The psychology of primate cooperation and competition: a call for realigning research agendas

Cooperation and competition are two key components of social life. Current research agendas investigating the psychological underpinnings of competition and cooperation in non-human primates are misaligned. The majority of work on competition has been done in the context of theory of mind and deception, while work on cooperation has mostly focused on collaboration and helping. The current impression that theory of mind is not necessarily implicated in cooperative activities and that helping could not be an integral part of competition might therefore be rather misleading. Furthermore, theory of mind research has mainly focused on cognitive aspects like the type of stimuli controlling responses, the nature of representation and how those representations are acquired, while collaboration and helping have focused primarily on motivational aspects like prosociality, common goals and a sense of justice and other-regarding concerns. We present the current state of these two bodies of research paying special attention to how they have developed and diverged over the years. We propose potential directions to realign the research agendas to investigate the psychological underpinnings of cooperation and competition in primates and other animals.     

The interplay of cognition and cooperation

Cooperation often involves behaviours that reduce immediate payoffs for actors. Delayed benefits have often been argued to pose problems for the evolution of cooperation because learning such contingencies may be difficult as partners may cheat in return. Therefore, the ability to achieve stable cooperation has often been linked to a species'' cognitive abilities, which is in turn linked to the evolution of increasingly complex central nervous systems. However, in their famous 1981 paper, Axelrod and Hamilton stated that in principle even bacteria could play a tit-for-tat strategy in an iterated Prisoner''s Dilemma. While to our knowledge this has not been documented, interspecific mutualisms are present in bacteria, plants and fungi. Moreover, many species which have evolved large brains in complex social environments lack convincing evidence in favour of reciprocity. What conditions must be fulfilled so that organisms with little to no brainpower, including plants and single-celled organisms, can, on average, gain benefits from interactions with partner species? On the other hand, what conditions favour the evolution of large brains and flexible behaviour, which includes the use of misinformation and so on? These questions are critical, as they begin to address why cognitive complexity would emerge when ‘simple’ cooperation is clearly sufficient in some cases. This paper spans the literature from bacteria to humans in our search for the key variables that link cooperation and deception to cognition.     

The evolution of strong reciprocity: cooperation in heterogeneous populations

How do human groups maintain a high level of cooperation despite a low level of genetic relatedness among group members? We suggest that many humans have a predisposition to punish those who violate group-beneficial norms, even when this imposes a fitness cost on the punisher. Such altruistic punishment is widely observed to sustain high levels of cooperation in behavioral experiments and in natural settings. We offer a model of cooperation and punishment that we call STRONG RECIPROCITY: where members of a group benefit from mutual adherence to a social norm, strong reciprocators obey the norm and punish its violators, even though as a result they receive lower payoffs than other group members, such as selfish agents who violate the norm and do not punish, and pure cooperators who adhere to the norm but free-ride by never punishing. Our agent-based simulations show that, under assumptions approximating likely human environments over the 100000 years prior to the domestication of animals and plants, the proliferation of strong reciprocators when initially rare is highly likely, and that substantial frequencies of all three behavioral types can be sustained in a population. As a result, high levels of cooperation are sustained. Our results do not require that group members be related or that group extinctions occur.     

Object exchange between captive chimpanzees: a case report

Intelligent resource exchange usually has been thought of as a strictly human phenomenon. Some searchers demonstrated experimentally that chimpanzees have the necessary cognitive capacities to exchange food with humans. This short article presents the first example of an immediate and spontaneous exchange of objects between chimpanzees. This exchange between Spock and Maya is not a direct exchange of objects, from hand to hand, as would be observed among humans. This leads us to suppose that exchange, if it really occurs amongst wild chimpanzees, is done indirectly, through the more or less concomitant deposit of the objects or food items on the ground, maybe because chimpanzees are quadrupedal animals. This observation is discussed in relation to the notion of reciprocity used in anthropological and sociological studies.     

Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment

Common vampire bats often regurgitate food to roost-mates that fail to feed. The original explanation for this costly helping behaviour invoked both direct and indirect fitness benefits. Several authors have since suggested that food sharing is maintained solely by indirect fitness because non-kin food sharing could have resulted from kin recognition errors, indiscriminate altruism within groups, or harassment. To test these alternatives, we examined predictors of food-sharing decisions under controlled conditions of mixed relatedness and equal familiarity. Over a 2 year period, we individually fasted 20 vampire bats (Desmodus rotundus) and induced food sharing on 48 days. Surprisingly, donors initiated food sharing more often than recipients, which is inconsistent with harassment. Food received was the best predictor of food given across dyads, and 8.5 times more important than relatedness. Sixty-four per cent of sharing dyads were unrelated, approaching the 67 per cent expected if nepotism was absent. Consistent with social bonding, the food-sharing network was consistent and correlated with mutual allogrooming. Together with past work, these findings support the hypothesis that food sharing in vampire bats provides mutual direct fitness benefits, and is not explained solely by kin selection or harassment.     

