an individual called "hunter" that expends a good deal of energy to capture a gazelle. As the hunter is consuming his small prey, a second individual called "recipient" approaches and begins feeding peacefully alongside the hunter. A few weeks later the roles reverse, such that the previous recipient has now captured a gazelle, and the previous hunter is taking advantage of the recipient's hard work. Could the hunter and recipient be Maasai warriors? Is it equally likely that they are common chimpanzees, African lions, or Nile crocodiles? All of these species hunt gazelle and live in groups, so why would this scenario apply to some species more appropriately than to others? The answer lies in the costs and benefits associated with sharing food with non-kin. Assuming that one individual can consume the entire gazelle, sharing food with the recipient constitutes an altruistic act-the hunter accepts a fitness cost (reduction in food intake) while increasing the fitness of another (increasing the intake of the recipient).
  • Article
    Data on a large sample of interventions that individuals in two mountain gorilla (Gorilla gorilla beringei) groups made in agonistic interactions between others corroborate and extend earlier analyses in several ways. Related females supported each other as often as those in some female-bonded primates and maintained alliances while they resided together. Most unrelated females rarely supported each other, but some developed alliances. Females mostly supported other females with whom they had affinitive relationships against those they often engaged in dyadic aggression. They showed reciprocity in support, and often intervened against individuals who, in turn, often intervened against them. But even female coalitions that outnumbered their opponents by more than two-to-one had limited effectiveness, largely because males intervened in many female contests to control aggression. By rendering coalitions ineffective, males contribute to a combination of factors (e.g. low potential to gain from cooperation in contest feeding competition) that limit the benefits of female philopatry. Male curtailment of female aggression may influence female mate choice. Co-resident mature males in the study groups competed to control female aggression. High-ranking males curtailed aggression to females by subordinates, although two males formed an alliance against two others in their group. Immature animals mostly received defensive support against larger individuals and did not receive support from adults that could lead to a nepotistic dominance system.
  • Article
    Current socioecological models argue that multi-female primate groups engaging in cooperative, between-group resource competition (BGC), should have egalitarian social relations that promote cohesion among group members, while those that experience strong within-group competition (WGC) should exhibit nepotistic and despotic social behaviour (van Schaik, 1989; Sterck et al., 1997). Here we investigate the idea that very slight WGC can have strong effects on social relationships, even in 'egalitarian' populations, and that individual responses to ecological conditions may vary among group members. We estimated the intensity of both BGC and WGC and used the Biological Markets model to examine their effects on female dominance and grooming distributions for a group of samango monkeys (Cercopithecus mitis erythrarchus) in a high-density, territorial population. We found high levels of territorial activity consistent with female resource defence, low levels of within-group aggression and only slight effects of contest competition on diet. Individual grooming bouts were reciprocal, with no effects of rank, demonstrating that grooming was not exchanged for feeding tolerance. However, in contrast to other C. mitis populations, female samangos maintained a consistent, linear dominance hierarchy that was reflected in the overall patterns of association and grooming, with high-ranking females receiving more grooming, and lower-ranking females were less likely to take part in territorial activity. Our results support the prediction of the current socioecological model that WGC effects on female relationships will always be greater than the cohesive effects of BGC (Wrangham, 1980; Cheney, 1992), and show that a simple 'egalitarian' description of C. mitis female relationships is insufficient.
  • Article
    Evidence is presented that the reciprocal exchange of social services among chimpanzees (Pan troglodytes) rests on cognitive abilities that allow current behavior to be contingent upon a history of interaction. Food sharing within a captive colony of chimpanzees was studied by means of 200 food trials, conducted on separate daus over a 3-year period, in which 6,972 approaches occurred among the nine adults in the colony. The success rate of each adult, A, to obtain food from another adult, B, was compared with grooming interactions between A and B in the 2 hours prior to each food trial. The tendency of B to share with A was higher if A had groomed B than if A had not done so. The exchange was partner-specific, i.e., the effect of previous grooming on the behavior of food possessors was limited to the grooming partner. Grooming did not affect subsequent sharing by the groomer, only by the groomee. The effect of grooming was greatest for pairs of adults who rarely groomed. Nevertheless, the effect was general: 31 dyadic directions showed an increase in sharing following grooming, and only 11 a decrease. Food possessors actively resisted approaches by individuals who had not groomed them. After food trials there was a significant reduction of grooming by previous possessors towards those individuals with whom they had shared.
  • Article
    This chapter discusses the dynamics of cooperation in primate groups; reviews observational and experimental evidence about turn‐taking, collaboration, and coordination in primate groups; and describe four gametheoretic models in which individuals can benefit from providing help to others, arguing that the formal payoff structures derived from these models provide a clear and cogent framework for understanding the processes underlying various types of cooperative interactions. It also focuses on the situations in which animals must work together to achieve a joint reward—a situation that corresponds loosely to the payoff structure of the Stag Hunt model.
