Evolution of cooperation by generalized reciprocity

The evolution of cooperation by direct reciprocity requires that individuals recognize their present partner and remember the outcome of their last encounter with that specific partner. Direct reciprocity thus requires advanced cognitive abilities. Here, we demonstrate that if individuals repeatedly interact within small groups with different partners in a two person Prisoner's Dilemma, cooperation can emerge and also be maintained in the absence of such cognitive capabilities. It is sufficient for an individual to base their decision of whether or not to cooperate on the outcome of their last encounter--even if it was with a different partner.     

Social Influences on Inequity Aversion in Children

Adults and children are willing to sacrifice personal gain to avoid both disadvantageous and advantageous inequity. These two forms of inequity aversion follow different developmental trajectories, with disadvantageous inequity aversion emerging around 4 years and advantageous inequity aversion emerging around 8 years. Although inequity aversion is assumed to be specific to situations where resources are distributed among individuals, the role of social context has not been tested in children. Here, we investigated the influence of two aspects of social context on inequity aversion in 4- to 9-year-old children: (1) the role of the experimenter distributing rewards and (2) the presence of a peer with whom rewards could be shared. Experiment 1 showed that children rejected inequity at the same rate, regardless of whether the experimenter had control over reward allocations. This indicates that children’s decisions are based upon reward allocations between themselves and a peer and are not attempts to elicit more favorable distributions from the experimenter. Experiment 2 compared rejections of unequal reward allocations in children interacting with or without a peer partner. When faced with a disadvantageous distribution, children frequently rejected a smaller reward when a larger reward was visible, even if no partner would obtain the larger reward. This suggests that nonsocial factors partly explain disadvantageous inequity rejections. However, rejections of disadvantageous distributions were higher when the larger amount would go to a peer, indicating that social context enhances disadvantageous inequity aversion. By contrast, children rejected advantageous distributions almost exclusively in the social context. Therefore, advantageous inequity aversion appears to be genuinely social, highlighting its potential relevance for the development of fairness concerns. By comparing social and nonsocial factors, this study provides a detailed picture of the expression of inequity aversion in human ontogeny and raises questions about the function and evolution of inequity aversion in humans.     

Crows and common ravens do not reciprocally exchange tokens with a conspecific to gain food rewards

Human economic transactions are based on complex forms of reciprocity, which involve the capacities to share and to keep track of what was given and received over time. Animals too engage in reciprocal interactions, but mechanisms such as calculated reciprocity have only been shown experimentally in few species. Various forms of cooperation, for example food and information sharing, are frequently observed in corvids, and they can engage in exchange interactions with human experimenters and accept delayed rewards. Here, we tested whether crows and common ravens would reciprocally exchange tokens with a conspecific in an exchange task. Birds received a set of three different types of tokens, some valuable for themselves, that is, they could exchange them for a food reward with a human experimenter, some valuable for their partner and some without value. The valuable tokens differed between the birds, which means that each bird could obtain more self-value tokens from their partner's compartment. We did not observe any active transfers, that is one individual giving a token to the experimental partner by placing it in its beak. We only observed 6 indirect transfers, that is one individual transferring a token into the compartment of the partner (3 no-value, 1 partner-value and 2 self-value tokens) and 67 “passive” transfers, that is one subject taking the token lying in reach in the compartment of the partner. Individuals took significantly more self-value tokens compared with no-value and partner-value tokens. This indicates a preference for tokens valuable to focal individuals. Significantly more no-value tokens compared with partner-value tokens were taken, likely to be caused by experimental partners exchanging self-value tokens with the human experimenter, and therefore, more no-value tokens being available in the compartment. Our results presently do not provide empirical support for reciprocity in crows and ravens, most likely caused by them not understanding the potential roles of receiver and donor. We therefore suggest further empirical tests of calculated reciprocity to be necessary in corvids.     

Strong reciprocity, human cooperation, and the enforcement of social norms

This paper provides strong evidence challenging the self-interest assumption that dominates the behavioral sciences and much evolutionary thinking. The evidence indicates that many people have a tendency to voluntarily cooperate, if treated fairly, and to punish noncooperators. We call this behavioral propensity “strong reciprocity” and show empirically that it can lead to almost universal cooperation in circumstances in which purely self-interested behavior would cause a complete breakdown of cooperation. In addition, we show that people are willing to punish those who behaved unfairly towards a third person or who defected in a Prisoner’s Dilemma game with a third person. This suggests that strong reciprocity is a powerful device for the enforcement of social norms involving, for example, food sharing or collective action. Strong reciprocity cannot be rationalized as an adaptive trait by the leading evolutionary theories of human cooperation (in other words, kin selection, reciprocal altruism, indirect reciprocity, and costly signaling theory). However, multilevel selection theories of cultural evolution are consistent with strong reciprocity.     

