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Social learning is often proposed as an important driver of the evolution of human cooperation. In this view, cooperation in other species might be restricted because it mostly relies on individually learned or innate behaviours. Here, we show that juvenile cleaner fish ( Labroides dimidiatus ) can learn socially about cheating consequences in an experimental paradigm that mimics cleaners’ cooperative interactions with client fish. Juvenile cleaners that had observed adults interacting with model clients learned to (1) behave more cooperatively after observing clients fleeing in response to cheating; (2) prefer clients that were tolerant to cheating; but (3) did not copy adults’ arbitrary feeding preferences. These results confirm that social learning can play an active role in the development of cooperative strategies in a non-human animal. They further show that negative responses to cheating can potentially shape the reputation of cheated individuals, influencing cooperation dynamics in interaction networks. Cleaner fish can cheat clients for higher rewards but this comes with a risk of punishment. Here, Truskanov et al. show that juvenile cleaner fish can learn by observing adults to behave more cooperatively themselves but also to prefer clients that are more tolerant to cheating.

Transitive inference (TI) is a reasoning capacity that allows individuals to deduce unknown pair relationships from previous knowledge of other pair relationships. Its occurrence in a wide range of animals, including insects, has been linked to their ecological needs. Thus, TI should be absent in species that do not rely on such inferences in their natural lives. We hypothesized that the latter applies to the cleaner wrasse Labroides dimidiatus and tested this with 19 individuals using a five-term series (A > B > C > D > E) experiment. Cleaners first learned to prefer a food-rewarding plate (+) over a non-rewarding plate (-) in four plate pairs that imply a hierarchy from plate A to plate E (A+B-, B+C-, C+D-, D+E-), with the learning order counterbalanced between subjects. We then tested for spontaneous preferences in the unknown pairs BD (transitive inference task) and AE (as a control for anchors), interspersed between trials involving a mix of all known adjacent pairs. The cleaners systematically preferred A over E and showed good performance for A+B- and D+E- trials. Conversely, cleaners did not prefer B over D. These results were unaffected by the reinforcement history, but the order of learning of the different pairs of plates had a main impact on the remembrance of the initial training pairs. Overall, cleaners performed randomly in B+C- and C+D- trials. Thus, a memory constraint may have prevented subjects from applying TI. Indeed, a parallel study on cleaner wrasse provided positive evidence for TI but was achieved following extensive training on the non-adjacent pairs which may have over-ridden the ecological relevance of the task.

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish ( Labroides dimidiatus ), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions. The causes and consequences of social intelligence are challenging to establish. A study on wild cleaner fish reports that large forebrains enable individuals to score higher in a social competence test, suggesting forebrain size is important for complex social decision-making.

When one individual helps another, it benefits the recipient and may also gain a reputation for being cooperative. This may induce others to favour the helper in subsequent interactions, so investing in being seen to help others may be adaptive. The best-known mechanism for this is indirect reciprocity (IR), in which the profit comes from an observer who pays a cost to benefit the original helper. IR has attracted considerable theoretical and empirical interest, but it is not the only way in which cooperative reputations can bring benefits. Signalling theory proposes that paying a cost to benefit others is a strategic investment which benefits the signaller through changing receiver behaviour, in particular by being more likely to choose the signaller as a partner. This reputation-based partner choice can result in competitive helping whereby those who help are favoured as partners. These theories have been confused in the literature. We therefore set out the assumptions, the mechanisms and the predictions of each theory for how developing a cooperative reputation can be adaptive. The benefits of being seen to be cooperative may have been a major driver of sociality, especially in humans. This article is part of the theme issue 'The language of cooperation: reputation and honest signalling'.

Some animals have the remarkable capacity for mirror self-recognition (MSR), yet any implications for self-awareness remain uncertain and controversial. This is largely because explicit tests of the two potential mechanisms underlying MSR are still lacking: mental image of the self and kinesthetic visual matching. Here, we test the hypothesis that MSR ability in cleaner fish, Labroides dimidiatus, is associated with a mental image of the self, in particular the self-face, like in humans. Mirror-naive fish initially attacked photograph models of both themselves and unfamiliar strangers. In contrast, after all fish had passed the mirror mark test, fish did not attack their own (motionless) images, but still frequently attacked those of unfamiliar individuals. When fish were exposed to composite photographs, the self-face/unfamiliar body were not attacked, but photographs of unfamiliar face/self-body were attacked, demonstrating that cleaner fish with MSR capacity recognize their own facial characteristics in photographs. Additionally, when presented with self-photographs with a mark placed on the throat, unmarked mirror-experienced cleaner fish demonstrated throat-scraping behaviors. When combined, our results provide clear evidence that cleaner fish recognize themselves in photographs and that the likely mechanism for MSR is associated with a mental image of the self-face, not a kinesthetic visual-matching model. Humans are also capable of having a mental image of the self-face, which is considered an example of private self-awareness. We demonstrate that combining mirror test experiments with photographs has enormous potential to further our understanding of the evolution of cognitive processes and private self-awareness across nonhuman animals.