  • Article
    Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged. Ecology Letters (2010) 13: 45–50
  • Article
    In this study, we examined the time frame of reciprocal partner choice in the grooming interactions of captive mandrills (Mandrillus sphinx) in order to test the hypothesis that the cognitive limitations of primates constrain the occurrence of reciprocation to short time intervals. In contrast to this hypothesis, mandrills groomed preferentially those individuals that groomed them more even when cases of immediate reciprocation were excluded from the analysis. These results show that mandrills were not limited to reciprocating grooming over short time intervals. It is proposed that a system of emotional bookkeeping may support the ability of primates to reciprocate over long time frames.
  • Article
    People feel grateful when they have benefited from someone's costly, intentional, voluntary effort on their behalf. Experiencing gratitude motivates beneficiaries to repay their benefactors and to extend generosity to third parties. Expressions of gratitude also reinforce benefactors for their generosity. These social features distinguish gratitude from related emotions such as happiness and feelings of indebtedness. Evolutionary theories propose that gratitude is an adaptation for reciprocal altruism (the sequential exchange of costly benefits between nonrelatives) and, perhaps, upstream reciprocity (a pay-it-forward style distribution of an unearned benefit to a third party after one has received a benefit from another benefactor). Gratitude therefore may have played a unique role in human social evolution.
  • Article
    Social relationship is a concept that links the observable social interactions between group members to the inferred group social system. Social relationships allow animals (as well as the human observers) to predict the actions and responses of their partners and therefore guide their own. Social relationships can also be described as investments that benefit the individuals involved in them. Some benefits simply require stable association and some level of mutual tolerance, whereas others depend on the establishment of more fully developed social relationships. The variation in the quality of social relationships leads to a great flexibility in the frequency and quality of interaction with various group members and with the same individual over time. A key issue is therefore to understand the proximate mechanisms underlying such flexibility since individuals need to be able to assess relationship quality in order to maximise the benefits that social relationships provide. Assessment of social relationships should be based on the information contained in the various interactions that the partners exchange. Assessment should therefore require bookkeeping of the various interactions, computation of their relative frequencies, and conversion of their quality and information associated with them into common currencies. We propose emotional mediation as a possible mechanism that fulfils such requirements and provides the individual with a timely assessment to guide its social decision. Emotions are viewed as intervening variables that result from the integration of the information contained in the various interactions between two partners. Before presenting evidence for relationship assessment through emotional mediation, we define the concept of emotion in animals and provide evidence for measuring relevant emotions in non-human primates. Then, we present four examples obtained by combining findings from multiple studies. The examples provide evidence for emotion resulting from information contained in the interactions exchanged by the partners and for emotional differences being at the basis of the variation in social interactions. Thus, animals may appreciate variation in their social relationships through emotional mediation. This is a promising avenue to disclose the proximate mechanisms of relationship assessment and we suggest new lines of research to gather further evidence for the role of emotional mediation.
  • Article
    Full-text available
    McCullough, Kilpatrick, Emmons, and Larson (2001) posited that gratitude prompts individuals to behave prosocially. However, research supporting the prosocial effect of gratitude has relied on scenario and self-report methodology. To address limitations of previous research, this experiment utilised a laboratory induction of gratitude, a method that is potentially more covert than scenarios and that elicits actual grateful emotion. Prosocial responses to gratitude—operationalised as the distribution of resources to another—were paired with a self-report measure of gratitude to test the prosocial effect of gratitude. To investigate positive mood as an alternative explanation, this experiment compared responses of individuals receiving a favour to responses of individuals receiving a positive outcome by chance. A total of 40 participants were randomly assigned to either a Favour or Chance condition. Participants receiving a favour helped more and reported more gratitude compared to participants in the Chance condition.
  • Article
    ALTRUISM is behaviour that benefits another individual at some cost to the altruist, costs and benefits being measured in terms of individual fitness. ‘Reciprocal altruism’ (ref. 1) implies the exchange of altruistic acts between unrelated individuals as well as between relatives. If the benefits to the recipient of an altruistic act exceed the costs to the altruist, and if the recipient is likely to reciprocate at a later time, then the cumulative benefits for both individuals will have exceeded the cumulative costs of their altruism. Natural selection would favour individuals that engaged in reciprocal altruism if they distributed their altruism with respect to the altruistic tendencies of the recipient, preferring individuals that were most likely to reciprocate and excluding nonaltruists from the benefits of further altruism. This model has been difficult to test because it is usually impossible to be certain that an example of altruism is not the product of ‘kin selection’2. The genetic relationships between individuals in animal populations are seldom known and reciprocal altruism can only be cited when it can be found to occur regularly between unrelated individuals. I report here that altruistic behaviour involving the formation of coalitions among male olive baboons (Papio anubis) fulfils the criteria for reciprocal altruism.
