Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Non-kin cooperation in bats

Many bats are extremely social. In some cases, individuals remain together for years or even decades and engage in mutually beneficial behaviours among non-related individuals. Here, we summarize ways in which unrelated bats cooperate while roosting, foraging, feeding or caring for offspring. For each situation, we ask if cooperation involves an investment, and if so, what mechanisms might ensure a return. While some cooperative outcomes are likely a by-product of selfish behaviour as they are in many other vertebrates, we explain how cooperative investments can occur in several situations and are particularly evident in food sharing among common vampire bats (Desmodus rotundus) and alloparental care by greater spear-nosed bats (Phyllostomus hastatus). Fieldwork and experiments on vampire bats indicate that sharing blood with non-kin expands the number of possible donors beyond kin and promotes reciprocal help by strengthening long-term social bonds. Similarly, more than 25 years of recapture data and field observations of greater spear-nosed bats reveal multiple cooperative investments occurring within stable groups of non-kin. These studies illustrate how bats can serve as models for understanding how cooperation is regulated in social vertebrates.     

Friendship, cliquishness, and the emergence of cooperation

The evolution of cooperation is a central problem in biology and the social sciences. While theoretical work using the iterated prisoner's dilemma (IPD) has shown that cooperation among non-kin can be sustained among reciprocal strategies (i.e. tit-for-tat), these results are sensitive to errors in strategy execution, cyclical invasions by free riders, and the specific ecology of strategies. Moreover, the IPD assumes that a strategy's probability of playing the PD game with other individuals is independent of the decisions made by others. Here, we remove the assumption of independent pairing by studying a more plausible cooperative dilemma in which players can preferentially interact with a limited set of known partners and also deploy longer-term accounting strategies that can counteract the effects of random errors. We show that cooperative strategies readily emerge and persist in a range of noisy environments, with successful cooperative strategies (henceforth, cliquers) maintaining medium-term memories for partners and low thresholds for acceptable cooperation (i.e. forgiveness). The success of these strategies relies on their cliquishness-a propensity to defect with strangers if they already have an adequate number of partners. Notably, this combination of medium-term accounting, forgiveness, and cliquishness fits with empirical studies of friendship and other long-term relationships among humans.     

The costs and benefits of resource sharing: reciprocity requires resource heterogeneity

The evolution of resource sharing requires that the fitness benefits to the recipients be much higher than the costs to the giver, which requires heterogeneity among individuals in the fitness value of acquiring additional resources. We develop four models of the evolution of resource sharing by either direct or indirect reciprocity, with equal or unequal partners. Evolution of resource sharing by reciprocity requires differences between interacting individuals in the fitness value of the resource, and these differences must reverse although previous acts of giving are remembered and both participants survive. Moreover, inequality in the expected reproductive value of the interacting individuals makes reciprocity more difficult to evolve, but may still allow evolution of sharing by kin selection. These constraints suggest that resource sharing should evolve much more frequently by kin selection than by reciprocity, a prediction that is well supported by observations in the natural world.     

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.     

Cooperation beyond the dyad: on simple models and a complex society

Players in Axelrod and Hamilton''s model of cooperation were not only in a Prisoner''s Dilemma, but by definition, they were also trapped in a dyad. But animals are rarely so restricted and even the option to interact with third parties allows individuals to escape from the Prisoner''s Dilemma into a much more interesting and varied world of cooperation, from the apparently rare ‘parcelling’ to the widespread phenomenon of market effects. Our understanding of by-product mutualism, pseudo-reciprocity and the snowdrift game is also enriched by thinking ‘beyond the dyad’. The concepts of by-product mutualism and pseudo-reciprocity force us to think again about our basic definitions of cooperative behaviour (behaviour by a single individual) and cooperation (the outcome of an interaction between two or more individuals). Reciprocity is surprisingly rare outside of humans, even among large-brained ‘intelligent’ birds and mammals. Are humans unique in having extensive cooperative interactions among non-kin and an integrated cognitive system for mediating reciprocity? Perhaps, but our best chance for finding a similar phenomenon may be in delphinids, which also live in large societies with extensive cooperative interactions among non-relatives. A system of nested male alliances in bottlenose dolphins illustrates the potential and difficulties of finding a complex system of cooperation close to our own.     