Punishers can benefit from a tough reputation, where future partners cooperate because they fear repercussions. Alternatively, punishers might receive help from bystanders if their act is perceived as just and other-regarding. Third-party punishment of selfish individuals arguably fits these conditions, but it is not known whether third-party punishers are rewarded for their investments. Here, we show that third-party punishers are indeed rewarded by uninvolved bystanders. Third parties were presented with the outcome of a dictator game in which the dictator was either selfish or fair and were allocated to one of three treatments in which they could choose to do nothing or (1) punish the dictator, (2) help the receiver, or (3) choose between punishment and helping, respectively. A fourth player (bystander) then see the third-party's decision and could choose to reward the third party or not. Third parties that punished selfish dictators were more likely to be rewarded by bystanders than third parties that took no action in response to a selfish dictator. However, helpful third parties were rewarded even more than third-party punishers. These results suggest that punishment could in principle evolve via indirect reciprocity, but also provide insights into why individuals typically prefer to invest in positive actions.

Humans are outstanding in their ability to cooperate with unrelated individuals, and punishment – paying a cost to harm others – is thought to be a key supporting mechanism. According to this view, cooperators punish defectors, who respond by behaving more cooperatively in future interactions. However, a synthesis of the evidence from laboratory and real-world settings casts serious doubts on the assumption that the sole function of punishment is to convert cheating individuals into cooperators. Instead, punishment often prompts retaliation and punishment decisions frequently stem from competitive, rather than deterrent motives. Punishment decisions often reflect the desire to equalise or elevate payoffs relative to targets, rather than the desire to enact revenge for harm received or to deter cheats from reoffending in future. We therefore suggest that punishment also serves a competitive function, where what looks like spiteful behaviour actually allows punishers to equalise or elevate their own payoffs and/or status relative to targets independently of any change in the target's behaviour. Institutions that reduce or remove the possibility that punishers are motivated by relative payoff or status concerns might offer a way to harness these competitive motives and render punishment more effective at restoring cooperation.

Humans are arguably unique in the extent and scale of cooperation with unrelated individuals. While pairwise interactions among non-relatives occur in some non-human species, there is scant evidence of the large-scale, often unconditional prosociality that characterizes human social behaviour. Consequently, one may ask whether research on cooperation in humans can offer general insights to researchers working on similar questions in non-human species, and whether research on humans should be published in biology journals. We contend that the answer to both of these questions is yes. Most importantly, social behaviour in humans and other species operates under the same evolutionary framework. Moreover, we highlight how an open dialogue between different fields can inspire studies on humans and non-human species, leading to novel approaches and insights. Biology journals should encourage these discussions rather than drawing artificial boundaries between disciplines. Shared current and future challenges are to study helping in ecologically relevant contexts in order to correctly interpret how payoff matrices translate into inclusive fitness, and to integrate mechanisms into the hitherto largely functional theory. We can and should study human cooperation within a comparative framework in order to gain a full understanding of the evolution of helping.

Animals exhibiting mirror self-recognition (MSR) are considered self-aware; however, studies on their level of self-awareness remain inconclusive. Recent research has indicated the potential for cleaner fish ( Labroides dimidiatus ) to possess a sophisticated level of private self-awareness. However, as this study revealed only an aspect of private self-awareness, further investigation into other elements is essential to substantiate this hypothesis. Here, we show that cleaner fish, having attained MSR, construct a mental image of their bodies by investigating their ability to recall body size. A size-based hierarchy governs the outcomes of their confrontations. The mirror-naïve fish behaved aggressively when presented with photographs of two unfamiliar conspecifics that were 10% larger and 10% smaller than their body sizes. After passing the MSR test, they refrained from aggression toward the larger photographs but still behaved aggressively toward the smaller ones without re-examining their mirror images. These findings suggest that cleaner fish accurately recognize their body size based on mental images of their bodies formed through MSR. Additionally, mirror-experienced fish frequently revisited the mirror when presented with an intimidating larger photograph, implying the potential use of mirrors for assessing body size. Our study established cleaner fish as the first non-human animal to be demonstrated to possess private self-awareness.

Collaborative hunting, the coordination of animal behaviour in space and time to capture prey, is reported in several vertebrate species. However, previous studies are observational, hampering our ability to identify individual decision rules that result in collaboration. We experimentally investigated collaborative hunting in yellow saddle goatfish (Parupeneus cyclostomus) by exposing pairs to a mock prey that fled to an artificial shelter with multiple entrances. The first fish to initiate the chase (the ‘initiator’) was always closest to the prey and pursued it directly in its path. Conversely, the behaviour of the second goatfish (the ‘follower’) depended on its spatial position relative to the initiator. When the follower was less than one body length behind the initiator, it also accelerated directly towards the prey in over 95% of cases. However, if the two goatfish were separated by a distance of one body length or more, the follower chose a less direct route to reach the prey in 87% of cases. In this scenario, the follower often reached the prey's more distant refuge first, which might increase its hunting success or block the prey's escape path under natural conditions. Our findings suggest that coordinated hunting behaviour can result from simple, self-serving decisions.