  • Article
    Studied interchange of support for being groomed by giving individual long-tailed macaques the opportunity to support others under 3 conditions: being groomed by the other, after grooming the other, and without prior grooming. Results provided direct evidence that after being groomed recently by another, a monkey is more likely to support its groomer than without prior grooming. Results concern aggressor support only, since victim support did not occur. The tendency to support others was not increased by any grooming interaction. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
  • Article
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    A model is presented to account for the natural selection of what is termed reciprocally altruistic behavior. The model shows how selection can operate against the cheater (non-reciprocator) in the system. Three instances of altruistic behavior are discussed, the evolution of which the model can explain: (1) behavior involved in cleaning symbioses; (2) warning cries in birds; and (3) human reciprocal altruism. Regarding human reciprocal altruism, it is shown that the details of the psychological system that regulates this altruism can be explained by the model. Specifically, friendship, dislike, moralistic aggression, gratitude, sympathy, trust, suspicion, trustworthiness, aspects of guilt, and some forms of dishonesty and hypocrisy can be explained as important adaptations to regulate the altruistic system. Each individual human is seen as possessing altruistic and cheating tendencies, the expression of which is sensitive to developmental variables that were selected to set the tendencies at a balance ap...
  • Article
    Full-text available
    1Animals can derive leverage over others from (a) resource holding power, based for instance on fighting ability or dominance, and (b) the possession of commodities, such as special skills and resources that cannot be taken away by force.2We contend that power based on the possession of commodities strongly depends on the level of supply and demand for that commodity, a phenomenon we call the ‘market effect’.3Several theoretical and empirical examples are given of social systems in which animals belong to two distinct classes that offer two different kinds of commodities.4The relative frequency of occurrence of the two classes is shown to determine the relative power of their members.5We consider the theoretical properties of bargaining processes by which relative power is converted into corresponding pay-off distributions.6We propose coalition games, a class of games with more than two players and in which bargaining is possible, as suitable paradigms for collaboration among members of social units.
  • Article
    Full-text available
    Cooperation is common across nonhuman animal taxa, from the hunt-ing of large game in lions to the harvesting of building materials in ants. Theorists have proposed a number of models to explain the evolution of cooperative behavior. These ultimate explanations, however, rarely consider the proximate constraints on the im-plementation of cooperative behavior. Here we review several types of cooperation and propose a suite of cognitive abilities required for each type to evolve. We propose that several types of cooperation, though theoretically possible and functionally adaptive, have not evolved in some animal species because of cognitive constraints. We argue, therefore, that future modeling efforts and experimental investigations into the adaptive function of cooperation in animals must be grounded in a realistic assessment of the psychological ingredients required for cooperation. Such an approach can account for the puzzling distribution of cooperative behaviors across taxa, especially the seemingly unique occurrence of cooperation observed in our own species.
  • Article
    The scarcity of evidence for contingent reciprocity has led to a growing interest in how market forces shape the distribution of exchanges in animal groups. In a biological market, supply and demand determines the value of an exchange, and individuals choose to trade with the partner offering the highest value. Partners maximize their immediate benefits without the need to monitor the balance of their exchange over time. Applied to grooming exchanges in primate groups, a market model predicts that females will primarily balance the amount of grooming they trade within single bouts, particularly when all partners offer similar value. If some partners can offer other benefits, like reduced aggression, females may exchange grooming for those benefits. In such cases, grooming will not be evenly balanced within bouts. Here, we examine the patterning of grooming in a group of free-ranging olive baboons (Papio anubis). In contrast to predictions derived from a biological market model, two-thirds of all grooming bouts in this group were completely one-sided and females did not consistently provide more grooming to higher-ranking partners. Grooming was more evenly balanced across multiple bouts than within single bouts, suggesting that females are not constrained to complete exchanges within single transactions.
  • Article
    Recent theoretical and experimental studies argued that reciprocity is constrained by the cognitive limitations of most animals and that, when reciprocation occurs, it should necessarily be short term. In this study, we examined the time frame of partner choice in the reciprocal grooming of captive female tufted capuchin monkeys (Cebus apella). Female capuchins groomed preferentially those individuals that overall groomed them most. Tufted capuchins did sometimes reciprocate grooming immediately. We quantified the time course and probability of immediate reciprocation, and excluded from the analysis cases of immediate reciprocation. We then showed that, even excluding immediate reciprocation, female capuchins still preferred to groom those individuals that groom them most. Our results show that partner choice is not necessarily based on immediate reciprocation and suggest that capuchins are able to reciprocate over longer time frames. These findings argue against the hypothesis that long-term reciprocation is absent in species lacking sophisticated cognitive abilities. We suggest that reciprocal altruism over long time frames relies on a system of emotional bookkeeping.
