Competitive helping increases with the size of biological markets and invades defection

Cooperation between unrelated individuals remains a puzzle in evolutionary biology. Recent work indicates that partner choice can select for high levels of helping. More generally, helping can be seen as but one strategy used to compete for partners within a broader biological market, yet giving within such markets has received little mathematical investigation. In the present model, individuals help others to attract attention from them and thus receive a larger share of any help actively or passively provided by those others. The evolutionarily stable level of helping increases with the size of the biological market and the degree of partner choice. Furthermore, if individuals passively produce some no-cost help to partners, competitive helping can then invade populations of non-helpers because helpers directly benefit from increasing their access to potential partners. This framework of competitive helping demonstrates how high helping can be achieved and why different populations may differ in helping levels.     

How conception risk affects competition and cooperation with attractive women and men

We investigated competition and cooperation for resources across the menstrual cycle in the context of bargaining games. Although bargaining has been studied within an evolutionary framework, little attention has been paid specifically to the role of mating motives in economic behavior. To investigate how motives related to reproductive success affect bargaining, participants at high or low risk for conception or who were on oral contraceptives played ultimatum and dictator games with partners who varied in sex and facial attractiveness. In ultimatum games, women in the fertile phase were more competitive over resources with attractive women than with less attractive women. Intrasexual competition was not observed in dictator games. Women were more cooperative with attractive men than with less attractive men in both games, regardless of fertility status. Low fertility women were more cooperative with attractive members than with less attractive members of both sexes in both games. Results support the view that, during periods of high fertility, when women are most intrasexually competitive for mates, withholding resources from potential rivals would enable women to gain the means to enhance their attractiveness and weaken competitors' abilities to do the same at a time when relative advantages in appearance are most crucial to reproductive success. The lack of a fertility effect for cooperation with potential mates supports the view that displays of generosity accrue benefits for women across the cycle in their efforts to attract men who will invest in relationships.     

Biological markets

In biological markets, two classes of traders exchange commodities to their mutual benefit. Characteristics of markets are: competition within trader classes by contest or outbidding; preference for partners offering the highest value; and conflicts over the exchange value of commodities. Biological markets are currently studied under at least three different headings: sexual selection, intraspecific cooperation and interspecific mutualism. The time is ripe for the development of game theoretic models that describe the common core of biological markets and integrate existing knowledge from the separate fields.     

Targeted Cooperative Actions Shape Social Networks

Individual acts of cooperation give rise to dynamic social networks. Traditionally, models for cooperation in structured populations are based on a separation of individual strategies and of population structure. Individuals adopt a strategy—typically cooperation or defection, which determines their behaviour toward their neighbours as defined by an interaction network. Here, we report a behavioural experiment that amalgamates strategies and structure to empirically investigate the dynamics of social networks. The action of paying a cost c to provide a benefit b is represented as a directed link point from the donor to the recipient. Participants can add and/or remove links to up to two recipients in each round. First, we show that dense networks emerge, where individuals are characterized by fairness: they receive to the same extent they provide. More specifically, we investigate how participants use information about the generosity and payoff of others to update their links. It turns out that aversion to payoff inequity was the most consistent update rule: adding links to individuals that are worse off and removing links to individuals that are better off. We then investigate the effect of direct reciprocation, showing that the possibility of direct reciprocation does not increase cooperation as compared to the treatment where participants are totally unaware of who is providing benefits to them.     

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.     

Exploring the causes and consequences of cooperative behaviour in wild animal populations using a social network approach

Understanding why individuals carry out behaviours that benefit others, especially genetically unrelated others, has been a major undertaking in many fields and particularly in biology. Here, we focus on the cooperation literature from natural populations and present the benefits of a social network approach in terms of how it can help to identify and understand factors that influence the maintenance and spread of cooperation, but are not easily captured when solely considering independent dyadic interactions. We describe how various routes to cooperation can be tested within the social network framework. Applying the social network approach to data from natural populations can help to uncover the evolutionary and ecological pressures that lead to differences in cooperation and other social processes.     

