From reciprocity to unconditional altruism through signalling benefits

Cooperation among genetically unrelated individuals is commonly explained by the potential for future reciprocity or by the risk of being punished by group members. However, unconditional altruism is more difficult to explain. We demonstrate that unconditional altruism can evolve as a costly signal of individual quality (i.e. a handicap) as a consequence of reciprocal altruism. This is because the emergent correlation between altruism and individual quality in reciprocity games can facilitate the use of altruism as a quality indicator in a much wider context, outside the reciprocity game, thus affecting its further evolution through signalling benefits. Our model, based on multitype evolutionary game theory shows that, when the additive signalling benefit of donating help exceeds the cost for only some individuals (of high-quality state) but not for others (of low-quality state), the population possesses an evolutionarily stable strategy (ESS) profile wherein high-quality individuals cooperate unconditionally while low-quality individuals defect or play tit-for-tat (TfT). Hence, as predicted by Zahavi's handicap model, signalling benefits of altruistic acts can establish a stable generosity by high-quality individuals that no longer depends on the probability of future reciprocation or punishment.     

The concepts of asymmetric and symmetric power can help resolve the puzzle of altruistic and cooperative behaviour

Evolutionary theory predicts competition in nature yet altruistic and cooperative behaviour appears to reduce the ability to compete in order to help others compete better. This evolutionary puzzle is usually explained by kin selection where close relatives perform altruistic and cooperative acts to help each other and by reciprocity theory (i.e. direct, indirect and generalized reciprocity) among non‐kin. Here, it is proposed that the concepts of asymmetry and symmetry in power and dominance are critical if we are ever to resolve the puzzle of altruism and cooperation towards non‐kin. Asymmetry in power and dominance is likely to emerge under competition in nature as individuals strive to gain greater access to the scarce resources needed to survive and reproduce successfully. Yet asymmetric power presents serious problems for reciprocity theory in that a dominant individual faces a temptation to cheat in interactions with subordinates that is likely to far outweigh any individual selective benefits gained through reciprocal mechanisms. Furthermore, action taken by subordinates to deter non‐reciprocation by dominants is likely to prove prohibitively costly to their fitness, making successful enforcement of reciprocal mechanisms unlikely. It is also argued here that many apparently puzzling forms of cooperation observed in nature (e.g. cooperative breeding in which unrelated subordinates help dominants to breed) might be best explained by asymmetry in power and dominance. Once it is recognized that individuals in these cooperative interactions are subject to the constraints and opportunities imposed on them by asymmetric power then they can be seen as pursuing a ‘least bad’ strategy to promote individual fitness – one that is nevertheless consistent with evolutionary theory. The concept of symmetric power also provides important insights. It can inhibit reciprocal mechanisms in the sense that symmetric power makes it easier for a cheat to appropriate common resources while incurring fewer penalties. Nevertheless under certain restrictive conditions, symmetric power is seen as likely to promote direct reciprocity through ‘tit for tat’.     

The evolution of generalized reciprocity on social interaction networks

Generalized reciprocity (help anyone, if helped by someone) is a minimal strategy capable of supporting cooperation between unrelated individuals. Its simplicity makes it an attractive model to explain the evolution of reciprocal altruism in animals that lack the information or cognitive skills needed for other types of reciprocity. Yet, generalized reciprocity is anonymous and thus defenseless against exploitation by defectors. Recognizing that animals hardly ever interact randomly, we investigate whether social network structure can mitigate this vulnerability. Our results show that heterogeneous interaction patterns strongly support the evolution of generalized reciprocity. The future probability of being rewarded for an altruistic act is inversely proportional to the average connectivity of the social network when cooperators are rare. Accordingly, sparse networks are conducive to the invasion of reciprocal altruism. Moreover, the evolutionary stability of cooperation is enhanced by a modular network structure. Communities of reciprocal altruists are protected against exploitation, because modularity increases the mean access time, that is, the average number of steps that it takes for a random walk on the network to reach a defector. Sparseness and community structure are characteristic properties of vertebrate social interaction patterns, as illustrated by network data from natural populations ranging from fish to primates.     

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.     