  • Article
    Despite its widespread practice among primates writ large, social scientists have given mutual grooming among humans little attention. This research provides an important first step in describing mutual grooming among humans. A scale was developed to measure self-reported giving and receiving of grooming. In Study 1, 184 female and 94 male participants first indicated their closest emotional relationship (for example, romantic partner, best friend, etcetera). They then completed the grooming measure pertaining to that emotionally close target person. Finally, they completed indices of relationship trust, relationship satisfaction, and parental/familial affection. Individuals who focused on their romantic partners (N = 134) reported more mutual grooming than individuals who focused on other types of relationships. Relationship satisfaction, previous experience of familial affection, and trust were positively correlated with mutual grooming for romantically involved individuals. Study 2 (N = 71 heterosexual couples) explored psychological correlates of mutual grooming within romantic dyads. Individuals with more promiscuous attitudes and those who scored high on the anxiety subscale of an adult attachment style measure reported grooming their partners most frequently. Findings were consistent with several proposed functions of grooming: (a) potential parental-investment indicator, (b) developing trust, and (c) courtship/flirtation—all of which play roles in pair-bonding. At first glance, humans may not appear to groom each other with the same fervor as other primates. However, we posit that humans are, in actuality, groomers par excellence.
  • Article
    Full-text available
    The study of reciprocal altruism, or the exchange of goods and services between individuals, requires attention to both evolutionary explanations and proximate mechanisms. Evolutionary explanations have been debated at length, but far less is known about the proximate mechanisms of reciprocity. Our own research has focused on the immediate causes and contingencies underlying services such as food sharing, grooming, and cooperation in brown capuchin monkeys and chimpanzees. Employing both observational and experimental techniques, we have come to distinguish three types of reciprocity. Symmetry-based reciprocity is cognitively the least complex form, based on symmetries inherent in dyadic relationships (e.g., mutual association, kinship). Attitudinal reciprocity, which is more cognitively complex, is based on the mirroring of social attitudes between partners and is exhibited by both capuchin monkeys and chimpanzees. Finally, calculated reciprocity, the most cognitively advanced form, is based on mental scorekeeping and is found only in humans and possibly chimpanzees.
  • Article
    Full-text available
    Although human behaviour abounds with reciprocal altruism, few examples exist documenting reciprocal altruism in animals. Recent non-experimental evidence suggests that reciprocal altruism may be more common in nature than previously documented. Here we present experimental evidence of mobbing behaviour, the joint assault on a predator in an attempt to drive it away, as reciprocal altruism in the breeding pied flycatcher (Ficedula hypoleuca). Given a choice, pied flycatchers assisted in mobbing initiated by co-operating neighbours and did not join in mobbing when initiated by conspecific neighbours which had defected from necessary assistance 1h before. The results suggest the birds followed a ‘tit-for-tat’-like strategy and that mobbing behaviour of breeding birds may be explained in terms of reciprocal altruism.
  • Article
    Full-text available
    We investigated the temporal relationship between grooming given and agonistic support received in a group of chimpanzees at Chester Zoo, U.K. We compared grooming levels the day before a conflict-with-support to those the day before a conflict-without-support and to baseline to investigate whether individuals groom potential supporters in anticipation of the need for support. We also compared grooming and aggression levels the day after conflicts-with-support to levels the day after conflicts-without-support and to baseline levels to determine whether chimpanzees reward individuals that support them or punish those that do not. Finally, we compared grooming and aggression levels the day after conflicts-with-unsuccessful-solicitations-for-support to those the day after conflicts-with-support and to baseline to examine the behavioral consequences of not providing support when an individual had solicited but did not receive it. Future recipients of support groomed future supporters more the day before receiving support, compared to the day before conflicts-without-support, indicating that grooming increased the likelihood of support. The relationship between prior grooming and support held true only for aggressor and not victim support and is consistent with behavior expected if chimpanzees anticipated the need for agonistic support and groomed their supporter the day before to increase the likelihood of support. We found evidence of a system of reward and punishment. Individuals experienced significantly lower rates of aggression after conflicts in which they provided support than at baseline and after conflicts in which they did not provide support. The finding was true only for aggressor support. We found no evidence that chimpanzees punished individuals whom or that they unsuccessfully solicited with aggression or a reduction in grooming. However, solicitors groomed individuals that they solicited for support significantly more after unsuccessful solicitations than after individuals provided support (but with no difference from baseline), indicating that individuals may attempt to recement their relationship after an unsuccessful solicitation. The findings are consistent with a mechanism of calculated interchange in chimpanzees.