On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality

In any given species, cooperation involves prosocial acts that usually return a fitness benefit to the actor. These acts are produced by a set of psychological rules, which will be similar in related species if they have a similar natural history of cooperation. Prosocial acts can be (i) reactive, i.e. in response to specific stimuli, or (ii) proactive, i.e. occur in the absence of such stimuli. We propose that reactive prosocial acts reflect sensitivity to (i) signals or signs of need and (ii) the presence and size of an audience, as modified by (iii) social distance to the partner or partners. We examine the evidence for these elements in humans and other animals, especially non-human primates, based on the natural history of cooperation, quantified in the context of food sharing, and various experimental paradigms. The comparison suggests that humans share with their closest living relatives reactive responses to signals of need, but differ in sensitivity to signs of need and cues of being watched, as well as in the presence of proactive prosociality. We discuss ultimate explanations for these derived features, in particular the adoption of cooperative breeding as well as concern for reputation and costly signalling during human evolution.     

The evolution of cooperation and altruism--a general framework and a classification of models

One of the enduring puzzles in biology and the social sciences is the origin and persistence of intraspecific cooperation and altruism in humans and other species. Hundreds of theoretical models have been proposed and there is much confusion about the relationship between these models. To clarify the situation, we developed a synthetic conceptual framework that delineates the conditions necessary for the evolution of altruism and cooperation. We show that at least one of the four following conditions needs to be fulfilled: direct benefits to the focal individual performing a cooperative act; direct or indirect information allowing a better than random guess about whether a given individual will behave cooperatively in repeated reciprocal interactions; preferential interactions between related individuals; and genetic correlation between genes coding for altruism and phenotypic traits that can be identified. When one or more of these conditions are met, altruism or cooperation can evolve if the cost-to-benefit ratio of altruistic and cooperative acts is greater than a threshold value. The cost-to-benefit ratio can be altered by coercion, punishment and policing which therefore act as mechanisms facilitating the evolution of altruism and cooperation. All the models proposed so far are explicitly or implicitly built on these general principles, allowing us to classify them into four general categories.     

Mechanistic constraints and the unlikely evolution of reciprocal cooperation

Social evolution theory faces a puzzle: a gap between theoretical and empirical results on reciprocity. On the one hand, models show that reciprocity should evolve easily in a wide range of circumstances. On the other hand, empirically, few clear instances of reciprocity (even in a broad sense) have been found in nonhuman animals. In this paper, I aim to suggest and evaluate a novel reason concurring to solve this puzzle. I propose that it is difficult for reciprocity to evolve because it raises an evolutionary problem of bootstrapping: it requires that two complementary functions: (i) the ability to cooperate and (ii) the ability to respond conditionally to the cooperation of others, arise together and reach a significant frequency, whereas neither of them can be favoured in the absence of the other. I develop analytical models and simulations showing that, for this reason, the evolutionary emergence of reciprocal cooperation is highly unlikely. I then discuss the consequences of this result for our understanding of cooperation.     

Getting a Fair Share: Attitudes and Perceptions of Biobank Stakeholders Concerning the Fairness of Sample Sharing

Biobanks are essential tools for furthering a broad range of medical research areas. However, despite the plethora of national and international laws and guidelines which apply to them, the access and sharing policies of biobanks are only sparsely addressed by regulatory bodies. The ‘give and take’ process of biosample sharing is largely left up to biobank stakeholders themselves to oversee; it is therefore both in stakeholders' power, and in their interest, to ensure that sample accessibility is fair. This is an important step in motivating researchers to collaborate and pool samples, and is crucial to fostering trust in the absence of universally accepted standard practices. To date, little attention has been paid to how fairness considerations affect scientific material sharing, and no empirical research has been carried out to determine the role that fairness plays in collaborative studies. In order to begin to gain understanding in this area, we interviewed 36 biobank stakeholders currently working in Switzerland, focusing on their perceptions of current and optimal fair sharing practices. Our findings reveal that fairness is an important feature of exchange situations for these stakeholders, and that they have well‐formed notions about the practical elements of fair sample access, although ideas about the concept of fairness itself are vague. In order to support efforts to network biobanks, attention should be paid to this issue to reassure all involved that they are getting a fair share in their cooperative efforts.     

