In comparative cognition, humans are often used as a reference point to determine whether other species possess similar cognitive abilities. Some researchers, in particular primatologists, use the comparative approach to find similarities due to common ancestry. Comparing all vertebrate taxa, including fishes, may thus reveal the shared cognitive tool box of vertebrates. A prime example is the recent discovery that all vertebrates share a network of brain areas that is involved in social decision making. The similarities strongly suggest that a verison of this network was present in the commmon ancestor of all vertebrates. On the other hand, studies on fishes may reveal that certain similarities between species are likely to be the result of convergent evolution. For example, a cichlid fish shares with some bird and mammal species including humans the ability to use transitive inference, i.e. the ability to conclude that if A>B and B>C then A>C. Such a similarity is best seen as independent adaptation to similar ecological conditions. Conversely, the ecological approach can be used to compare closely related fish species that occupy divergent niches in order to identify differences in cognitive abilities (cognitive ecology). Fishes have undergone multiple adaptive radiations where closely related species occupy diverse niches linked to important differences in habitat as well as social organization. Thus, one can repeatedly compare closely related species and correlate environmental factors with differences in brain structures and differences in cognitive task performance. A classic model system is that of the cichlids occupying African rift lakes. Comparisons within lakes have shown that brains and cognition have been shaped by both the physical and social environment. Comparisons between adjacent lakes reveal amazing cases of convergent evolution of species which occupy similar niches.

This anthropocentrically organized phylogenetic tree illustrates two non-mutually exclusive approaches to comparative cognition. The ‘anthropocentric’ or ‘phylogenetic’ approach aims to infer similarities due to shared ancestry. While typically used by primatologists interested in the evolution of cognitive processes used by humans, the study of fishes may inform us about the general shared cognition toolbox of vertebrates. The ‘ecological’ or ‘functional’ approach is rooted in standard evolutionary theory based on natural selection, which predicts that a species’ cognitive abilities are a reflection of its ecological (social and environmental) complexity. Fishes offer great opportunities to use this approach, either within taxa showing adaptive radiations or in tests for convergent evolution among vertebrates.

Below, we provide some examples of fish cognition research. We highlight two major areas in which fish have made a substantial contribution to our understanding of the evolution of cognition: social cognition and spatial learning.

Social intelligence

Figure 2 Examples of fish cognitive social abilities. Show full caption (A) The cichlid Astatotilapia burtoni uses transitive inference to predict male hierarchies.(Image: Russ Fernald.) (B) Spawning migrations in the wrasse Thalassoma bifasciatus as an example for arbitrary traditions. (Image: Robert Warner.) (C) Cleaner wrasse adjust service quality to the presence of bystanders. (D) Rock pool blennies use cognitive maps to jump ‘blindly’ between pools. (E) Groupers coordinate joint hunting with moray eels. (Image: Alexander Vail.) It has long been argued that the large human brain and associated cognitive skills were favored by natural selection to cope with our complex social interactions. This rationale can readily be generalized to any species that lives in complex social groups. Fish are capable of individual, kin and olfactory self-recognition, the basis for most sophisticated social behaviors. In most instances, chemical cues play a very important role in the recognition process and may be reinforced by visual cues. In guppies, individuals become familiar with one another over a period of about 2 weeks. When given a choice, fish nearly always chose to shoal with familiar rather than unfamiliar individuals, and there appear to be foraging and anti-predator benefits associated with this choice. Shoaling fish also have good numerical abilities used to track shoal size. These abilities appear to rely on two separate systems. The first is an object tracking system that enables them to keep track of up to four objects simultaneously and thus they can make very accurate judgments when comparing small quantities. The other system is more useful for comparing larger quantities and relies on the relative rather than the absolute differences between two sets. It has been argued that other vertebrates (including humans) also use these two systems. Other key findings on fish social cognition are listed below ( Figure 2 ).

Traditions and social learning rules Outside humans, the best experimental evidence for rather arbitrary traditions in wild animal populations stems from birdsong and coral reef fish spawning migrations. Various fish species aggregate at dawn or dusk on the reef to swim together to a site suitable for spawning. In a most spectacular experiment, entire local populations of blue-headed wrasse were exchanged between locations. Robert Warner showed that without local knowledge, the translocated populations selected new spawning sites, showing that both the old and new locations were somewhat arbitrarily chosen. Moreover, they kept the new locations for the entire 20 years of study, i.e. across generations. While the information transfer seems to be rather simple — naïve individuals may learn by following knowledgeable ones — recent research has demonstrated that nine-spined sticklebacks can use highly sophisticated updating rules, so-called ‘hill climbing’ rules, to decide whether and from whom to learn about the location of food sources. They compare their own experience with the success of observed conspecifics in order to decide where to feed. At the time, such decision rules about social learning had been only described in humans.

Social decision making Being a member of a group has been suggested to convey advantages concerning optimal decision making. Ignorant individuals may rely and knowledgeable ones to find food or shelter and to avoid predators. Shoaling fish species yield highly suitable systems to test theories concerning the precise decision rules. ‘Robofish’ ( Figure 3 ), whose movement patterns are experimentally programmed and towards which real fish react relatively naturally, have been instrumental to investigate causality. Through the use of robofish, researchers have shown that single stickleback are susceptible to a leader behaving in a maladaptive way (going towards a predator), while larger groups avoid this pitfall by using a quorum response. The personality of particular individuals within the group can also greatly affect the level of influence that individual has on guiding group behavior. Figure 3 A powerful tool for experimental manipulation. Show full caption ‘Robofish’, a model whose movement patterns are experimentally programmed and towards which real fish react relatively naturally, allows precise testing of fish decisions in the context of group coordination. (Image: Jens Krause.)

Reputation as a basis of cooperation The literature on humans emphasizes the fact that humans often achieve stable cooperation through reputation. Reputation matters as observers will only help those individuals in need who have helped others. Reputation mechanisms involve the ability to properly assess outcomes even without personal experience, and to adjust ones’ own levels of cooperation conditionally on the partner’s past behavior and to the presence of bystanders. In fishes, the cleaner wrasse Labroides dimidiatus must manage its reputation. Cleaner wrasse remove ectoparasites from cooperating so-called ‘client’ reef fish but prefer to eat client mucus, which harms the fish and thus constitutes cheating. Cleaners have 2000 interactions per day. Therefore, clients visiting a cleaner may often witness the end of an ongoing interaction and invite inspection if the observed service was good but avoid cleaners that cheated. Cleaners thus have a social prestige, and they are indeed more cooperative to current clients if bystanders are present.