  • Article
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    The formation of collaborating pairs by individuals belonging to two different classes occurs in the contexts of reproduction and intea-specific cooperation as well as of inter-specific mutualism. There is potential for partner choice and for competition for access to preferred partners in all three contexts. These selective forces have long been recognised as important in sexual selection, but their impact is not yet appreciated in cooperative and mutualistic systems. The formation of partnerships between members of different classes has much in common with the conclusion of trade agreements in human markets with two classes of traders, like producers and consumers, or employers and employees. Similar game-theoretical models can be used to predict the behaviour of rational traders in human markets and the evolutionarily stable strategies used in biological markets. We present a formal model in which the influence of the market mechanism on selection is made explicit. We restrict ourselves to biological markets in which: (1) Individuals do not compete over access to partners in an agonistic manner, but rather by outcompeting each other in those aspects that are preferred by the choosing party. (2) The commodity the partner has to offer cannot be obtained by the use of force, but requires the consent of the partner. These two restrictions ensure a dominant role for partner choice in the formation of partnerships. In a biological market model the decision to cooperate is based on the comparison between the offers of several potential partners, rather than on the behaviour of a single potential partner, as is implicitly assumed in currently accepted models of cooperation. In our example the members of one class A offer a commodity of fixed value in exchange for a commodity of variable value supplied by the other class, B. We show that when the B-class outnumbers the A-class sufficiently and the cost for the A-class to sample the offers of the B-class are low, the choosiness of the A-class will lead to selection for the supply of high value commodities by the B-class (Fig. 3a). Under the same market conditions, but with a high sampling cost this may still be the evolutionariy stable outcome, but another pair of strategies proves to be stable too: relaxed choosiness of class A coupled with low value commodities supplied by class B (Fig. 3b). We give a number of examples of mating, cooperative and mutualistic markets that resemble the low sampling cost situation depicted in Fig. 3a.
  • Article
    Agonistic intervention behavior was observed in captive groups of chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and stumptail monkeys (M. arctoides). Reciprocity correlations of interventions were determined while removing from the data the effects of several symmetrical relationship characteristics, that is, matrillineal kinship, proximity relations, and same-sex combination. It was considered likely that if significant reciprocity persisted after controlling for these characteristics, the reciprocity was based on cognitive mechanisms. Statistical significance was tested by means of recently developed matrix permutation procedures. All three species exhibited significant reciprocity with regard to beneficial interventions, even after controlling for symmetrical traits. Harmful interventions were, however, reciprocal among chimpanzees only. This species showed a “revenge system”, that is, if A often intervened against B, B did the same to A. In contrast, both macaque species showed significantly inversed reciprocity in their harmful interventions: if A often intervened against B, B rarely intervened against A. Further analysis indicates that the strict hierarchy of macaques prevents them from achieving complete reciprocity. Compared to chimpanzees, macaques rarely intervene against higher ranking group members. The observed contrast can be partially explained on the basis of differences in available space, as indicated by a comparison of indoor and outdoor living conditions for the chimpanzee colony. Yet, even when such spatial factors are taken into account, substantial behavior differences between chimpanzees and macaques remain.
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    Male savanna baboons, Papio cynocephalus, form coalitions with each other as a technique for gaining access to a female in consort with another male. Reciprocal altruism has been invoked as the primary mechanism which underlies this reproductive tactic, but a 19-month field study of the reproductive behaviour of olive baboons, P. c. anubis, in Kenya contradicted this interpretation. Males who solicited others for coalition formation were not more likely to gain access to consort females than were their fellow coalition members. Males who refused to participate in a coalition at one time were still sought as coalition partners at other times by the same male. Coalitions were generally formed by older, middle- to lower-ranking males and targeted at younger, higher-ranking males. Coalitions are a low risk reproductive tactic and the benefits are not partitioned according to initiator/joiner status. Coalitions are likely to be an outcome of cooperation between males which results from the pursuit of self-interest.
