Kyriacos Kareklas
@gulbenkian.pt
Integrative Behavioural Biology Group
Gulbenkian Research Institute
RESEARCH, TEACHING, or OTHER INTERESTS
Ecology, Evolution, Behavior and Systematics, Animal Science and Zoology, Behavioral Neuroscience
Scopus Publications
Scholar Citations
Scholar h-index
Scholar i10-index
Scopus Publications
Kyriacos Kareklas and Rui F. Oliveira
Springer International Publishing
Kyriacos Kareklas, Magda C. Teles, Elena Dreosti, and Rui F. Oliveira
Springer Science and Business Media LLC
Abstract Background Animal models enable targeting autism-associated genes, such as the shank3 gene, to assess their impact on behavioural phenotypes. However, this is often limited to simple behaviours relevant for social interaction. Social contagion is a complex phenotype forming the basis of human empathic behaviour and involves attention to the behaviour of others for recognizing and sharing their emotional or affective state. Thus, it is a form of social communication, which constitutes the most common developmental impairment across autism spectrum disorders (ASD). Methods Here we describe the development of a zebrafish model that identifies the neurocognitive mechanisms by which shank3 mutation drives deficits in social contagion. We used a CRISPR-Cas9 technique to generate mutations to the shank3a gene, a zebrafish paralogue found to present greater orthology and functional conservation relative to the human gene. Mutants were first compared to wild types during a two-phase protocol that involves the observation of two conflicting states, distress and neutral, and the later recall and discrimination of others when no longer presenting such differences. Then, the whole-brain expression of different neuroplasticity markers was compared between genotypes and their contribution to cluster-specific phenotypic variation was assessed. Results The shank3 mutation markedly reduced social contagion via deficits in attention contributing to difficulties in recognising affective states. Also, the mutation changed the expression of neuronal plasticity genes. However, only downregulated neuroligins clustered with shank3a expression under a combined synaptogenesis component that contributed specifically to variation in attention. Limitations While zebrafish are extremely useful in identifying the role of shank3 mutations to composite social behaviour, they are unlikely to represent the full complexity of socio-cognitive and communication deficits presented by human ASD pathology. Moreover, zebrafish cannot represent the scaling up of these deficits to higher-order empathic and prosocial phenotypes seen in humans. Conclusions We demonstrate a causal link between the zebrafish orthologue of an ASD-associated gene and the attentional control of affect recognition and consequent social contagion. This models autistic affect-communication pathology in zebrafish and reveals a genetic attention-deficit mechanism, addressing the ongoing debate for such mechanisms accounting for emotion recognition difficulties in autistic individuals.
Júlia S. Pinho, Vincent Cunliffe, Kyriacos Kareklas, Giovanni Petri, and Rui F. Oliveira
Springer Science and Business Media LLC
AbstractGroup living animals use social and asocial cues to predict the presence of reward or punishment in the environment through associative learning. The degree to which social and asocial learning share the same mechanisms is still a matter of debate. We have used a classical conditioning paradigm in zebrafish, in which a social (fish image) or an asocial (circle image) conditioned stimulus (CS) have been paired with an unconditioned stimulus (US=food), and we have used the expression of the immediate early gene c-fos to map the neural circuits associated with each learning type. Our results show that the learning performance is similar to social and asocial CSs. However, the brain regions activated in each learning type are distinct and a community analysis of brain network data reveals segregated functional submodules, which seem to be associated with different cognitive functions involved in the learning tasks. These results suggest that, despite localized differences in brain activity between social and asocial learning, they share a common learning module and social learning also recruits a specific social stimulus integration module. Therefore, our results support the occurrence of a common general-purpose learning module, that is differentially modulated by localized activation in social and asocial learning.