Participation costs can suppress the evolution of upstream reciprocity

Indirect reciprocity, one of the many mechanisms proposed to explain the evolution of cooperation, is the idea that altruistic actions can be rewarded by third parties. Upstream or generalized reciprocity is one type of indirect reciprocity in which individuals help someone if they have been helped by somebody else in the past. Although empirically found to be at work in humans, the evolution of upstream reciprocity is difficult to explain from a theoretical point of view. A recent model of upstream reciprocity, first proposed by Nowak and Roch (2007) and further analyzed by Iwagami and Masuda (2010), shows that while upstream reciprocity alone does not lead to the evolution of cooperation, it can act in tandem with mechanisms such as network reciprocity and increase the total level of cooperativity in the population. We argue, however, that Nowak and Roch's model systematically leads to non-uniform interaction rates, where more cooperative individuals take part in more games than less cooperative ones. As a result, the critical benefit-to-cost ratios derived under this model in previous studies are not invariant with respect to the addition of participation costs. We show that accounting for these costs can hinder and even suppress the evolution of upstream reciprocity, both for populations with non-random encounters and graph-structured populations.     

Three-person game facilitates indirect reciprocity under image scoring

Reputation building plays an important role in the evolution of reciprocal altruism when the same individuals do not interact repeatedly because, by referring to reputation, a reciprocator can know which partners are cooperative and can reciprocate with a cooperator. This reciprocity based on reputation is called indirect reciprocity. Previous studies of indirect reciprocity have focused only on two-person games in which only two individuals participate in a single interaction, and have claimed that indirectly reciprocal cooperation cannot be established under image scoring reputation criterion where the reputation of an individual who has cooperated (defected) becomes good (bad). In this study, we specifically examine three-person games, and reveal that indirectly reciprocal cooperation can be formed and maintained stably, even under image scoring, by a nucleus shield mechanism. In the nucleus shield, reciprocators are a shield that keeps out unconditional defectors, whereas unconditional cooperators are the backbone of cooperation that retains a good reputation among the population.     

Cooperation can improve the resilience of common-pool resource systems against over-harvesting

Currently common-pool resource systems world-wide are under pressure due to overexploitation and environmental change. To ensure that these systems continue to provide vital ecosystem services it is necessary to sustain or increase their resilience against such pressure. One way of doing this may be to improve cooperation among agents who are heavily involved in common-pool resource systems, such as farmers, fishers, managers, and companies. Historical examples suggest that the persistence or collapse of common-pool resource systems may hinge on agents collaborating or not, but cooperation as a mechanism to improve resilience is not commonly included in existing models for studying resilience. Cooperation may be sustained through indirect reciprocity, i.e., cooperative behaviour by one agent that may be repaid by other agents. In this paper we develop a suite of agent-based models that represent an abstract version of a generic spatial common-pool resource system. This suite of models contains various mechanisms for cooperation based on trust. We investigate how the resilience of the models is affected by these mechanisms. The resilience of the models is assessed by applying various shocks which make it more difficult to gather resource, and measuring whether and how fast the agent population can recover from these shocks. The results suggest that although indirect reciprocity positively affects the level of cooperation in the system, cooperation could be common even without indirect reciprocity. It is shown that the presence of cooperation increases the resilience of the models against shocks.     

Cooperation among non-relatives evolves by state-dependent generalized reciprocity

For decades, attempts to understand cooperation between non-kin have generated substantial theoretical and empirical interest in the evolutionary mechanisms of reciprocal altruism. There is growing evidence that the cognitive limitations of animals can hinder direct and indirect reciprocity because the necessary mental capacity is costly. Here, we show that cooperation can evolve by generalized reciprocity (help anyone, if helped by someone) even in large groups, if individuals base their decision to cooperate on a state variable updated by the outcome of the last interaction with an anonymous partner. We demonstrate that this alternative mechanism emerges through small evolutionary steps under a wide range of conditions. Since this state-based generalized reciprocity works without advanced cognitive abilities it may help to understand the evolution of complex social behaviour in a wide range of organisms.     

Integrating cooperative breeding into theoretical concepts of cooperation

In cooperative breeding systems, some individuals help to raise offspring that are not their own. While early explanations for such altruistic behaviour were predominantly based on kin selection, recent evidence suggests that direct benefits may be important in the maintenance of cooperation. To date, however, discussions of cooperative breeding have made little reference to more general theories of cooperation between unrelated individuals (while these theories rarely address cooperative breeding). Here, we attempt to integrate the two fields. We identify four key questions that can be used to categorise different mechanisms for the maintenance of cooperative behaviour: (1) whether or not individuals invest in others; (2) whether or not this initial investment elicits a return investment by the beneficiary; (3) whether the interaction is direct, i.e. between two partners, or indirect (involving third parties) and (4) whether only actions that increase the fitness of the partner or also fitness reducing actions (punishment) are involved in the interaction. Asking these questions with regards to concepts in the literature on cooperative breeding, we found that (a) it is often straightforward to relate these concepts to general mechanisms of cooperation, but that (b) a single term (such as 'pay-to-stay', 'group augmentation' or 'prestige') may sometimes subsume two or more distinct mechanisms, and that (c) at least some mechanisms that are thought to be important in cooperative breeding systems have remained largely unexplored in the theoretical literature on the evolution of cooperation. Future theoretical models should incorporate asymmetries in power and pay off structure caused for instance by dominance hierarchies or partner choice, and the use of N-player games. The key challenges for both theoreticians and empiricists will be to integrate the hitherto disparate fields and to disentangle the parallel effects of kin and non-kin based mechanisms of cooperation.     