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    Over the last two decades a large number of experiments have been conducted in which two conspecifics, mainly vertebrates, could obtain rewards through cooperation. At least three different motivations to perform such experiments can be distinguished: (1) detecting the mechanistic basis of naturally occurring forms of cooperation; (2) analysing behavioural strategies specific to cooperation; and (3) testing game-theoretical models. Experimenters in the latter two categories, on which this review concentrates, make use of highly artificial devices. The impression of cooperation in the third category is created because two animals are tested simultaneously after having been trained to interact with an apparatus individually before the experiment. These results can be explained most parsimoniously as the product of instrumental (‘trial-and-error’) learning, hence my label ‘instrumental cooperation’. The underlying philosophy of several studies is reminiscent of the strongly disputed ideas of the ‘behaviourist school’. Results from experiments in the second category highlight the importance of communication; therefore I call this ‘communicative cooperation’. The crucial role of communication identified by studies in the second category calls into question the relevance of the most popular paradigm used in the third category, the two-player Iterated Prisoner's Dilemma. Its stringent conditions, which are hardly ever fulfilled in nature, are very difficult to fulfil in experiments too. I propose that future studies concentrate on experiments that emphasize the role of communication and partner choice with the aim of explaining the emergence and maintenance of naturally occurring forms of cooperation.
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    Seyfarth (1977, Journal of Theoretical Biology,65, 671–698) proposed a model of social grooming among female monkeys that has had an enormous influence in the primatological literature. To test this model, I reviewed published data on primate grooming behaviour, using meta-analytical techniques. An analysis of grooming behaviour in 27 different social groups belonging to 14 different species revealed that a significant role in the distribution of grooming was played by attraction to high-ranking animals, attraction to kin and competition for grooming partners. These results confirm the majority of the predictions of the model. The need for more observational data on grooming (and other affiliative interactions) in New World monkeys, and experimental data on the relations between the exchange of grooming and the formation of agonistic alliances, is emphasized.
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    According to a widely accepted paradigm, cooperation among animals resembles an iterated, two-player Prisoner's Dilemma game. In this symmetrical game the two players have equivalent strategic options. Decisions are based only on information obtained in similar interactions with the same player in the past. The Prisoner's Dilemma model ignores the social organization within which cooperation occurs. This paper advocates a set of alternative models based on N-player coalition games that apply especially to collaboration (that is, cooperation and reciprocity) within social groups. The model takes into account the effect of competition for the favours of suitable partners. In Coalition games negotiations are possible and the strategic options of the players can be unequal. An example of a Coalition game, the Veto game, is illustrated by patterns of coalition formation among adult males in a group of wild baboons Papio c. cynocephalus.
  • Article
    The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5–7% of macaque grooming bouts, and 12–27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.
  • Article
    This paper reviews recent work on reciprocal altruism in primates with the aim of highlighting the roles that reciprocal partner choice may have had in the evolution of primate altruism, and that emotions may play in supporting primates' ability to exert such reciprocal partner choice. Individual studies and meta‐analyses show that primates reciprocate a variety of behaviors that benefit other individuals (be they altruistic or mutualistic). These behaviors include grooming, agonistic support, and food sharing. Analyses of the time frame of these reciprocal exchanges suggest primates deploy their altruistic behaviors among group mates on the basis of long‐term accounts of altruism received, and are thus not constrained to immediate reciprocation. We argue that a system of emotional bookkeeping of benefits received may be at the basis of primate reciprocation. This hypothesis is consistent with behavioral data and with our current knowledge about primate cognitive abilities and the neurobiological correlates of affiliative behaviors. Investigations of the role that emotions play in the social life of primates may help us bridging the gap between the apparent complexity of their social life and the relative simplicity of their cognitive abilities.
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    In biological markets, two classes of traders exchange commodities to their mutual benefit. Characteristics of markets are: competition within trader classes by contest or outbidding; preference for partners offering the highest value; and conflicts over the exchange value of commodities. Biological markets are currently studied under at least three different headings: sexual selection, intraspecific cooperation and interspecific mutualism. The time is ripe for the development of game theoretic models that describe the common core of biological markets and integrate existing knowledge from the separate fields.
  • Article
    The growing number of empirical studies performed in ecology and evolution creates a need for quantitative summaries of research domains to generate higher-order conclusions about general trends and patterns. Recent developments In meta-analysis (the area of statistics that is designed for summarizing and analyzing multiple independent studies) have opened up new and exciting possibilities. Unlike more traditional qualitative and narrative reviews, meta-analysis allows powerful quantitative analyses of the magnitude of effects and has a high degree of objectivity because it is based on a standardized set of statistical procedures. The first pioneering applications in ecology and evolution demonstrate that meta-analysis is both tractable and powerful.