Predicting decisions in human social interactions using real-time fMRI and pattern classification

Negotiation and trade typically require a mutual interaction while simultaneously resting in uncertainty which decision the partner ultimately will make at the end of the process. Assessing already during the negotiation in which direction one's counterpart tends would provide a tremendous advantage. Recently, neuroimaging techniques combined with multivariate pattern classification of the acquired data have made it possible to discriminate subjective states of mind on the basis of their neuronal activation signature. However, to enable an online-assessment of the participant's mind state both approaches need to be extended to a real-time technique. By combining real-time functional magnetic resonance imaging (fMRI) and online pattern classification techniques, we show that it is possible to predict human behavior during social interaction before the interacting partner communicates a specific decision. Average accuracy reached approximately 70% when we predicted online the decisions of volunteers playing the ultimatum game, a well-known paradigm in economic game theory. Our results demonstrate the successful online analysis of complex emotional and cognitive states using real-time fMRI, which will enable a major breakthrough for social fMRI by providing information about mental states of partners already during the mutual interaction. Interestingly, an additional whole brain classification across subjects confirmed the online results: anterior insula, ventral striatum, and lateral orbitofrontal cortex, known to act in emotional self-regulation and reward processing for adjustment of behavior, appeared to be strong determinants of later overt behavior in the ultimatum game. Using whole brain classification we were also able to discriminate between brain processes related to subjective emotional and motivational states and brain processes related to the evaluation of objective financial incentives.     

Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees

Tolerant food sharing among human foragers can largely be explained by reciprocity. In contrast, food sharing among chimpanzees and bonobos may not always reflect reciprocity, which could be explained by different dominance styles: in egalitarian societies reciprocity is expressed freely, while in more despotic groups dominants may hinder reciprocity. We tested the degree of reciprocity and the influence of dominance on food sharing among chimpanzees and bonobos in two captive groups. First, we found that chimpanzees shared more frequently, more tolerantly, and more actively than bonobos. Second, among chimpanzees, food received was the best predictor of food shared, indicating reciprocal exchange, whereas among bonobos transfers were mostly unidirectional. Third, chimpanzees had a shallower and less linear dominance hierarchy, indicating that they were less despotic than bonobos. This suggests that the tolerant and reciprocal sharing found in chimpanzees, but not bonobos, was made possible by the absence of despotism. To investigate this further, we tested the relationship between despotism and reciprocity in grooming using data from an additional five groups and five different study periods on the main groups. The results showed that i) all chimpanzee groups were less despotic and groomed more reciprocally than bonobo groups, and ii) there was a general negative correlation between despotism and grooming reciprocity across species. This indicates that an egalitarian hierarchy may be more common in chimpanzees, at least in captivity, thus fostering reciprocal exchange. We conclude that a shallow dominance hierarchy was a necessary precondition for the evolution of human‐like reciprocal food sharing. Am J Phys Anthropol 143:41–51, 2010. © 2010 Wiley‐Liss, Inc.     

Generalized reciprocity in rats

The evolution of cooperation among nonrelatives has been explained by direct, indirect, and strong reciprocity. Animals should base the decision to help others on expected future help, which they may judge from past behavior of their partner. Although many examples of cooperative behavior exist in nature where reciprocity may be involved, experimental evidence for strategies predicted by direct reciprocity models remains controversial; and indirect and strong reciprocity have been found only in humans so far. Here we show experimentally that cooperative behavior of female rats is influenced by prior receipt of help, irrespective of the identity of the partner. Rats that were trained in an instrumental cooperative task (pulling a stick in order to produce food for a partner) pulled more often for an unknown partner after they were helped than if they had not received help before. This alternative mechanism, called generalized reciprocity, requires no specific knowledge about the partner and may promote the evolution of cooperation among unfamiliar nonrelatives.     