Genetic differentiation and the evolution of cooperation in chimpanzees and humans

It has been proposed that human cooperation is unique among animals for its scale and complexity, its altruistic nature and its occurrence among large groups of individuals that are not closely related or are even strangers. One potential solution to this puzzle is that the unique aspects of human cooperation evolved as a result of high levels of lethal competition (i.e. warfare) between genetically differentiated groups. Although between-group migration would seem to make this scenario unlikely, the plausibility of the between-group competition model has recently been supported by analyses using estimates of genetic differentiation derived from contemporary human groups hypothesized to be representative of those that existed during the time period when human cooperation evolved. Here, we examine levels of between-group genetic differentiation in a large sample of contemporary human groups selected to overcome some of the problems with earlier estimates, and compare them with those of chimpanzees. We find that our estimates of between-group genetic differentiation in contemporary humans are lower than those used in previous tests, and not higher than those of chimpanzees. Because levels of between-group competition in contemporary humans and chimpanzees are also similar, these findings suggest that the identification of other factors that differ between chimpanzees and humans may be needed to provide a compelling explanation of why humans, but not chimpanzees, display the unique features of human cooperation.     

Prelinguistic development of children and chimpanzees

What was unique about our laboratory was the detailed simulation of a human rearing environment for infant chimpanzees, together with continuous, intensive observation and recording of behavioral development. Communication in American Sign Language (ASL) was integrated into this procedure in a way that simulates the teaching of vocal and gestural languages to human children. The result is a comprehensive longitudinal record of the stage by stage development of two-way communication in sign language and its relation to basic aspects of behavioral development such as: locomotion, manipulative skills, observational learning, and social play. In the longitudinal records of five infant chimpanzees, we can trace the patterns of development and also examine the consistency of individual differences through the first five years. The central question is the relation between developing skills in the use of American Sign Language and the rest of behavioral development. To analyze factors that influence development, we have compared records for infant chimpanzees reared in the crossfostering laboratory with records for chimpanzees reared in the wild by their own mothers and chimpanzees reared in cages under conventional laboratory conditions, as well as with records of development for human children, reared in homes and reared in institutions.     

Reciprocity,culture and human cooperation: previous insights and a new cross-cultural experiment

Understanding the proximate and ultimate sources of human cooperation is a fundamental issue in all behavioural sciences. In this paper, we review the experimental evidence on how people solve cooperation problems. Existing studies show without doubt that direct and indirect reciprocity are important determinants of successful cooperation. We also discuss the insights from a large literature on the role of peer punishment in sustaining cooperation. The experiments demonstrate that many people are ‘strong reciprocators’ who are willing to cooperate and punish others even if there are no gains from future cooperation or any other reputational gains. We document this in new one-shot experiments, which we conducted in four cities in Russia and Switzerland. Our cross-cultural approach allows us furthermore to investigate how the cultural background influences strong reciprocity. Our results show that culture has a strong influence on positive and in especially strong negative reciprocity. In particular, we find large cross-cultural differences in ‘antisocial punishment’ of pro-social cooperators. Further cross-cultural research and experiments involving different socio-demographic groups document that the antisocial punishment is much more widespread than previously assumed. Understanding antisocial punishment is an important task for future research because antisocial punishment is a strong inhibitor of cooperation.     

The smell of cooperation: rats increase helpful behaviour when receiving odour cues of a conspecific performing a cooperative task

Reciprocity can explain cooperative behaviour among non-kin, where individuals help others depending on their experience in previous interactions. Norway rats (Rattus norvegicus) cooperate reciprocally according to direct and generalized reciprocity. In a sequence of four consecutive experiments, we show that odour cues from a cooperating conspecific are sufficient to induce the altruistic help of rats in a food-exchange task. When rats were enabled to help a non-cooperative partner while receiving olfactory information from a rat helping a conspecific in a different room, they helped their non-cooperative partner as if it was a cooperative one. We further show that the cues inducing altruistic behaviour are released during the act of cooperation and do not depend on the identity of the cue provider. Remarkably, olfactory cues seem to be more important for cooperation decisions than experiencing a cooperative act per se. This suggests that rats may signal their cooperation propensity to social partners, which increases their chances to receive help in return.     

Evolutionary games of cooperation: Insights through integration of theory and data

Cooperation is central to the regulation of many ecological processes and the persistence of ecosystems and their associated functions. However, the evolution of cooperation amongst non-kin appears paradoxical. Games such as the prisoner's dilemma, snowdrift and stag hunt have been borrowed from game theory and used extensively to investigate cooperation. Advances in this area have been numerous and have been provided by both empirical and theoretical studies. We outline some of the common games used and review some of the major findings and recent advancements made in this area. We show a clear link between data and theory, and how this link has been key to our understanding of cooperation.