Reputation-based partner choice is an effective alternative to indirect reciprocity in solving social dilemmas

When group interests clash with individual ones, maintaining cooperation poses a problem. However, cooperation can be facilitated by introducing reputational incentives. Through indirect reciprocity, people who cooperate in a social dilemma are more likely to receive cooperative acts from others. Another mechanism that enhances group cooperation is reputation-based partner choice, or competitive altruism. According to this framework, cooperators benefit via increased access to cooperative partners. Our study compared the effectiveness of indirect reciprocity and competitive altruism in re-establishing cooperation after the typical decline found during repeated public goods games. Twenty groups of four participants first played a series of public goods games, which confirmed the expected decline. Subsequently, public goods games were alternated with either indirect reciprocity games (in which participants had an opportunity to give to another individual from whom they would never receive a direct return) or competitive altruism games (in which they could choose partners for directly reciprocal interactions). We found that public goods game contributions increased when interspersed with competitive altruism games; they were also higher than in public goods games interspersed with indirect reciprocity games. Investing in reputation by increasing contributions to public goods was a profitable strategy in that it increased returns in subsequent competitive altruism and indirect reciprocity games. There was also some evidence that these returns were greater under competitive altruism than indirect reciprocity. Our findings indicate that strategic reputation building through competitive altruism provides an effective alternative to indirect reciprocity as a means for restoring cooperation in social dilemmas.     

Distinctions among reciprocal altruism,kin selection,and cooperation and a model for the initial evolution of beneficent behavior

Reciprocal altruism is usually regarded as distinct from kin selection. However, because reciprocators are likely to establish long-term relations and to deliver most of their aid to other individuals genetically predisposed to reciprocation, most acts of reciprocal altruism should involve indirect increments to inclusive fitness, at least as regards alleles for reciprocation. Thus, as usually defined, reciprocal altruism is not clearly distinct from kin selection because both involve indirect increments to inclusive fitness. We propose a new definition for reciprocal altruism that makes the phenomenon distinct from kin selection and allows for reciprocation between nonrelatives in which current costs exceed future benefits returned to the reciprocal altruist. Cooperation and reciprocal altruism are often considered synonymous or different only in the timing of donating and receiving aid. We show, however, that there are other critical differences between reciprocal altruism and other forms of cooperation, most importantly, the latter often involve no clearly identifiable aid. We propose a four-category system to encompass the range of cooperative and beneficent behaviors that occur in nature (reciprocal altruism, pseudoreciprocity, simultaneous cooperation and by-product beneficence). Reciprocal altruism must involve aid that is returned to an original donor as a result of behavior that has a net cost to an original recipient. Our simplest category of cooperative/beneficent behavior, “by-product beneficence,” occurs when a selfish act also benefits another individual and requires no prior or subsequent interactions between the individuals involved. By-product beneficence may be the primitive state from which more complicated types of cooperative/beneficent behavior evolved. We show via simple models that by-product beneficence can allow for the initial increase of helping behavior in a completely unstructured population although the individuals showing such behavior pay all the costs while sharing the benefits with other individuals. Previous models that attempted to explain the initial increase of cooperative/beneficent behavior were much more complex and were based on the prisoner's dilemma, which does not accurately reflect most forms of cooperation and beneficence that occur in nature.     

Indirect reciprocity among imperfect individuals

Reciprocal cooperation occurs when the overall benefits of receiving help exceed the costs of donating help (Q. Rev. Biol. 46 (197) 35). That is, individuals in good condition--for whom the pertinent costs are relatively small; donate help in order to secure reciprocity in their hour of need--when the benefits of receiving a donation are large. Consequently, reciprocity occurs among individuals who occasionally need help. In particular, such individuals will be unable to help others, no matter how deserving, when in need of help themselves--involuntary defection. This paper deals with the effects of involuntary defection in the context of a specific model of indirect reciprocity (i.e. reciprocal altruism that is directed toward all the cooperative members of the community) due to Nowak and Sigmund (J. Theor. Biol.194 (1998b) 561: Sections 2-4). In that model, the authors formulate the decision rules for conditional cooperation in the context of indirect reciprocity, and demonstrate that these decision rules can account for a long-term persistence of cooperation. Here we show that addition of involuntary defection to the decision rules formulated by Nowak and Sigmund results in indirect reciprocity that is evolutionary stable under appropriate conditions. Moreover, for a wide range of parameter values, evolutionary stability of cooperation requires a mixture of conditional- and unconditional-altruist behaviors. To recollect, unconditional altruist strategy can be viewed as conditional altruist strategy sans the ability to decide when the help-soliciting individual should be refused help. That is, given involuntary defection, stability of cooperation requires an occasional forgiveness, if only by default, of a failure to donate help. Thus, we see that evolutionary stable indirect reciprocity does not require perfection in either the ability to assess the merits of the help-soliciting individuals, or the ability to donate help when it is merited. On the contrary, we are forced to conclude that reciprocity, at least in the current case, is stable only among imperfect individuals.     