Revisiting “The Evolution of Reciprocity in Sizable Groups”: Continuous reciprocity in the repeated n-person prisoner's dilemma

For many years in evolutionary science, the consensus view has been that while reciprocal altruism can evolve in dyadic interactions, it is unlikely to evolve in sizable groups. This view had been based on studies which have assumed cooperation to be discrete rather than continuous (i.e., individuals can either fully cooperate or else fully defect, but they cannot continuously vary their level of cooperation). In real world cooperation, however, cooperation is often continuous. In this paper, we re-examine the evolution of reciprocity in sizable groups by presenting a model of the n-person prisoner's dilemma that assumes continuous rather than discrete cooperation. This model shows that continuous reciprocity has a dramatically wider basin of attraction than discrete reciprocity, and that this basin's size increases with efficiency of cooperation (marginal per capita return). Further, we find that assortative interaction interacts synergistically with continuous reciprocity to a much greater extent than it does with discrete reciprocity. These results suggest that previous models may have underestimated reciprocity's adaptiveness in groups. However, we also find that the invasion of continuous reciprocators into a population of unconditional defectors becomes realistic only within a narrow parameter space in which the efficiency of cooperation is close to its maximum bound. Therefore our model suggests that continuous reciprocity can evolve in large groups more easily than discrete reciprocity only under unusual circumstances.     

A tale of two defectors: the importance of standing for evolution of indirect reciprocity

Indirect reciprocity occurs when the cooperative behavior between two individuals is contingent on their previous behavior toward others. Previous theoretical analysis indicates that indirect reciprocity can evolve if individuals use an image-scoring strategy. In this paper, we show that, when errors are added, indirect reciprocity cannot be based on an image-scoring strategy. However, if individuals use a standing strategy, then cooperation through indirect reciprocity is evolutionarily stable. These two strategies differ with respect to the information to which they attend. While image-scoring strategies only need attend to the actions of others, standing strategies also require information about intent. We speculate that this difference may shed light on the evolvability of indirect reciprocity. Additionally, we show that systems of indirect reciprocity are highly sensitive to the availability of information. Finally, we present a model which shows that if indirect reciprocity were to evolve, selection should also favor trusting behavior in relations between strangers.     

Sexual Selection of Human Cooperative Behaviour: An Experimental Study in Rural Senegal

Human cooperation in large groups and between non-kin individuals remains a Darwinian puzzle. Investigations into whether and how sexual selection is involved in the evolution of cooperation represent a new and important research direction. Here, 69 groups of four men or four women recruited from a rural population in Senegal played a sequential public-good game in the presence of out-group observers, either of the same sex or of the opposite sex. At the end of the game, participants could donate part of their gain to the village school in the presence of the same observers. Both contributions to the public good and donations to the school, which reflect different components of cooperativeness, were influenced by the sex of the observers. The results suggest that in this non-Western population, sexual selection acts mainly on men’s cooperative behaviour with non-kin, whereas women’s cooperativeness is mainly influenced by nonsexual social selection.     

On the further integration of cooperative breeding and cooperation theory

We present a synopsis about the commentaries to the target article "Integrating cooperative breeding into theoretical concepts of cooperation", in which we attempted to integrate general mechanisms to explain cooperative behaviour among unrelated individuals with classic concepts to explain helping behaviour in cooperative breeders that do not invoke kin-based benefits. Here we (1) summarize the positions of the commentators concerning the main issues we raised in the target article and discuss important criticisms and extensions. (2) We relate our target article to some recent reviews on the evolution of cooperation and, (3) clarify how we use terminology with regard to cooperation and cooperative behaviour. (4) We discuss several aspects that were raised with respect to cooperative interactions including by-product mutualism, generalised reciprocity and multi-level selection and, (5) examine the alternatives to our classification scheme as proposed by some commentaries. (6) Finally, we highlight several aspects that might hinder the application of game theoretical mechanisms of cooperation in cooperatively breeding systems. Although there is broad agreement that cooperative breeding theory should be integrated within the more general concepts of cooperation, there is some debate about how this may be achieved. We conclude that the contributions in this special issue provide a fruitful first step and ample suggestions for future directions with regard to a more unified framework of cooperation in cooperative breeders.     

