Intraspecific variation in invertebrate cognition: a review

A well-established field of research in vertebrates focuses on the variability of cognitive abilities within species. From mammals to fish, numerous studies have revealed remarkable differences in the cognitive phenotype among individuals, particularly in terms of sex or personality. However, many aspects of the mechanisms, genetics, and selective pressures that underlie individual cognitive variation remain unclear. Surprisingly, intraspecific variability in cognition has received much less attention in invertebrates, despite the increasing evidence of remarkable cognitive abilities in this group and the insights that could be gained from examining simultaneously two distinct taxa, namely vertebrates and invertebrates. In this review, we provide evidence that certain invertebrate species exhibit all the key features of cognitive variation observed in vertebrates, including differences related to sex and personality. In many cases, invertebrate studies have provided insights into the genetic basis, evolvability and response to selection of cognitive variability. Moreover, we highlight evidence for caste differences in eusocial insects, which are linked to task specialisation within the colony. This makes insect eusociality a valuable system for understanding how selection influences cognitive variation. We propose that cognitive variation in invertebrates may be more widespread than currently thought, and that selection may operate in a similar manner on two distantly related cognitive systems (vertebrates and invertebrates). Finally, we suggest that invertebrates hold the potential to serve both as alternative and complementary models to vertebrates, contributing to a deeper understanding of cognitive evolution

Familiarity effects on fish behaviour are disrupted in shoals that contain also unfamiliar individuals

Research on several social fishes has revealed that shoals constituted by familiar individuals behave remarkably differently compared to shoals formed by unfamiliar individuals. However, whether these behavioural changes may arise also in shoals composed by a mixture of familiar and unfamiliar individuals, a situation that may commonly occur in nature, is not clear. Here, we observed the behaviour of Mediterranean killifish (Aphanius fasciatus) shoals that were composed by both familiar and unfamiliar individuals (i.e. individuals were familiar to each other in pairs) and compared it with shoals entirely made by either unfamiliar or familiar individuals. Shoals formed by familiar individuals took longer to emerge from a refuge and swam more cohesively compared to shoals formed by unfamiliar fish. Shoals formed by a mixture of familiar and unfamiliar individuals behaved as shoals formed by unfamiliar individuals. Moreover, mixed shoals did not segregate in pairs according to their familiarity. This study suggests that mixed shoals do not show the behavioural effects of familiarity. Significance statement Laboratory studies have compared the behaviour of shoals formed by familiar fish versus shoals formed by unfamiliar fish, finding notable advantages in the former ones, such as improved antipredator and foraging behaviour. However, comparing these two opposite shoal types may not provide information on the natural situation, because in nature, shoals often change composition. We investigated how shoals formed by a mixture of familiar and unfamiliar fish behaved. We analysed shoals' preference for open environment versus covers and shoals' swimming cohesion. Results showed that shoals formed by both familiar and unfamiliar individuals mostly behave like shoals entirely formed by unfamiliar individuals. This suggests that the advantages of social groups formed by familiar fish might be hardly seen in nature for species in which shoal composition changes frequently

Quantity discrimination in newly hatched zebrafish suggests hardwired numerical abilities

An intriguing hypothesis to explain the ubiquity of numerical abilities is that all vertebrates are born with hardwired neuronal networks for processing numbers. To date, only studies on human foetuses have clearly supported this hypothesis. Zebrafish hatch 48–72 h after fertilisation with an embryonic nervous system, providing a unique opportunity for investigating this hypothesis. Here, we demonstrated that zebrafish larvae exposed to vertical bars at birth acquired an attraction for bar stimuli and we developed a numerical discrimination task based on this preference. When tested with a series of discriminations of increasing difficulty (1vs.4, 1vs.3, 1vs.2, and 2vs.4 bars), zebrafish larvae reliably selected the greater numerosity. The preference was significant when stimuli were matched for surface area, luminance, density, and convex hull, thereby suggesting a true capacity to process numerical information. Converging results from two phylogenetically distant species suggests that numerical abilities might be a hallmark feature of vertebrates’ brains

Individual differences and knockout in zebrafish reveal similar cognitive effects of BDNF between teleosts and mammals

The remarkable similarities in cognitive performance between teleosts and mammals suggest that the underlying cognitive mechanisms might also be similar in these two groups. We tested this hypothesis by assessing the effects of the brain-derived neurotrophic factor (BDNF), which is critical for mammalian cognitive functioning, on fish's cognitive abilities. We found that individual differences in zebrafish's learning abilities were positively correlated with bdnf expression. Moreover, a CRISPR/Cas9 mutant zebrafish line that lacks the BDNF gene (bdnf(-/-)) showed remarkable learning deficits. Half of the mutants failed a colour discrimination task, whereas the remaining mutants learned the task slowly, taking three times longer than control bdnf(+/+) zebrafish. The mutants also took twice as long to acquire a T-maze task compared to control zebrafish and showed difficulties exerting inhibitory control. An analysis of habituation learning revealed that cognitive impairment in mutants emerges early during development, but could be rescued with a synthetic BDNF agonist. Overall, our study indicates that BDNF has a similar activational effect on cognitive performance in zebrafish and in mammals, supporting the idea that its function is conserved in vertebrates