Evolution of indirect reciprocity by social information: the role of trust and reputation in evolution of altruism

The complexity of human's cooperative behavior cannot be fully explained by theories of kin selection and group selection. If reciprocal altruism is to provide an explanation for altruistic behavior, it would have to depart from direct reciprocity, which requires dyads of individuals to interact repeatedly. For indirect reciprocity to rationalize cooperation among genetically unrelated or even culturally dissimilar individuals, information about the reputation of individuals must be assessed and propagated in a population. Here, we propose a new framework for the evolution of indirect reciprocity by social information: information selectively retrieved from and propagated through dynamically evolving networks of friends and acquaintances. We show that for indirect reciprocity to be evolutionarily stable, the differential probability of trusting and helping a reputable individual over a disreputable individual, at a point in time, must exceed the cost-to-benefit ratio of the altruistic act. In other words, the benefit received by the trustworthy must out-weigh the cost of helping the untrustworthy.     

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.     

Competitive altruism: from reciprocity to the handicap principle

Current work on cooperation is focused on the theory of reciprocal altruism. However, reciprocity is just one way of getting a return on an investment in altruism and is difficult to apply to many examples. Reciprocity theory addresses how animals respond dynamically to others so as to cooperate without being exploited. I discuss how introducing differences in individual generosity together with partner choice into models of reciprocity can lead to an escalation in altruistic behaviour. Individuals may compete for the most altruistic partners and non-altruists may become ostracized. I refer to this phenomenon as competitive altruism and propose that it can represent a move away from the dynamic responsiveness of reciprocity. Altruism may be rewarded in kind, but rewards may be indirectly accrued or may not involve the return of altruism at all, for example if altruists tend to be chosen as mates. This variety makes the idea of competitive altruism relevant to behaviours which cannot be explained by reciprocity. I consider whether altruism might act as a signal of quality, as proposed by the handicap principle. I suggest that altruistic acts could make particularly effective signals because of the inherent benefits to receivers. I consider how reciprocity and competitive altruism are related and how they may be distinguished.     

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.     

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.     

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. Sarah F. Brosnan is a graduate student in the Population Biology, Ecology, and Evolution Program at Emory University. Her interests include proximate mechanisms of cooperation and reciprocity in primates, and social learning in primates and other species. Frans B. M. de Waal is the C. H. Candler Professor of Psychology and the director of the Living Links Center at Emory University. His interests include social behavior and cognition of monkeys and apes, and their relevance for questions on the evolution of human politics, economy, morality, and culture.     

Reciprocal altruism in birds: A critical review

Many proposed examples of reciprocal altruism are either misidentified or involve questionable assumptions concerning the costs and benefits accruing to the interactors. Waltz's (Am. Nat. 118: 588–592, 1981) definition of reciprocal altruism as an interaction in which “one individual aids another in anticipation that the recipient will return the favor benefiting the actor in the future” is not sufficiently restrictive: there must also be a direct fitness cost to the individual performing the original beneficent act that is less than the fitness benefit received when the act is reciprocated (again at a cost) by the second individual.Several recurring problems in identifying potential examples of reciprocal altruism are discussed, including the assumption that restraint is an act of altruism and the misclassification of “generational mutualisms,” in which individuals helping to raise young are “repaid” one generation later by the offspring they assisted in raising. No definite case of reciprocal altruism is currently known in birds, but examples in which this phenomenon may be involved include helping behavior in a few cooperative breeders and communal feeding in several taxa including gulls, jays, and juncos.     

Evolution of spite through indirect reciprocity

How can cooperation persist in the face of a temptation to ''cheat''? Several recent papers have suggested that the answer may lie in indirect reciprocity. Altruistic individuals may benefit by eliciting altruism from observers, rather than (as in direct reciprocity) from the recipient of the aid they provide. Here, we point out that indirect reciprocity need not always favour cooperation; by contrast, it may support spiteful behaviour, which is costly for the both actor and recipient. Existing theory suggests spite is unlikely to persist, but we demonstrate that it may do so when spiteful individuals are less likely to incur aggression from observers (a negative form of indirect reciprocity).     