A BIOLOGICAL MARKET ANALYSIS OF THE PLANT‐MYCORRHIZAL SYMBIOSIS

It has been argued that cooperative behavior in the plant‐mycorrhizal mutualism resembles trade in a market economy and can be understood using economic tools. Here, we assess the validity of this “biological market” analogy by investigating whether a market mechanism—that is, competition between partners over the price at which they provide goods—could be the outcome of natural selection. Then, we consider the conditions under which this market mechanism is sufficient to maintain mutualistic trade. We find that: (i) as in a market, individuals are favored to divide resources among trading partners in direct relation to the relative amount of resources received, termed linear proportional discrimination; (ii) mutualistic trade is more likely to be favored when individuals are able to interact with more partners of both species, and when there is a greater relative difference between the species in their ability to directly acquire different resources; (iii) if trade is favored, then either one or both species is favored to give up acquiring one resource directly, and vice versa. We then formulate testable predictions as to how environmental changes and coevolved responses of plants and mycorrhizal fungi will influence plant fitness (crop yields) in agricultural ecosystems.     

Partner choice creates competitive altruism in humans

Reciprocal altruism has been the backbone of research on the evolution of altruistic behaviour towards non-kin, but recent research has begun to apply costly signalling theory to this problem. In addition to signalling resources or abilities, public generosity could function as a costly signal of cooperative intent, benefiting altruists in terms of (i) better access to cooperative relationships and (ii) greater cooperation within those relationships. When future interaction partners can choose with whom they wish to interact, this could lead to competition to be more generous than others. Little empirical work has tested for the possible existence of this 'competitive altruism'. Using a cooperative monetary game with and without opportunities for partner choice and signalling cooperative intent, we show here that people actively compete to be more generous than others when they can benefit from being chosen for cooperative partnerships, and the most generous people are correspondingly chosen more often as cooperative partners. We also found evidence for increased scepticism of altruistic signals when the potential reputational benefits for dishonest signalling were high. Thus, this work supports the hypothesis that public generosity can be a signal of cooperative intent, which people sometimes 'fake' when conditions permit it.     

An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction

Mutualisms can be viewed as biological markets in which partners of different species exchange goods and services to their mutual benefit. Trade between partners with conflicting interests requires mechanisms to prevent exploitation. Partner choice theory proposes that individuals might foil exploiters by preferentially directing benefits to cooperative partners. Here, we test this theory in a wild legumerhizobium symbiosis. Rhizobial bacteria inhabit legume root nodules and convert atmospheric dinitrogen (N2) to a plant available form in exchange for photosynthates. Biological market theory suits this interaction because individual plants exchange resources with multiple rhizobia. Several authors have argued that microbial cooperation could be maintained if plants preferentially allocated resources to nodules harbouring cooperative rhizobial strains. It is well known that crop legumes nodulate non-fixing rhizobia, but allocate few resources to those nodules. However, this hypothesis has not been tested in wild legumes which encounter partners exhibiting natural, continuous variation in symbiotic benefit. Our greenhouse experiment with a wild legume, Lupinus arboreus, showed that although plants frequently hosted less cooperative strains, the nodules occupied by these strains were smaller. Our survey of wild-grown plants showed that larger nodules house more Bradyrhizobia, indicating that plants may prevent the spread of exploitation by favouring better cooperators.     

Empirical tests of reciprocity theory: Problems in assessment

Observations and experiments designed to test Trivers' (1971) theory of reciprocal altruism face two difficulties. First, in many cases the costs and benefits of behaviors being exchanged cannot be expressed directly in terms of effects on the actors' fitness. This is particularly true when an exchange of cooperative acts involves different types of behavior, such as grooming and alliance formation in non-human primates. Second, in many social groups individuals differ widely in their ability to confer benefits on others. High-ranking animals can, for example, offer greater assistance than low-ranking animals and adults can help offspring more than offspring can help adults. As a result, what appears not to be a reciprocal interaction from the observer's point of view may in fact support Trivers' theory when costs and benefits are calculated from the animals' own perspectives. We discuss these issues with special reference to our own experiments on reciprocal exchanges of grooming and alliance formation in free-ranging vervet monkeys.     

