Image scoring and cooperation in a cleaner fish mutualism

Humans are highly social animals and often help unrelated individuals that may never reciprocate the altruist's favour. This apparent evolutionary puzzle may be explained by the altruist's gain in social image: image-scoring bystanders, also known as eavesdroppers, notice the altruistic act and therefore are more likely to help the altruist in the future. Such complex indirect reciprocity based on altruistic acts may evolve only after simple indirect reciprocity has been established, which requires two steps. First, image scoring evolves when bystanders gain personal benefits from information gathered, for example, by finding cooperative partners. Second, altruistic behaviour in the presence of such bystanders may evolve if altruists benefit from access to the bystanders. Here, we provide experimental evidence for both of the requirements in a cleaning mutualism involving the cleaner fish Labroides dimidiatus. These cleaners may cooperate and remove ectoparasites from clients or they may cheat by feeding on client mucus. As mucus may be preferred over typical client ectoparasites, clients must make cleaners feed against their preference to obtain a cooperative service. We found that eavesdropping clients spent more time next to 'cooperative' than 'unknown cooperative level' cleaners, which shows that clients engage in image-scoring behaviour. Furthermore, trained cleaners learned to feed more cooperatively when in an 'image-scoring' than in a 'non-image-scoring' situation.     

Pairs of cooperating cleaner fish provide better service quality than singletons

Service providers may vary service quality depending on whether they work alone or provide the service simultaneously with a partner. The latter case resembles a prisoner's dilemma, in which one provider may try to reap the benefits of the interaction without providing the service. Here we present a game-theory model based on the marginal value theorem, which predicts that as long as the client determines the duration, and the providers cooperate towards mutual gain, service quality will increase in the pair situation. This prediction is consistent with field observations and with an experiment on cleaning mutualism, in which stable male-female pairs of the cleaner wrasse Labroides dimidiatus repeatedly inspect client fish jointly. Cleaners cooperate by eating ectoparasites off clients but actually prefer to cheat and eat client mucus. Because clients often leave in response to such cheating, the benefits of cheating can be gained by only one cleaner during a pair inspection. In both data sets, the increased service quality during pair inspection was mainly due to the smaller females behaving significantly more cooperatively than their larger male partners. In contrast, during solitary inspections, cleaning behaviour was very similar between the sexes. Our study highlights the importance of incorporating interactions between service providers to make more quantitative predictions about cooperation between species.     

Inclusive fitness theory and eusociality

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.