The ability to perceive and recognise a reflected mirror image as self (mirror self-recognition, MSR) is considered a hallmark of cognition across species. Although MSR has been reported in mammals and birds, it is not known to occur in any other major taxon. Potentially limiting our ability to test for MSR in other taxa is that the established assay, the mark test, requires that animals display contingency testing and self-directed behaviour. These behaviours may be difficult for humans to interpret in taxonomically divergent animals, especially those that lack the dexterity (or limbs) required to touch a mark. Here, we show that a fish, the cleaner wrasse Labroides dimidiatus, shows behaviour that may reasonably be interpreted as passing through all phases of the mark test: (i) social reactions towards the reflection, (ii) repeated idiosyncratic behaviours towards the mirror, and (iii) frequent observation of their reflection. When subsequently provided with a coloured tag in a modified mark test, fish attempt to remove the mark by scraping their body in the presence of a mirror but show no response towards transparent marks or to coloured marks in the absence of a mirror. This remarkable finding presents a challenge to our interpretation of the mark test—do we accept that these behavioural responses, which are taken as evidence of self-recognition in other species during the mark test, lead to the conclusion that fish are self-aware? Or do we rather decide that these behavioural patterns have a basis in a cognitive process other than self-recognition and that fish do not pass the mark test? If the former, what does this mean for our understanding of animal intelligence? If the latter, what does this mean for our application and interpretation of the mark test as a metric for animal cognitive abilities?Editor’s noteThis Short Report received both positive and negative reviews by experts. The Academic Editor has written an accompanying Primer that we are publishing alongside this article (https://doi.org/10.1371/journal.pbio.3000112). The linked Primer presents a complementary expert perspective; it discusses how the current study should be interpreted in the context of evidence for and against self-awareness in a wide range of animals.

No abstract

Cooperative breeding has been studied intensively in many species of birds and mammals but remain less well studied in fish. We report a remarkable new example of a cooperatively breeding cichlid from Lake Tanganyika, Neolamprologus obscurus. Using field observations and microsatellite DNA analyses, we studied group structure, helping behavior, relatedness, and dispersal of this species. We present four major observations. First, large territorial breeding males mated with one to eight breeding females, each of which was territorial and unrelated to another. Second, one to ten smaller fish ("subordinates") of both sexes were allowed to stay inside the breeding females' territories. Subordinates were often highly related to both the respective breeding male and female and performed territory defense and shelter maintenance, which is regarded as helping behaviors. Third, one to three subordinate males, similar in size to breeding females, were allowed to stay inside a breeding male's territory but were not tolerated in the breeding females' territories. Pairwise relatedness suggests these individuals are usually sons of the respective breeding male. Fourth, pairwise relatedness estimates suggest that juveniles delay dispersal and assist their mothers in raising offspring. As female subordinates grow up, they leave the father's territory and disperse into other groups. In contrast, male subordinates leave their mother's territory but remain within the territory of their father. The described social system makes N. obscurus a promising new model species to study the evolution of cooperative breeding.

An animal that tries to remove a mark from its body that is only visible when looking into a mirror displays the capacity for mirror self-recognition (MSR), which has been interpreted as evidence for self-awareness. Conservative interpretations of existing data conclude that convincing evidence for MSR is currently restricted to great apes. Here, we address proposed shortcomings of a previous study on MSR in the cleaner wrasse Labroides dimidiatus, by varying preexposure to mirrors and by marking individuals with different colors. We found that (1) 14/14 new individuals scraped their throat when a brown mark had been provisioned, but only in the presence of a mirror; (2) blue and green color marks did not elicit scraping; (3) intentionally injecting the mark deeper beneath the skin reliably elicited spontaneous scraping in the absence of a mirror; (4) mirror-naive individuals injected with a brown mark scraped their throat with lower probability and/or lower frequency compared to mirror-experienced individuals; (5) in contrast to the mirror images, seeing another fish with the same marking did not induce throat scraping; and (6) moving the mirror to another location did not elicit renewed aggression in mirror-experienced individuals. Taken together, these results increase our confidence that cleaner fish indeed pass the mark test, although only if it is presented in ecologically relevant contexts. Therefore, we reiterate the conclusion of the previous study that either self-awareness in animals or the validity of the mirror test needs to be revised.

Unravelling the evolution of complex social organization in animals is an important aim, not least because it helps to understand the evolutionary roots of human sociality. Recent advances in comparative methods allow to approach this question in a phylogenetic context. The validity of such comparative approaches depends strongly on the quality of information regarding the behaviour, sociality, and reproduction of animals in natural systems, and on the quality of the phylogenetic reconstruction. Applying a novel comparative approach, a recent study of Dey et al. (, Nature Ecology & Evolution, 1, 137) concluded that evolutionary transitions to cooperative breeding in cichlid fishes were not associated with the social mating pattern. Here we argue that this result was adversely affected by equivocal classifications of mating patterns, and inadequate phylogenetic data. In order to illustrate the impact of the mating system misclassifications, we scored mating patterns as reported in the original literature and re‐analysed the dataset based on Dey et al.’s tree topology. The result suggests that the mating system does in fact significantly explain the evolutionary transition to cooperative breeding in lamprologine cichlids, but we submit that a reliable conclusion cannot be reached before improving the behavioural information and the underlying phylogenetic reconstruction. The problems identified in this case study are not unique and we urge caution in the interpretation of results from comparative phylogenetic studies in general. We do agree with Dey et al. () though that the lamprologine cichlids of Lake Tanganyika may constitute a fundamental test case for the theory of social evolution, but better information on their behaviour and phylogenetic relationships is needed to allow meaningful analyses.