Sarah F. Brosnan

Monkeys reject unequal pay

During the evolution of cooperation it may have become critical for individuals to compare their own efforts and pay-offs with those of others. Negative reactions may occur when expectations are violated. One theory proposes that aversion to inequity can explain human cooperation within the bounds of the rational choice model, and may in fact be more inclusive than previous explanations. Although there exists substantial cultural variation in its particulars, this ‘sense of fairness’ is probably a human universal that has been shown to prevail in a wide variety of circumstances. However, we are not the only cooperative animals, hence inequity aversion may not be uniquely human. Many highly cooperative nonhuman species seem guided by a set of expectations about the outcome of cooperation and the division of resources. Here we demonstrate that a nonhuman primate, the brown capuchin monkey (Cebus apella), responds negatively to unequal reward distribution in exchanges with a human experimenter. Monkeys refused to participate if they witnessed a conspecific obtain a more attractive reward for equal effort, an effect amplified if the partner received such a reward without any effort at all. These reactions support an early evolutionary origin of inequity aversion.

Chimpanzees are indifferent to the welfare of unrelated group members.

Humans are an unusually prosocial species—we vote, give blood, recycle, give tithes and punish violators of social norms. Experimental evidence indicates that people willingly incur costs to help strangers in anonymous one-shot interactions, and that altruistic behaviour is motivated, at least in part, by empathy and concern for the welfare of others (hereafter referred to as other-regarding preferences). In contrast, cooperative behaviour in non-human primates is mainly limited to kin and reciprocating partners, and is virtually never extended to unfamiliar individuals. Here we present experimental tests of the existence of other-regarding preferences in non-human primates, and show that chimpanzees (Pan troglodytes) do not take advantage of opportunities to deliver benefits to familiar individuals at no material cost to themselves, suggesting that chimpanzee behaviour is not motivated by other-regarding preferences. Chimpanzees are among the primates most likely to demonstrate prosocial behaviours. They participate in a variety of collective activities, including territorial patrols, coalitionary aggression, cooperative hunting, food sharing and joint mate guarding. Consolation of victims of aggression and anecdotal accounts of solicitous treatment of injured individuals suggest that chimpanzees may feel empathy. Chimpanzees sometimes reject exchanges in which they receive less valuable rewards than others, which may be one element of a ‘sense of fairness’, but there is no evidence that they are averse to interactions in which they benefit more than others.

Tolerance for inequity may increase with social closeness in chimpanzees

Economic decision–making depends on our social environment. Humans tend to respond differently to inequity in close relationships, yet we know little about the potential for such variation in other species. We examine responses to inequity in several groups of chimpanzees (Pan troglodytes) in a paradigm similar to that used previously in capuchin monkeys (Cebus apella). We demonstrate that, like capuchin monkeys, chimpanzees show a response to inequity of rewards that is based upon the partner receiving the reward rather than the presence of the reward alone. However, we also found a great amount of variation between groups tested, indicating that chimpanzees, like people, respond to inequity in a variable manner, which we speculate could be caused by such variables as group size, the social closeness of the group (as reflected in length of time that the group has been together) and group–specific traditions.

A proximate perspective on reciprocal altruism.

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.

Nonhuman Species’ Reactions to Inequity and their Implications for Fairness

It is well known that humans respond negatively to inequity, but until recently little has been known about such responses in animals. Previous observational research in animals has shown hints that animals do respond to inequity. Chimpanzees respond with temper tantrums if they do not get what they desire, social canids refuse to play with individuals who violate social rules, and ravens show third party intervention against norm violations. Recent experimental work with nonhuman primates has given us a more detailed understanding. Capuchin monkeys and chimpanzees both respond negatively to distributional inequity. Moreover, chimpanzees show significant variation in response depending upon the social group they inhabit, with those from a short-term group or a relatively asocial living situation showing a much greater response to inequity than those from a long-term stable group. This mirrors human variation in responses to inequity, which are based upon the quality of the relationship. In this paper, I attempt to define “fairness” in a way that is useful for nonhuman studies and clarify what aspects are being examined in animal societies. I then place the animal work in the context of the studies on humans, especially as related to research in social psychology and economics. I conclude that studying the inequity response in animals is useful for a number of reasons, including the opportunity to gain insight into how this response functions in less complex organisms and social systems and clarification of our understanding of the evolution of this behavior.