Natural selection of cooperation and degree hierarchy in heterogeneous populations

One of the current theoretical challenges to the explanatory powers of Evolutionary Theory is the understanding of the observed evolutionary survival of cooperative behavior when selfish actions provide higher fitness (reproductive success). In unstructured populations natural selection drives cooperation to extinction. However, when individuals are allowed to interact only with their neighbors, specified by a graph of social contacts, cooperation-promoting mechanisms (known as lattice reciprocity) offer to cooperation the opportunity of evolutionary survival. Recent numerical works on the evolution of Prisoner's Dilemma in complex network settings have revealed that graph heterogeneity dramatically enhances the lattice reciprocity. Here we show that in highly heterogeneous populations, under the graph analog of replicator dynamics, the fixation of a strategy in the whole population is in general an impossible event, for there is an asymptotic partition of the population in three subsets, two in which fixation of cooperation or defection has been reached and a third one which experiences cycles of invasion by the competing strategies. We show how the dynamical partition correlates with connectivity classes and characterize the temporal fluctuations of the fluctuating set, unveiling the mechanisms stabilizing cooperation in macroscopic scale-free structures.     

Chaos, oscillation and the evolution of indirect reciprocity in n-person games

Evolution of cooperation among genetically unrelated individuals has been of considerable concern in various fields such as biology, economics, and psychology. The evolution of cooperation is often explained by reciprocity. Under reciprocity, cooperation can prevail in a society because a donor of cooperation receives reciprocation from the recipient of the cooperation, called direct reciprocity, or from someone else in the community, called indirect reciprocity. Nowak and Sigmund [1993. Chaos and the evolution of cooperation. Proc. Natl. Acad. Sci. USA 90, 5091-5094] have demonstrated that directly reciprocal cooperation in two-person prisoner's dilemma games with mutation of strategies can be maintained dynamically as periodic or chaotic oscillation. Furthermore, Eriksson and Lindgren [2005. Cooperation driven by mutations in multi-person Prisoner's Dilemma. J. Theor. Biol. 232, 399-409] have reported that directly reciprocal cooperation in n-person prisoner's dilemma games (n>2) can be maintained as periodic oscillation. Is dynamic cooperation observed only in direct reciprocity? Results of this study show that indirectly reciprocal cooperation in n-person prisoner's dilemma games can be maintained dynamically as periodic or chaotic oscillation. This is, to our knowledge, the first demonstration of chaos in indirect reciprocity. Furthermore, the results show that oscillatory dynamics are observed in common in the evolution of reciprocal cooperation whether for direct or indirect.     

Altruism may arise from individual selection

The fact that humans cooperate with non-kin in large groups, or with people they will never meet again, is a long-standing evolutionary puzzle. Altruism, the capacity to perform costly acts that confer benefits on others, is at the core of cooperative behavior. Behavioral experiments show that humans have a predisposition to cooperate with others and to punish non-cooperators at personal cost (so-called strong reciprocity) which, according to standard evolutionary game theory arguments, cannot arise from selection acting on individuals. This has led to the suggestion of group and cultural selection as the only mechanisms that can explain the evolutionary origin of human altruism. We introduce an agent-based model inspired on the Ultimatum Game, that allows us to go beyond the limitations of standard evolutionary game theory and show that individual selection can indeed give rise to strong reciprocity. Our results are consistent with the existence of neural correlates of fairness and in good agreement with observations on humans and monkeys.     

A neural basis for social cooperation

Cooperation based on reciprocal altruism has evolved in only a small number of species, yet it constitutes the core behavioral principle of human social life. The iterated Prisoner's Dilemma Game has been used to model this form of cooperation. We used fMRI to scan 36 women as they played an iterated Prisoner's Dilemma Game with another woman to investigate the neurobiological basis of cooperative social behavior. Mutual cooperation was associated with consistent activation in brain areas that have been linked with reward processing: nucleus accumbens, the caudate nucleus, ventromedial frontal/orbitofrontal cortex, and rostral anterior cingulate cortex. We propose that activation of this neural network positively reinforces reciprocal altruism, thereby motivating subjects to resist the temptation to selfishly accept but not reciprocate favors.     

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.