Schoolchildren cooperate more successfully with non-kin than with siblings

Cooperation plays a key role in the development of advanced societies and can be stabilized through shared genes (kinship) or reciprocation. In humans, cooperation among kin occurs more readily than cooperation among non-kin. In many organisms, cooperation can shift with age (e.g. helpers at the nest); however, little is known about developmental shifts between kin and non-kin cooperation in humans. Using a cooperative game, we show that 3- to 10-year-old French schoolchildren cooperated less successfully with siblings than with non-kin children, whether or not non-kin partners were friends. Furthermore, children with larger social networks cooperated better and the perception of friendship among non-friends improved after cooperating. These results contrast with the well-established preference for kin cooperation among adults and indicate that non-kin cooperation in humans might serve to forge and extend non-kin social relationships during middle childhood and create opportunities for future collaboration beyond kin. Our results suggest that the current view of cooperation in humans may only apply to adults and that future studies should focus on how and why cooperation with different classes of partners might change during development in humans across cultures as well as other long-lived organisms.     

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.     

Resolving the iterated prisoner's dilemma: theory and reality

Pairs of unrelated individuals face a prisoner's dilemma if cooperation is the best mutual outcome, but each player does best to defect regardless of his partner's behaviour. Although mutual defection is the only evolutionarily stable strategy in one-shot games, cooperative solutions based on reciprocity can emerge in iterated games. Among the most prominent theoretical solutions are the so-called bookkeeping strategies, such as tit-for-tat, where individuals copy their partner's behaviour in the previous round. However, the lack of empirical data conforming to predicted strategies has prompted the suggestion that the iterated prisoner's dilemma (IPD) is neither a useful nor realistic basis for investigating cooperation. Here, we discuss several recent studies where authors have used the IPD framework to interpret their data. We evaluate the validity of their approach and highlight the diversity of proposed solutions. Strategies based on precise accounting are relatively uncommon, perhaps because the full set of assumptions of the IPD model are rarely satisfied. Instead, animals use a diverse array of strategies that apparently promote cooperation, despite the temptation to cheat. These include both positive and negative reciprocity, as well as long-term mutual investments based on 'friendships'. Although there are various gaps in these studies that remain to be filled, we argue that in most cases, individuals could theoretically benefit from cheating and that cooperation cannot therefore be explained with the concept of positive pseudo-reciprocity. We suggest that by incorporating empirical data into the theoretical framework, we may gain fundamental new insights into the evolution of mutual reciprocal investment in nature.     

Evolutionary game theory meets social science: Is there a unifying rule for human cooperation?

Evolutionary game theory has shown that human cooperation thrives in different types of social interactions with a PD structure. Models treat the cooperative strategies within the different frameworks as discrete entities and sometimes even as contenders. Whereas strong reciprocity was acclaimed as superior to classic reciprocity for its ability to defeat defectors in public goods games, recent experiments and simulations show that costly punishment fails to promote cooperation in the IR and DR games, where classic reciprocity succeeds. My aim is to show that cooperative strategies across frameworks are capable of a unified treatment, for they are governed by a common underlying rule or norm. An analysis of the reputation and action rules that govern some representative cooperative strategies both in models and in economic experiments confirms that the different frameworks share a conditional action rule and several reputation rules. The common conditional rule contains an option between costly punishment and withholding benefits that provides alternative enforcement methods against defectors. Depending on the framework, individuals can switch to the appropriate strategy and method of enforcement. The stability of human cooperation looks more promising if one mechanism controls successful strategies across frameworks.     

Cooperation under indirect reciprocity and imitative trust

Indirect reciprocity, a key concept in behavioral experiments and evolutionary game theory, provides a mechanism that allows reciprocal altruism to emerge in a population of self-regarding individuals even when repeated interactions between pairs of actors are unlikely. Recent empirical evidence show that humans typically follow complex assessment strategies involving both reciprocity and social imitation when making cooperative decisions. However, currently, we have no systematic understanding of how imitation, a mechanism that may also generate negative effects via a process of cumulative advantage, affects cooperation when repeated interactions are unlikely or information about a recipient's reputation is unavailable. Here we extend existing evolutionary models, which use an image score for reputation to track how individuals cooperate by contributing resources, by introducing a new imitative-trust score, which tracks whether actors have been the recipients of cooperation in the past. We show that imitative trust can co-exist with indirect reciprocity mechanisms up to a threshold and then cooperation reverses -revealing the elusive nature of cooperation. Moreover, we find that when information about a recipient's reputation is limited, trusting the action of third parties towards her (i.e. imitating) does favor a higher collective cooperation compared to random-trusting and share-alike mechanisms. We believe these results shed new light on the factors favoring social imitation as an adaptive mechanism in populations of cooperating social actors.