Cooperating in the face of uncertainty: a consistent framework for understanding the evolution of cooperation

The evolution of cooperative behaviour, whereby individuals enhance the fitness of others at an apparent cost to themselves, represents one of the greatest paradoxes of evolution. Individuals that engage in such cooperative behaviour can, however, be favoured by natural selection if cooperative actions confer higher fitness than alternative actions. To understand the evolution of cooperative behaviour, the direct and indirect genetic benefits that individuals accrue in the present and future must be summed - this can be accomplished without any reference to the colorful vocabulary typically associated with studies of cooperation. When benefits are accrued indirectly through relatives or directly in the future individuals must be able to assess and enhance their probability of accruing those benefits and behave accordingly. We suggest that, in the same way that studies of kin recognition systems improved our understanding of how individuals assess and enhance their probability of accruing indirect benefits, studies of various forms of inheritance and reciprocation recognition systems will improve our understanding of how individuals assess and enhance their probability of accruing future benefits. Recognizing the parallel between studies of indirect fitness and future fitness, at multiple levels of analysis, will move us toward a simpler and more consistent framework for understanding the evolution of cooperative behaviour.     

Charitable giving as a signal of trustworthiness: Disentangling the signaling benefits of altruistic acts

It has been shown that psychological predispositions to benefit others can motivate human cooperation and the evolution of such social preferences can be explained with kin or multi-level selection models. It has also been shown that cooperation can evolve as a costly signal of an unobservable quality that makes a person more attractive with regard to other types of social interactions. Here we show that if a proportion of individuals with social preferences is maintained in the population through kin or multi-level selection, cooperative acts that are truly altruistic can be a costly signal of social preferences and make altruistic individuals more trustworthy interaction partners in social exchange. In a computerized laboratory experiment, we test whether altruistic behavior in the form of charitable giving is indeed correlated with trustworthiness and whether a charitable donation increases the observing agents' trust in the donor. Our results support these hypotheses and show that, apart from trust, responses to altruistic acts can have a rewarding or outcome-equalizing purpose. Our findings corroborate that the signaling benefits of altruistic acts that accrue in social exchange can ease the conditions for the evolution of social preferences.     

Selection for cheating across disparate environments in the legume‐rhizobium mutualism

The primary dilemma in evolutionarily stable mutualisms is that natural selection for cheating could overwhelm selection for cooperation. Cheating need not entail parasitism; selection favours cheating as a quantitative trait whenever less‐cooperative partners are more fit than more‐cooperative partners. Mutualisms might be stabilised by mechanisms that direct benefits to more‐cooperative individuals, which counter selection for cheating; however, empirical evidence that natural selection favours cheating in mutualisms is sparse. We measured selection on cheating in single‐partner pairings of wild legume and rhizobium lineages, which prevented legume choice. Across contrasting environments, selection consistently favoured cheating by rhizobia, but did not favour legumes that provided less benefit to rhizobium partners. This is the first simultaneous measurement of selection on cheating across both host and symbiont lineages from a natural population. We empirically confirm selection for cheating as a source of antagonistic coevolutionary pressure in mutualism and a biological dilemma for models of cooperation.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.     

A friend in need: Time-dependent effects of stress on social discounting in men

Stress is often associated with a tend-and-befriend response, a putative coping mechanism where people behave generously towards others in order to invest in social relationships to seek comfort and mutual protection. However, this increase in generosity is expected to be directed only towards a delimited number of socially close, but not distant individuals, because it would be maladaptive to befriend everyone alike. In addition, the endocrinological stress response follows a distinct temporal pattern, and it is believed that tend-and-befriend tendencies can be observed mainly under acute stress. By contrast, the aftermath (> 1 h after) of stress is associated with endocrinological regulatory processes that are proposed to cause increased executive control and reduced emotional reactivity, possibly eliminating the need to tend-and-befriend. In the present experiment, we set out to investigate how these changes immediately and > 1 h after a stressful experience affect social-distance-dependent generosity levels, a phenomenon called social discounting. We hypothesized that stress has a time-dependent effect on social discounting, with decisions made shortly after (20 min), but not 90 min after stress showing increased generosity particularly to close others. We found that men tested 20 min after stressor onset indeed showed increased generosity towards close but not distant others compared to non-stressed men or men tested 90 min after stressor onset. These findings contribute to our understanding on how stress affects prosocial behavior by highlighting the importance of social closeness and the timing of stress relative to the decision as modulating factors in this type of decision making in men.     

