Maxwell N. Burton-Chellew

The Evolution of Altruism in Humans

Humans are an intensely social species, frequently performing costly behaviors that benefit others. Efforts to solve the evolutionary puzzle of altruism have a lengthy history, and recent years have seen many important advances across a range of disciplines. Here we bring together this interdisciplinary body of research and review the main theories that have been proposed to explain human prosociality, with an emphasis on kinship, reciprocity, indirect reciprocity, punishment, and morality. We highlight recent methodological advances that are stimulating research and point to some areas that either remain controversial or merit more attention.

Prosocial preferences do not explain human cooperation in public-goods games.

It has become an accepted paradigm that humans have “prosocial preferences” that lead to higher levels of cooperation than those that would maximize their personal financial gain. However, the existence of prosocial preferences has been inferred post hoc from the results of economic games, rather than with direct experimental tests. Here, we test how behavior in a public-goods game is influenced by knowledge of the consequences of actions for other players. We found that (i) individuals cooperate at similar levels, even when they are not informed that their behavior benefits others; (ii) an increased awareness of how cooperation benefits others leads to a reduction, rather than an increase, in the level of cooperation; and (iii) cooperation can be either lower or higher than expected, depending on experimental design. Overall, these results contradict the suggested role of the prosocial preferences hypothesis and show how the complexity of human behavior can lead to misleading conclusions from controlled laboratory experiments.

Resistance to extreme strategies, rather than prosocial preferences, can explain human cooperation in public goods games

The results of numerous economic games suggest that humans behave more cooperatively than would be expected if they were maximizing selfish interests. It has been argued that this is because individuals gain satisfaction from the success of others, and that such prosocial preferences require a novel evolutionary explanation. However, in previous games, imperfect behavior would automatically lead to an increase in cooperation, making it impossible to decouple any form of mistake or error from prosocial cooperative decisions. Here we empirically test between these alternatives by decoupling imperfect behavior from prosocial preferences in modified versions of the public goods game, in which individuals would maximize their selfish gain by completely (100%) cooperating. We found that, although this led to higher levels of cooperation, it did not lead to full cooperation, and individuals still perceived their group mates as competitors. This is inconsistent with either selfish or prosocial preferences, suggesting that the most parsimonious explanation is imperfect behavior triggered by psychological drives that can prevent both complete defection and complete cooperation. More generally, our results illustrate the caution that must be exercised when interpreting the evolutionary implications of economic experiments, especially the absolute level of cooperation in a particular treatment.

Cooperation, quorum sensing, and evolution of virulence in Staphylococcus aureus.

ABSTRACT The virulence and fitness in vivo of the major human pathogen Staphylococcus aureus are associated with a cell-to-cell signaling mechanism known as quorum sensing (QS). QS coordinates the production of virulence factors via the production and sensing of autoinducing peptide (AIP) signal molecules by the agr locus. Here we show, in a wax moth larva virulence model, that (i) QS in S. aureus is a cooperative social trait that provides a benefit to the local population of cells, (ii) agr mutants, which do not produce or respond to QS signal, are able to exploit the benefits provided by the QS of others (“cheat”), allowing them to increase in frequency when in mixed populations with cooperators, (iii) these social interactions between cells determine virulence, with the host mortality rate being negatively correlated to the percentage of agr mutants (“cheats”) in a population, and (iv) a higher within-host relatedness (lower strain diversity) selects for QS and hence higher virulence. Our results provide an explanation for why agr mutants show reduced virulence in animal models but can be isolated from infections of humans. More generally, by providing the first evidence that QS is a cooperative social behavior in a Gram-positive bacterium, our results suggest convergent, and potentially widespread, evolution for signaling to coordinate cooperation in bacteria.

Kin selection, quorum sensing and virulence in pathogenic bacteria

Bacterial growth and virulence often depends upon the cooperative release of extracellular factors excreted in response to quorum sensing (QS). We carried out an in vivo selection experiment in mice to examine how QS evolves in response to variation in relatedness (strain diversity), and the consequences for virulence. We started our experiment with two bacterial strains: a wild-type that both produces and responds to QS signal molecules, and a lasR (signal-blind) mutant that does not release extracellular factors in response to signal. We found that: (i) QS leads to greater growth within hosts; (ii) high relatedness favours the QS wild-type; and (iii) low relatedness favours the lasR mutant. Relatedness matters in our experiment because, at relatively low relatedness, the lasR mutant is able to exploit the extracellular factors produced by the cells that respond to QS, and hence increase in frequency. Furthermore, our results suggest that because a higher relatedness favours cooperative QS, and hence leads to higher growth, this will also lead to a higher virulence, giving a relationship between relatedness and virulence that is in the opposite direction to that usually predicted by virulence theory.