Inequity responses of monkeys modified by effort

Without joint benefits, joint actions could never have evolved. Cooperative animals need to monitor closely how large a share they receive relative to their investment toward collective goals. This work documents the sensitivity to reward division in brown, or tufted, capuchin monkeys (Cebus apella). In addition to confirming previous results with a larger subject pool, this work rules out several alternative explanations and adds data on effort sensitivity. Thirteen adult monkeys exchanged tokens for rewards, showing negative reactions to receiving a less-favored reward than their partner. Because their negative reaction could not be attributed to the mere visibility of better rewards (greed hypothesis) nor to having received such rewards in the immediate past (frustration hypothesis), it must have been caused by seeing their partner obtain the better reward. Effort had a major effect in that by far the lowest level of performance in the entire study occurred in subjects required to expend a large effort while at the same time seeing their partner receive a better reward. It is unclear whether this effort–effect was based on comparisons with the partner, but it added significantly to the intensity of the inequity response. These effects are as expected if the inequity response evolved in the context of cooperative survival strategies.

Endowment Effects in Chimpanzees

Human behavior is not always consistent with standard rational choice predictions. Apparent deviations from rational choice predictions provide a promising arena for the merger of economics and biology [1-6]. Although little is known about the extent to which other species exhibit these seemingly irrational patterns [7-9], similarities across species would suggest a common evolutionary root to the phenomena. The present study investigated whether chimpanzees exhibit an endowment effect, a seemingly paradoxical behavior in which humans tend to value a good they have just come to possess more than they would have only a moment before [10-13]. We show the first evidence that chimpanzees do exhibit an endowment effect, by favoring items they just received more than their preferred items that could be acquired through exchange. Moreover, the effect is stronger for food than for less evolutionarily salient objects, perhaps because of historically greater risks associated with keeping a valuable item versus attempting to exchange it for another [14, 15]. These findings suggest that many seeming deviations from rational choice predictions may be common to humans and chimpanzees and that the evaluation of these through a lens of evolutionary relevance may yield further insights in humans and other species.

Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task

Chimpanzees provide help to unrelated individuals in a broad range of situations. The pattern of helping within pairs suggests that contingent reciprocity may have been an important mechanism in the evolution of altruism in chimpanzees. However, correlational analyses of the cumulative pattern of interactions over time do not demonstrate that helping is contingent upon previous acts of altruism, as required by the theory of reciprocal altruism. Experimental studies provide a controlled approach to examine the importance of contingency in helping interactions. In this study, we evaluated whether chimpanzees would be more likely to provide food to a social partner from their home group if their partner had previously provided food for them. The chimpanzees manipulated a barpull apparatus in which actors could deliver rewards either to themselves and their partners or only to themselves. Our findings indicate that the chimpanzees’ responses were not consistently influenced by the behavior of their partners in previous rounds. Only one of the 11 dyads that we tested demonstrated positive reciprocity. We conclude that contingent reciprocity does not spontaneously arise in experimental settings, despite the fact that patterns of behavior in the field indicate that individuals cooperate preferentially with reciprocating partners.