Reciprocity on the Hardwood: Passing Patterns among Professional Basketball Players

Past theory and research view reciprocal resource sharing as a fundamental building block of human societies. Most studies of reciprocity dynamics have focused on trading among individuals in laboratory settings. But if motivations to engage in these patterns of resource sharing are powerful, then we should observe forms of reciprocity even in highly structured group environments in which reciprocity does not clearly serve individual or group interests. To this end, we investigated whether patterns of reciprocity might emerge among teammates in professional basketball games. Using data from logs of National Basketball Association (NBA) games of the 2008–9 season, we estimated a series of conditional logistic regression models to test the impact of different factors on the probability that a given player would assist another player in scoring a basket. Our analysis found evidence for a direct reciprocity effect in which players who had “received” assists in the past tended to subsequently reciprocate their benefactors. Further, this tendency was time-dependent, with the probability of repayment highest soon after receiving an assist and declining as game time passed. We found no evidence for generalized reciprocity – a tendency to “pay forward” assists – and only very limited evidence for indirect reciprocity – a tendency to reward players who had sent others many assists. These findings highlight the power of reciprocity to shape human behavior, even in a setting characterized by extensive planning, division of labor, quick decision-making, and a focus on inter-group competition.     

Democracy in animals: the evolution of shared group decisions

A 'consensus decision' is when the members of a group choose, collectively, between mutually exclusive actions. In humans, consensus decisions are often made democratically or in an 'equally shared' manner, i.e. all group members contribute to the decision. Biologists are only now realizing that shared consensus decisions also occur in social animals (other than eusocial insects). Sharing of decisions is, in principle, more profitable for groups than accepting the 'unshared' decision of a single dominant member. However, this is not true for all individual group members, posing a question as to how shared decision making could evolve. Here, we use a game theory model to show that sharing of decisions can evolve under a wide range of circumstances but especially in the following ones: when groups are heterogeneous in composition; when alternative decision outcomes differ in potential costs and these costs are large; when grouping benefits are marginal; or when groups are close to, or above, optimal size. Since these conditions are common in nature, it is easy to see how mechanisms for shared decision making could have arisen in a wide range of species, including early human ancestors.     

Attribution and Expression of Incentive Salience Are Differentially Signaled by Ultrasonic Vocalizations in Rats

During Pavlovian incentive learning, the affective properties of rewards are thought to be transferred to their predicting cues. However, how rewards are represented emotionally in animals is widely unknown. This study sought to determine whether 50-kHz ultrasonic vocalizations (USVs) in rats may signal such a state of incentive motivation to natural, nutritional rewards. To this end, rats learned to anticipate food rewards and, across experiments, the current physiological state (deprived vs. sated), the type of learning mechanism recruited (Pavlovian vs. instrumental), the hedonic properties of UCS (low vs. high palatable food), and the availability of food reward (continued vs. discontinued) were manipulated. Overall, we found that reward-cues elicited 50-kHz calls as they were signaling a putative affective state indicative of incentive motivation in the rat. Attribution and expression of incentive salience, however, seemed not to be an unified process, and could be teased apart in two different ways: 1) under high motivational state (i.e., hunger), the attribution of incentive salience to cues occurred without being expressed at the USVs level, if reward expectations were higher than the outcome; 2) in all experiments when food rewards were devalued by satiation, reward cues were still able to elicit USVs and conditioned anticipatory activity although reward seeking and consumption were drastically weakened. Our results suggest that rats are capable of representing rewards emotionally beyond apparent, immediate physiological demands. These findings may have translational potential in uncovering mechanisms underlying aberrant and persistent motivation as observed in drug addiction, gambling, and eating disorders.     

Nominal kinship cues facilitate altruism.

We investigated whether names in common promote altruistic behaviour, predicting that this would be especially so for relatively uncommon names, for surnames (which are better kinship cues than first names), and among women (who, although less willing than men to help strangers, according to prior research, are also the primary "kin keepers"). We solicited help from 2960 email addressees, with the request ostensibly coming from a same-sex person sharing both, either, or neither of the addressee''s first and last names. As anticipated, addressees were most likely to respond helpfully when senders shared both their names (12.3%) and least likely when they shared neither (2.0%), and this was especially true for relatively uncommon names. A shared surname was more effective than a shared first name only if it was relatively uncommon. Women were substantially more likely to reply than men. These results indicate that names elicit altruism because they function as salient cues of kinship.     

The shared reward dilemma

One of the most direct human mechanisms of promoting cooperation is rewarding it. We study the effect of sharing a reward among cooperators in the most stringent form of social dilemma, namely the prisoner's dilemma (PD). Specifically, for a group of players that collect payoffs by playing a pairwise PD game with their partners, we consider an external entity that distributes a fixed reward equally among all cooperators. Thus, individuals confront a new dilemma: on the one hand, they may be inclined to choose the shared reward despite the possibility of being exploited by defectors; on the other hand, if too many players do that, cooperators will obtain a poor reward and defectors will outperform them. By appropriately tuning the amount to be shared a vast variety of scenarios arises, including the traditional ones in the study of cooperation as well as more complex situations where unexpected behavior can occur. We provide a complete classification of the equilibria of the n-player game as well as of its evolutionary dynamics.     