Pseudocompetition among groups increases human cooperation in a public-goods game

Economic games are often used in an attempt to reveal the underlying preferences or motivations that govern human behaviour. However, this approach relies on the implicit assumption that individuals are rational and fully aware of the consequences of their decisions. We examined behaviour in a standard economic game that is often used to measure social preferences: the public-goods game. We found that giving information to individuals about the relative success of their group led to (1) significantly higher levels of cooperation and (2) emotional responses to group success. This is despite the fact that group success had no effect on the payoffs in our game, and so knowledge of group success should not influence the behaviour of rational players. Consequently, these results suggest that cues of group competition have an automatic or unconscious effect on human behaviour that can induce increased within-group cooperation. More generally, this framing effect emphasizes the potential problem with drawing biological conclusions from the quantitative comparison of cooperation levels in economic games with the predictions of theory. Instead, our results emphasize the advantage of testing theory by qualitatively comparing behaviour across treatments, and with regard to expected adaptations and expected ontogeny.

Conditional cooperation and confusion in public-goods experiments

Significance The finding that people vary in how they play economic games has led to the conclusion that people vary in their preference for fairness. Consequently, people have been divided into fair cooperators that make sacrifices for the good of the group and selfish free-riders that exploit the cooperation of others. This conclusion has been used to challenge evolutionary theory and economic theory and to guide social policy. We show that variation in behavior in the public-goods game is better explained by variation in understanding and that misunderstanding leads to cooperation. Economic experiments are often used to study if humans altruistically value the welfare of others. A canonical result from public-good games is that humans vary in how they value the welfare of others, dividing into fair-minded conditional cooperators, who match the cooperation of others, and selfish noncooperators. However, an alternative explanation for the data are that individuals vary in their understanding of how to maximize income, with misunderstanding leading to the appearance of cooperation. We show that (i) individuals divide into the same behavioral types when playing with computers, whom they cannot be concerned with the welfare of; (ii) behavior across games with computers and humans is correlated and can be explained by variation in understanding of how to maximize income; (iii) misunderstanding correlates with higher levels of cooperation; and (iv) standard control questions do not guarantee understanding. These results cast doubt on certain experimental methods and demonstrate that a common assumption in behavioral economics experiments, that choices reveal motivations, will not necessarily hold.

Payoff-based learning explains the decline in cooperation in public goods games.

Economic games such as the public goods game are increasingly being used to measure social behaviours in humans and non-human primates. The results of such games have been used to argue that people are pro-social, and that humans are uniquely altruistic, willingly sacrificing their own welfare in order to benefit others. However, an alternative explanation for the empirical observations is that individuals are mistaken, but learn, during the game, how to improve their personal payoff. We test between these competing hypotheses, by comparing the explanatory power of different behavioural rules, in public goods games, where individuals are given different amounts of information. We find: (i) that individual behaviour is best explained by a learning rule that is trying to maximize personal income; (ii) that conditional cooperation disappears when the consequences of cooperation are made clearer; and (iii) that social preferences, if they exist, are more anti-social than pro-social.

Combined inequality in wealth and risk leads to disaster in the climate change game

It is generally agreed that the risk of catastrophic climate change can only be reduced if agents cooperate to reduce greenhouse gas emissions over the course of the 21st Century. Previous economic experiments have suggested that sufficient cooperation can often be achieved providing individuals are adequately and convincingly informed of the consequences of their actions and the stakes involved. However, this previous work, has not allowed for the fact that in the real world agents vary in both: (1) their resources to mitigate climate change, and (2) the consequences that they face from climate change. We develop and expand the protocol of previous economic experiments to investigate the introduction of such combined asymmetries. We find that when inequality in resources is combined with a greater relative risk for poorer members, cooperation collapses, with tragic consequences. This is because the rich invest proportionally less into preventing climate change when they are less at risk. We also find, through the use of a post-game questionnaire, that those individuals who were more skeptical about climate change in the real world cooperated less in our games. Insofar as such experiments can be trusted as a guide to either people’s everyday behaviour or the interactions of nation states, these results suggest that voluntary cooperation to avoid climate catastrophe in the real world is likely to be hard to achieve.

Social learning and the demise of costly cooperation in humans

Humans have a sophisticated ability to learn from others, termed social learning, which has allowed us to spread over the planet, construct complex societies, and travel to the moon. It has been hypothesized that social learning has played a pivotal role in making human societies cooperative, by favouring cooperation even when it is not favoured by genetical selection. However, this hypothesis lacks direct experimental testing, and the opposite prediction has also been made, that social learning disfavours cooperation. We experimentally tested how different aspects of social learning affect the level of cooperation in public-goods games. We found that: (i) social information never increased cooperation and usually led to decreased cooperation; (ii) cooperation was lowest when individuals could observe how successful individuals behaved; and (iii) cooperation declined because individuals preferred to copy successful individuals, who cooperated less, rather than copy common behaviours. Overall, these results suggest that individuals use social information to try and improve their own success, and that this can lead to lower levels of cooperation.