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. 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.

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.

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.

The insight that animals' cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners' ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.