Can Monkeys Make Investments Based on Maximized Pay-off?

Animals can maximize benefits but it is not known if they adjust their investment according to expected pay-offs. We investigated whether monkeys can use different investment strategies in an exchange task. We tested eight capuchin monkeys (Cebus apella) and thirteen macaques (Macaca fascicularis, Macaca tonkeana) in an experiment where they could adapt their investment to the food amounts proposed by two different experimenters. One, the doubling partner, returned a reward that was twice the amount given by the subject, whereas the other, the fixed partner, always returned a constant amount regardless of the amount given. To maximize pay-offs, subjects should invest a maximal amount with the first partner and a minimal amount with the second. When tested with the fixed partner only, one third of monkeys learned to remove a maximal amount of food for immediate consumption before investing a minimal one. With both partners, most subjects failed to maximize pay-offs by using different decision rules with each partner' quality. A single Tonkean macaque succeeded in investing a maximal amount to one experimenter and a minimal amount to the other. The fact that only one of over 21 subjects learned to maximize benefits in adapting investment according to experimenters' quality indicates that such a task is difficult for monkeys, albeit not impossible.     

Emotional reactions to learning in cattle

It has been suggested that during instrumental learning, animals are likely to react emotionally to the reinforcer. They may in addition react emotionally to their own achievements. These reactions are of interest with regard to the animals’ capacity for self-awareness. Therefore, we devised a yoked control experiment involving the acquisition of an operant task. We aimed to identify the emotional reactions of young cattle to their own learning and to separate these from reactions to a food reward. Twelve Holstein–Friesian heifers aged 7–12 months were divided into two groups. Heifers in the experimental group were conditioned over a 14-day period to press a panel in order to open a gate for access to a food reward. For heifers in the control group, the gate opened after a delay equal to their matched partner’s latency to open it. To allow for observation of the heifers’ movements during locomotion after the gate had opened, there was a 15 m distance in the form of a race from the gate to the food trough. The heart rate of the heifers, and their behaviour when moving along the race towards the food reward were measured. When experimental heifers made clear improvements in learning, they were more likely than on other occasions to have higher heart rates and tended to move more vigorously along the race in comparison with their controls. This experiment found some, albeit inconclusive, indication that cattle may react emotionally to their own learning improvement.     

Feel good,do good? Disentangling reciprocity from unconditional prosociality

Direct and generalised reciprocity can establish evolutionarily stable levels of cooperation among unrelated individuals, with animals reciprocating help based on whether they have been helped by a social partner before. It has been argued that the actual cooperative act by a social partner may be of minor importance for seemingly reciprocal cooperation and that a mere positive experience might suffice to enhance helpful behaviour towards a conspecific (‘feel good, do good’). However, this effect could easily be exploited by defectors free‐riding on an individual's enhanced propensity to cooperate after an unspecific positive experience, without investing in reciprocity themselves. Here, we use female Norway rats (Rattus norvegicus) to test if a positive experience that was not provided by a helping partner increases the propensity to subsequently help a social partner. We manipulated the experience of test subjects by providing them with treats, either in the presence or absence of a conspecific. Thereafter, we assessed whether they produce treats and if so, how many, for an unfamiliar social partner compared to a situation in which they had not received treats before. As the treats the test subject received had not been provided by a social partner even if the partner was present, we predicted that the rats should not be more cooperative after they had received treats than if they had not. Indeed, the helping behaviour of rats was apparently not influenced by prior experience made either in a social or non‐social context. Rats have been shown previously to perform both direct and generalised reciprocity in the same variant of the iterated prisoner's dilemma game. Our results suggest that this behaviour cannot be explained by an unspecific positive experience. The decision to help a social partner seems to be contingent on previously receiving help from a social partner (reciprocity), not on any positive experience (unconditional prosociality).     

The selfish nature of generosity: harassment and food sharing in primates

Animals may share food to gain immediate or delayed fitness benefits. Previous studies of sharing have concentrated on delayed benefits such as reciprocity, trade and punishment. This study tests an alternative model (the harassment or sharing-under-pressure hypothesis) in which a food owner immediately benefits because sharing avoids costly harassment from a beggar. I present an experiment that varies the potential ability of the beggar to harass, and of the owner to defend the food, to examine the effects of harassment on food sharing in two primate species: chimpanzees (Pan troglodytes) and squirrel monkeys (Saimiri boliviensis). For both species, high levels of harassment potential significantly increased both beggar harassment and sharing by the owner. Food defensibility did not affect harassment or sharing. Interestingly, squirrel monkeys and chimpanzees shared equally frequently with conspecifics despite a much higher natural sharing rate in chimpanzees. These results suggest that harassment can play a significant role in primate food sharing, providing a simple alternative to reciprocity. The selfish nature of harassment has implications for economic, psychological and evolutionary studies of cooperative systems.     