  • Article
    Grooming and agonistic support are 2 common primate behaviors that have been hypothesized to constitute examples of reciprocal altruism. In particular, because primates often direct their grooming up the dominance hierarchy, it has been suggested that they may exchange grooming for agonistic support. Empirical tests of this hypothesis have resulted in highly inconsistent findings. I synthesized the published literature on the relation between grooming and agonistic support in primates using modern meta-analytical techniques. A meta-analysis of 36 studies carried out on 14 different species showed that a significant positive relation exists between grooming and agonistic support (weighted average r = 0.154, corrected for publication bias). These findings suggest that grooming and agonistic support may have evolved as part of a system of low-cost reciprocal altruism. They also highlight the potential of meta-analysis in tackling the study of behavioral phenomena characterized by low overall frequency and small effect sizes.
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    Grooming among female Japanese macaques (Macaca fuscata) was studied to test some predictions derived from the application of biological market theory. Contrary to expectations, Japanese macaques did not time match the duration of grooming episodes, their degree of reciprocation was not related to rank distance, and they did not distribute their immediately reciprocated and nonreciprocated grooming in different ways. However, they did reciprocate total amount of grooming received. These results suggest that the use of the temporal patterning of grooming (immediately reciprocated versus nonreciprocated grooming) to distinguish the different classes of traders predicted by the theory (reciprocal versus interchange traders) is unsuccessful. Copyright 2003.
  • Article
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    Primate female allogrooming models based on biological markets theory predict that grooming is "time matched" within bouts, that is, the amount of time the first female grooms predicts the amount of time the second one grooms. The models also predict that when female--female contest competition is weak, grooming is traded for grooming, but when female--female contest competition is strong, grooming may be traded for other commodities such as feeding tolerance, and grooming discrepancy between members of dyads is rank related. We tested these predictions using data collected from adult and subadult female gray-cheeked mangabeys (Lophocebus albigena) (N = 26) in 5 groups in Kibale National Park, Uganda. We found that, overall, females reciprocated in 33% of grooming bouts. Among reciprocated bouts, females in all 5 groups showed time matching. In 2 groups, we also found rank-related grooming discrepancies but showing opposite patterns to each other. Consistent with predictions based on biological markets theory, these groups may have been under greater feeding competition, revealed more by adjustments in ranging behavior than increased agonistic rates. Although these results support current allogrooming models, they also suggest that the models may become more robust if the influence of scramble competition is incorporated. In addition, they emphasize the flexibility and dynamic nature of female competitive relationships within the same population of primates. Copyright 2009, Oxford University Press.
  • Article
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    Animals neither negotiate verbally nor conclude binding contracts, but nevertheless regularly exchange goods and services without overt coercion and manage to arrive at agreements over exchange rates. Biological market theory predicts that such exchange rates fluctuate according to the law of supply and demand. Previous studies showed that primates pay more when commodities become scarcer: subordinates groomed dominants longer before being tolerated at food sites in periods of shortage; females groomed mothers longer before obtaining permission to handle their infants when there were fewer newborns and males groomed fertile females longer before obtaining their compliance when fewer such females were present. We further substantiated these results by conducting a 2-step experiment in 2 groups of free-ranging vervet monkeys in the Loskop Dam Nature Reserve, South Africa. We first allowed a single low-ranking female to repeatedly provide food to her entire group by triggering the opening of a container and measured grooming bouts involving this female in the hour after she made the reward available. We then measured the shifts in grooming patterns after we added a second food container that could be opened by another low-ranking female, the second provider. All 4 providers received more grooming, relative to the amount of grooming they provided themselves. As biological market theory predicts, the initial gain of first providers was partially lost again after the introduction of a second provider in both groups. We conclude that grooming was fine-tuned to changes in the value of these females as social partners.
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    We argue that grooming is a commodity that female primates can trade, either for itself or in exchange for other services (sensu biological markets theory) and that the decision to do either will depend on the degree of competition within a social group. We test this using data from four chacma baboon troops, living in two populations that differ markedly in the degree of contest competition. As predicted by the predominance of grooming dyads in which females are closely ranked there was, in all four troops, a positive correlation between the time invested by one partner and that by the other. In addition, as predicted, the allocation of time was more closely matched in troops where grooming could not be exchanged for anything else. In troops where resource competition was high, we found in one of two troops a positive relationship between rank distance and the discrepancy in time allocation, with the lower ranking of the partners contributing more grooming.