Cooperation and the scale of competition in humans

Explaining cooperation is one of the greatest challenges for evolutionary biology. It is particularly a problem in species such as humans, where there is cooperation between nonrelatives. Numerous possible solutions have been suggested for the problem of cooperation between nonrelatives, including punishment, policing, and various forms of reciprocity. Here, we suggest that local competition for resources can pose a problem for these hypotheses, analogous to how it can select against cooperation between relatives. We extend the prisoner's dilemma (PD) game to show that local competition between interacting individuals can reduce selection for cooperation between nonrelatives. This is because, with local competition, fitness is relative to social partners, and cooperation benefits social partners. We then test whether nonrelated humans adjust their level of cooperation facultatively in response to the scale of competition when playing the PD for cash prizes. As predicted, we found that individuals were less likely to cooperate when competition was relatively local. Cooperation between humans will therefore be most likely when repeated interactions take place on a local scale between small numbers of people, and competition for resources takes place on a more global scale among large numbers of people.     

Evolution of equal division among unequal partners

One of the hallmarks of human fairness is its insensitivity to power: although strong individuals are often in a position to coerce weak individuals, fairness requires them to share the benefits of cooperation equally. The existence of such egalitarianism is poorly explained by current evolutionary models. We present a model based on cooperation and partner choice that can account for the emergence of a psychological disposition toward fairness, whatever the balance of power between the cooperative partners. We model the evolution of the division of a benefit in an interaction similar to an ultimatum game, in a population made up of individuals of variable strength. The model shows that strong individuals will not receive any advantage from their strength, instead having to share the benefits of cooperation equally with weak individuals at the evolutionary equilibrium, a result that is robust to variations in population size and the proportion of weak individuals. We discuss how this model suggests an explanation for why egalitarian behaviors toward everyone, including the weak, should be more likely to evolve in humans than in any other species.     

Upstream reciprocity and the evolution of gratitude

If someone is nice to you, you feel good and may be inclined to be nice to somebody else. This every day experience is borne out by experimental games: the recipients of an act of kindness are more likely to help in turn, even if the person who benefits from their generosity is somebody else. This behaviour, which has been called ‘upstream reciprocity’, appears to be a misdirected act of gratitude: you help somebody because somebody else has helped you. Does this make any sense from an evolutionary or a game theoretic perspective? In this paper, we show that upstream reciprocity alone does not lead to the evolution of cooperation, but it can evolve and increase the level of cooperation if it is linked to either direct or spatial reciprocity. We calculate the random walks of altruistic acts that are induced by upstream reciprocity. Our analysis shows that gratitude and other positive emotions, which increase the willingness to help others, can evolve in the competitive world of natural selection.     

Expanding comparative-advantage biological market models: contingency of mutualism on partners' resource requirements and acquisition trade-offs

We expand the comparative-advantage biological market-modelling framework to show how differences between partners, both in their abilities to acquire two resources and in their requirements for those resources, can affect the net benefit of participating in interspecific resource exchange. In addition, the benefits derived from resource trading depend strongly on the nature of the trade-off between the acquisition of one resource and the acquisition of another, described here by the shape (linear, convex or concave) of the resource acquisition constraints of the individuals involved. Combined with previous results, these analyses provide a suite of predictions about whether or not resource exchange is beneficial for two heterospecific individuals relative to a strategy of non-interaction. The benefit derived from resource exchange depends on three factors: (i) relative differences between the partners in their resource acquisition abilities; (ii) relative differences between the partners in their resource requirements; and (iii) variation in the shape of resource acquisition trade-offs. We find that such an explicit consideration of resource requirements and acquisition abilities can provide useful and sometimes non-intuitive predictions about the benefits of resource exchange, and also which resources should be traded by which species.