Gratitude Depends on the Relational Model of Communal Sharing

We studied the relation between benefits, perception of social relationships and gratitude. Across three studies, we provide evidence that benefits increase gratitude to the extent to which one applies a mental model of a communal relationship. In Study 1, the communal sharing relational model, and no other relational models, predicted the amount of gratitude participants felt after imagining receiving a benefit from a new acquaintance. In Study 2, participants recalled a large benefit they had received. Applying a communal sharing relational model increased feelings of gratitude for the benefit. In Study 3, we manipulated whether the participant or another person received a benefit from an unknown other. Again, we found that the extent of communal sharing perceived in the relationship with the stranger predicted gratitude. An additional finding of Study 2 was that communal sharing predicted future gratitude regarding the relational partner in a longitudinal design. To conclude, applying a communal sharing model predicts gratitude regarding concrete benefits and regarding the relational partner, presumably because one perceives the communal partner as motivated to meet one''s needs. Finally, in Study 3, we found in addition that being the recipient of a benefit without opportunity to repay directly increased communal sharing, and indirectly increased gratitude. These circumstances thus seem to favor the attribution of communal norms, leading to a communal sharing representation and in turn to gratitude. We discuss the importance of relational models as mental representations of relationships for feelings of gratitude.     

Sexual selection for moral virtues

Moral evolution theories have emphasized kinship, reciprocity, group selection, and equilibrium selection. Yet, moral virtues are also sexually attractive. Darwin suggested that sexual attractiveness may explain many aspects of human morality. This paper updates his argument by integrating recent research on mate choice, person perception, individual differences, costly signaling, and virtue ethics. Many human virtues may have evolved in both sexes through mutual mate choice to advertise good genetic quality, parenting abilities, and/or partner traits. Such virtues may include kindness, fidelity, magnanimity, and heroism, as well as quasi-moral traits like conscientiousness, agreeableness, mental health, and intelligence. This theory leads to many testable predictions about the phenotypic features, genetic bases, and social-cognitive responses to human moral virtues.     

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus

Intranasal oxytocin (OT) delivery has been used to non-invasively manipulate mammalian cooperative behavior. Such manipulations can potentially provide insight into both shared and species-specific mechanisms underlying cooperation. Vampire bats are remarkable for their high rates of allogrooming and the presence of regurgitated food sharing among adults. We administered intranasal OT to highly familiar captive vampire bats of varying relatedness to test for an effect on allogrooming and food sharing. We found that intranasal OT did not have a detectable effect on food-sharing occurrence, but it did increase the size of regurgitated food donations when controlling for dyad and amount of allogrooming. Intranasal OT in females increased the amount of allogrooming per partner and across all partners per trial, but not the number of partners. We also found that the peak effect of OT treatments occurred 30–50 min after administration, which is consistent with the reported latency for intranasal OT to affect relevant brain areas in rats and mice. Our results suggest that intranasal OT is a potential tool for influencing dyadic cooperative investments, but measuring prior social relationships may be necessary to interpret the results of hormonal manipulations of cooperative behavior and it may be difficult to alter partner choice in vampire bats using intranasal OT alone.     

Accepting loss: the temporal limits of reciprocity in brown capuchin monkeys

Delayed reciprocity is a potentially important mechanism for cooperation to occur. It is however rarely reported among animals, possibly because it requires special skills like the ability to plan a loss. We tested six brown capuchin monkeys (Cebus apella) in such skills. Subjects were studied in exchange tasks in which they had to retain a food item for a given time lag before returning it to an experimenter and obtaining a more desirable reward. Experiments showed that the subjects could wait for several minutes when allowed to return only part of the initial item. When required to return the full item intact, however, most subjects could not sustain a time lag longer than 10 s. Although the duration of waiting increased with the amount of return expected by subjects, in most cases it did not extend beyond 20 s even when the eperimenter offered a food amount 40 fold the initial item. The failure of capuchin monkeys to sustain long-lasting waiting periods may be explained by limited self-control abilities. This would prevent them achieving reciprocal altruism.