Evolution of responses to (un)fairness

Background The human sense of fairness presents an evolutionary puzzle because it appears to run counter to the short-term interests of at least some parties. We not only react negatively to getting less than a partner but sometimes also to getting more, which seems illogical. Following an ideal of impartiality, we seek appropriate outcomes for everyone within the community, not just a few individuals, and, in particular, not just ourselves. Why do we react this way? Are we the only species to do so? Here, we consider the evidence with regard to nonhuman primates and other animals to illuminate the evolution of the sense of fairness. Because social ideals escape measurement, we focus on behavioral responses to equal versus unequal reward division. Moreover, a true sense of fairness includes taking account of receiving both less than a partner and more than a partner. Therefore, we consider the evidence for both of these in other species and how this informs our understanding of the evolution of fairness in humans. A diagram of the relationship between first-order IA and second-order IA. Individual A received high-level rewards, and individual B received low-level rewards. Individuals who recognize when they receive less than another may react against this situation—for instance, by finding a new cooperative partner. As reliance on cooperation increases, individuals also benefit from recognizing when they receive more, as this allows them to forestall first-order IA reactions in their partners and thereby maintain a successful cooperative relationship. This is the foundation of the full-blown human sense of fairness. A diagram of the relationship between first-order IA and second-order IA. Individual A received high-level rewards, and individual B received low-level rewards. Individuals who recognize when they receive less than another may react against this situation—for instance, by finding a new cooperative partner. As reliance on cooperation increases, individuals also benefit from recognizing when they receive more, as this allows them to forestall first-order IA reactions in their partners and thereby maintain a successful cooperative relationship. This is the foundation of the full-blown human sense of fairness. Advances There is widespread evidence for sensitivity to receiving less than a partner, or “first-order inequity aversion” (IA), in species that cooperate outside mating bonds and kinship. In these studies, animals are paired with a social partner who receives a preferred reward for completing a task. Subjects may respond by refusing to participate or refusing to accept the food reward, and such reactions are compared with those following control tests in which both subjects receive the same reward for the same effort. Increased responses when the partner receives a preferred reward are indicative of a sensitivity to inequity. Thus far, passive and active protest against unfavorable outcomes has been documented in monkeys, apes, dogs, and birds. It is thought that these species compare their outcomes with those of others so as to judge the merit of their partnerships. They may turn away from partners that appropriate more than their fair share of the yields of cooperation. A complete sense of fairness also includes second-order IA, however, which seeks to equalize outcomes even at a short-term cost to the self. This requires individuals to give up an immediate benefit to stabilize a long-term valuable cooperative relationship. Second-order IA reactions have thus far been found only in humans and apes. We hypothesize that second-order IA requires anticipation of first-order IA in the partner and its negative impact on the relationship. To forestall these consequences, and ensure continued cooperation, outcomes are equalized between partners. Outlook Thus, humans and other species seem to share basic reactions to inequity, which serves to sustain cooperation. We postulate that the basic emotional reactions and calculations underlying our sense of fairness are rooted in our primate background and offer a model that places these reactions in the context of cooperative relationships. Future research should more explicitly investigate the key variables underlying IA, such as the degree of dependence on cooperation, anticipation of the way resource division affects relationships, and the freedom to choose among and change partners. A cross-species investigation with a standardized paradigm, including both first- and second-order IA, may further illuminate the factors involved and help verify or falsify the model proposed. The evolutionary benefits of behaving fairly Humans have a deep and innate sense of fairness. Humans, however, are not the only species to react to apparent inequities. Brosnan and de Waal propose that inequity aversion can be broken down into two levels. At the most basic level, individuals react to immediate unequal distribution of a reward for equal effort expended, whereas at the second, they show the ability to accept a current unequal distribution with the expectation that over time distribution will equalize. This second level facilitates cooperation over time and requires the cognitive abilities both to assess current distribution and envision future opportunities for equalization. As cognitive abilities advanced across the primate lineage, this more complex accounting of equal distribution and cooperation may have developed into the complete sense of fairness we see in humans today. Science, this issue 10.1126/science.1251776 The human sense of fairness is an evolutionary puzzle. To study this, we can look to other species, in which this can be translated empirically into responses to reward distribution. Passive and active protest against receiving less than a partner for the same task is widespread in species that cooperate outside kinship and mating bonds. There is less evidence that nonhuman species seek to equalize outcomes to their own detriment, yet the latter has been documented in our closest relatives, the apes. This reaction probably reflects an attempt to forestall partner dissatisfaction with obtained outcomes and its negative impact on future cooperation. We hypothesize that it is the evolution of this response that allowed the development of a complete sense of fairness in humans, which aims not at equality for its own sake but for the sake of continued cooperation.

Chimpanzees play the ultimatum game

Is the sense of fairness uniquely human? Human reactions to reward division are often studied by means of the ultimatum game, in which both partners need to agree on a distribution for both to receive rewards. Humans typically offer generous portions of the reward to their partner, a tendency our close primate relatives have thus far failed to show in experiments. Here we tested chimpanzees (Pan troglodytes) and human children on a modified ultimatum game. One individual chose between two tokens that, with their partner’s cooperation, could be exchanged for rewards. One token offered equal rewards to both players, whereas the other token favored the chooser. Both apes and children responded like humans typically do. If their partner’s cooperation was required, they split the rewards equally. However, with passive partners—a situation akin to the so-called dictator game—they preferred the selfish option. Thus, humans and chimpanzees show similar preferences regarding reward division, suggesting a long evolutionary history to the human sense of fairness.