Inhibitory control in zebrafish, Danio rerio

We assessed whether zebrafish, Danio rerio, display inhibitory control using a simple and rapid behavioural test. Zebrafish were exposed to a prey stimulus placed inside a transparent tube, which initially elicited attack behaviour. However, zebrafish showed a rapid reduction in the number of attacks towards the prey, which indicated the ability to inhibit their foraging behaviour. Zebrafish also exhibited mnemonic retention of foraging inhibition, as indicated by a reduced number of attacks in a subsequent exposure to the unreachable prey. The ability to inhibit the foraging behaviour varied across three genetically separated wild-type strains and across different individuals within strains, suggesting that zebrafish show heritable within-species differences in inhibitory control. Our behavioural test might be suitable for screening large zebrafish populations in mutational studies and assessing the effects of pharmacologically active substances on inhibitory control

Tadpoles modulate antipredator responses according to the abundance of vegetation experienced during the embryonic stage

Because of the selection pressures imposed by predation and the costs of antipredator responses, prey often exhibit phenotypically plastic behavioural defences that vary with risk level. For anuran larvae, the presence of vegetation is a critical environmental factor that predicts predation risk: in habitats with abundant vegetation, tadpoles are much less likely to be caught by fish and invertebrate predators. Hence, tadpoles might display the ability to match their antipredator behaviour with the amount of vegetation in the environment. I investigated this hypothesis by comparing the acute antipredator responses of tadpoles experimentally raised under high-vegetation and low-vegetation treatment from the egg stage. To address at which developmental stage the behavioural plasticity appeared, I additionally tested two groups of tadpoles that switched from a high- to low-vegetation habitat and vice versa soon after hatching. I observed a stronger antipredator response in tadpoles that experienced the environment with abundant vegetation at the embryonic stage. The environment experienced during the larval stage did not affect the tadpoles' antipredator behaviour. The direction of the observed plasticity aligns with the prediction of the risk allocation model. Therefore, my study seems to support the hypothesis that tadpoles can tune their antipredator behaviour not only based on the direct risk experienced (i.e. the number of predatory attacks) but also based on vegetation, an environmental factor that indirectly predicts predation risk

Personality traits covary with individual differences in inhibitory abilities in 2 species of fish

In a number of animal species, individuals differ in their ability to solve cognitive tasks. However, the mechanisms underlying this variability remain unclear. It has been proposed that individual differences in cognition may be related to individual differences in behavior (i.e., personality); a hypothesis that has received mixed support. In this study, we investigated whether personality correlates with the cognitive ability that allows inhibiting behavior in 2 teleost fish species, the zebrafish Danio rerio and the guppy Poecilia reticulata. In both species, individuals that were bolder in a standard personality assay, the open-field test, showed greater inhibitory abilities in the tube task, which required them to inhibit foraging behavior toward live prey sealed into a transparent tube. This finding reveals a relationship between boldness and inhibitory abilities in fish and lends support to the hypothesis of a link between personality and cognition. Moreover, this study suggests that species separated by a relatively large phylogenetic distance may show the same link between personality and cognition, when tested on the same tasks

Guppies show rapid and lasting inhibition of foraging behaviour

To cope with the variable environment, animals are continuously required to learn novel behaviours or, in certain cases, to inhibit automatic and previously learned behaviours. Traditionally, inhibition has been regarded as cognitively demanding and studied mostly in primates, other mammals and birds, using laboratory tasks, such as the cylinder task. Recent studies have also revealed that fish show high levels of inhibition in the cylinder task. However, conclusions on such results are undermined by evidence that the cylinder task may be inappropriate to compare such phylogenetically distant species. Here, we studied whether a fish, the guppy, Poecilia reticulata, could learn to inhibit behaviour using a different paradigm, which exploited spontaneous foraging behaviour and overcame some drawbacks that characterised the cylinder task. We exposed guppies to live brine shrimp nauplii, Artemia salina, enclosed within a transparent tube. Initially, the guppies attempted to attack the prey but over time showed a rapid decrease of the attacks. Control tests seemed to exclude the possibility that this behavioural trend was due to response to novelty or habituation, and suggested that the guppies were learning to inhibit the foraging behaviour. Memory tests indicated that guppies retained the inhibition of foraging behaviour for at least 24 h. Our study seems to indicate that teleost fish display rapid and durable inhibition of spontaneous foraging behaviour; this may be related to previous evidence, from the cylinder task, supporting efficient behavioural inhibition in this taxon

Guppies show rapid and lasting inhibition of foraging behaviour

To cope with the variable environment, animals are continuously required to learn novel behaviours or, in certain cases, to inhibit automatic and previously learned behaviours. Traditionally, inhibition has been regarded as cognitively demanding and studied mostly in primates, other mammals and birds, using laboratory tasks, such as the cylinder task. Recent studies have also revealed that fish show high levels of inhibition in the cylinder task. However, conclusions on such results are undermined by evidence that the cylinder task may be inappropriate to compare such phylogenetically distant species. Here, we studied whether a fish, the guppy, Poecilia reticulata, could learn to inhibit behaviour using a different paradigm, which exploited spontaneous foraging behaviour and overcame some drawbacks that characterised the cylinder task. We exposed guppies to live brine shrimp nauplii, Artemia salina, enclosed within a transparent tube. Initially, the guppies attempted to attack the prey but over time showed a rapid decrease of the attacks. Control tests seemed to exclude the possibility that this behavioural trend was due to response to novelty or habituation, and suggested that the guppies were learning to inhibit the foraging behaviour. Memory tests indicated that guppies retained the inhibition of foraging behaviour for at least 24 h. Our study seems to indicate that teleost fish display rapid and durable inhibition of spontaneous foraging behaviour; this may be related to previous evidence, from the cylinder task, supporting efficient behavioural inhibition in this taxon