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    Humans and chimpanzees are unusual among primates in that they frequently perform group hunts of mammalian prey and share meat with conspecifics. Especially interesting are cases in which males give meat to unrelated females. The meat-for-sex hypothesis aims at explaining these cases by proposing that males and females exchange meat for sex, which would result in males increasing their mating success and females increasing their caloric intake without suffering the energetic costs and potential risk of injury related to hunting. Although chimpanzees have been shown to share meat extensively with females, there has not been much direct evidence in this species to support the meat-for-sex hypothesis. Here we show that female wild chimpanzees copulate more frequently with those males who, over a period of 22 months, share meat with them. We excluded other alternative hypotheses to exchanging meat for sex, by statistically controlling for rank of the male, age, rank and gregariousness of the female, association patterns of each male-female dyad and meat begging frequency of each female. Although males were more likely to share meat with estrous than anestrous females given their proportional representation in hunting parties, the relationship between mating success and sharing meat remained significant after excluding from the analysis sharing episodes with estrous females. These results strongly suggest that wild chimpanzees exchange meat for sex, and do so on a long-term basis. Similar studies on humans will determine if the direct nutritional benefits that women receive from hunters in foraging societies could also be driving the relationship between reproductive success and good hunting skills.
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    Transfers and services are frequent in the animal kingdom. However, there is no clear evidence in animals that such transactions are based on weighing costs and benefits when giving or returning favours and keeping track of them over time (i.e. calculated reciprocity). We tested two orang-utans (Pongo pygmaeus abelii) in a token-exchange paradigm, in which each individual could exchange a token for food with the experimenter but only after first obtaining the token from the other orang-utan. Each orang-utan possessed tokens valuable to their partner but useless to themselves. Both orang-utans actively transferred numerous tokens (mostly partner-valuable) to their partner. One of the orang-utans routinely used gestures to request tokens while the other complied with such requests. Although initially the transfers were biased in one direction, they became more balanced towards the end of the study. Indeed, data on the last three series produced evidence of reciprocity both between and within trials. We observed an increase in the number and complexity of exchanges and alternations. This study is the first experimental demonstration of the occurrence of direct transfers of goods based on calculated reciprocity in non-human-primates.
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    Humans are well known for their ability to keep track of social debts over extended periods of time, and for their tendency to preferentially cooperate with closely bonded partners. Non-human primates have been shown to cooperate with kin and non-kin, and reciprocate helpful acts. However, there is ongoing debate over whether they keep track of previous interactions and, if so, whether they can do it over extended periods of time, or are constrained to finalize exchanges within a single encounter. In this study, we used 3000 hours of all-day focal follows of wild chimpanzees (Pan troglodytes verus) to investigate whether both females and males reciprocate grooming within a single interaction, throughout the day, or over longer periods of time. We found that grooming was reciprocated more symmetrically when measured on a long-term, rather than on an immediate or short-term basis. Random giving, general allocation of grooming efforts, similarities among individuals and kinship do not appear to explain these highly reciprocal exchanges. Previously collected consecutive focal follows of single individuals revealed that dyads groomed an average of once every 7 days. Our findings strongly suggest that chimpanzees, similar to humans, are able to keep track of past social interactions, at least for a one-week period, and balance services over repeated encounters.
  • Article
    Grooming networks among adult female monkeys exhibit two similar features across a number of different species. High-ranking animals receive more grooming than others, and the majority of grooming occurs between females of adjacent rank. A theoretical model which duplicates these features is presented, and the properties of the model are used to explain the possible causation and function of female grooming behaviour. The model illustrates how relatively simple principles governing the behaviour of individuals may be used to explain more complex aspects of the social structure of non-human primate groups.
  • Article
    The problems of achieving mutual cooperation can be formalized in a game called the Prisoner's Dilemma in which selfish defection is always more rewarding than cooperation. If the two protagonists have a certain minimum probability of meeting again a strategy called TIT FOR TAT is very successful. In TIT FOR TAT the player cooperates on the first move and thereafter does whatever the opponent did on the previous move. I have studied the behaviour of fish when confronting a potential predator, because conflicts can arise within pairs of fish in these circumstances which I argue resemble a series of games of Prisoner's Dilemma. Using a system of mirrors, single three-spined sticklebacks (Gasterosteus aculeatus) approaching a live predator were provided with either a simulated cooperating companion or a simulated defecting one. In both cases the test fish behaved according to TIT FOR TAT supporting the hypothesis that cooperation can evolve among egoists.
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    A genetical mathematical model is described which allows for interactions between relatives on one another's fitness. Making use of Wright's Coefficient of Relationship as the measure of the proportion of replica genes in a relative, a quantity is found which incorporates the maximizing property of Darwinian fitness. This quantity is named “inclusive fitness”. Species following the model should tend to evolve behaviour such that each organism appears to be attempting to maximize its inclusive fitness. This implies a limited restraint on selfish competitive behaviour and possibility of limited self-sacrifices.Special cases of the model are used to show (a) that selection in the social situations newly covered tends to be slower than classical selection, (b) how in populations of rather non-dispersive organisms the model may apply to genes affecting dispersion, and (c) how it may apply approximately to competition between relatives, for example, within sibships. Some artificialities of the model are discussed.