Kyriacos Kareklas, Magda C. Teles, Ana Rita Nunes, and Rui F. Oliveira
Wiley
AbstractThe fitness benefits of social life depend on the ability of animals to affiliate with others and form groups, on dominance hierarchies within groups that determine resource distribution, and on cognitive capacities for recognition, learning and information transfer. The evolution of these phenotypes is coupled with that of neuroendocrine mechanisms, but the causal link between the two remains underexplored. Growing evidence from our research group and others demonstrates that the tools available in zebrafish, Danio rerio, can markedly facilitate progress in this field. Here, we review this evidence and provide a synthesis of the state‐of‐the‐art in this model system. We discuss the involvement of generalized motivation and cognitive components, neuroplasticity and functional connectivity across social decision‐making brain areas, and how these are modulated chiefly by the oxytocin‐vasopressin neuroendocrine system, but also by reward‐pathway monoamine signaling and the effects of sex‐hormones and stress physiology.
Ibukun Akinrinade, Kyriacos Kareklas, Magda C. Teles, Thais K. Reis, Michael Gliksberg, Giovanni Petri, Gil Levkowitz, and Rui F. Oliveira
American Association for the Advancement of Science (AAAS)
Emotional contagion is the most ancestral form of empathy. We tested to what extent the proximate mechanisms of emotional contagion are evolutionarily conserved by assessing the role of oxytocin, known to regulate empathic behaviors in mammals, in social fear contagion in zebrafish. Using oxytocin and oxytocin receptor mutants, we show that oxytocin is both necessary and sufficient for observer zebrafish to imitate the distressed behavior of conspecific demonstrators. The brain regions associated with emotional contagion in zebrafish are homologous to those involved in the same process in rodents (e.g., striatum, lateral septum), receiving direct projections from oxytocinergic neurons located in the pre-optic area. Together, our results support an evolutionary conserved role for oxytocin as a key regulator of basic empathic behaviors across vertebrates.
Kyriacos Kareklas, Hansjoerg P. Kunc, and Gareth Arnott
Springer Science and Business Media LLC
Abstract Background Animals use contests to attain resources and employ strategic decisions to minimise contest costs. These decisions are defined by behavioural response to resource value and competitive ability, but remain poorly understood. This is because the two factors are typically studied separately. Also, their study relies on overgeneralised assumptions that (i) strategies are fixed, (ii) modulated by the motivation or drive to fight and (iii) used to manage costs proportional to the timing of the loser’s retreat. To address these problems, we adopt an integrative sequential analysis that incorporates competitive ability and resource value factors, to characterise territorial contest decisions in male Siamese fighting fish (Betta splendens). Results Individuals exhibited a chronological organisation of behaviour, engaging opponents first with frontal display, then switching to lateral display before deciding to attack, and reserved retreats for later stages. Using asymmetries in retreats as a proxy for outcome, the likelihood of winning was found to be mostly dependent on display. However, resource and contest conditions affected initiation latency, display, attack and retreat, suggesting that strategic decisions influence all behaviour. Overall, sequential behaviour varied consistently with individual aggressiveness and resource-value factors, and increasingly with information on competitive ability collected during the contest. This enabled shifts in tactics, such as disadvantaged individuals responding first with aggression and later with submission. Motivation to continue fighting, after interruption by startle, was also adjusted to information gathered during the contest and progressively with energetic state. Two clusters of correlated behaviours were identified, cost-mitigation (display and retreat) and escalation (initiation and attack), but changes in motivation were associated only with cost mitigation. Conclusions Our findings contrast dominant assumptions that strategic decisions are fixed, controlled by motivational state and sufficiently described by outcome-dependent measures. We instead demonstrate that strategic decisions are complex, comprising functional changes in assessment, information use and motivational effects, which are not always inter-dependent.
Claúdia Gonçalves, Kyriacos Kareklas, Magda C. Teles, Susana A. M. Varela, João Costa, Ricardo B. Leite, Tiago Paixão, and Rui F. Oliveira
Wiley
AbstractSociality relies on motivational and cognitive components that may have evolved independently, or may have been linked by phenotypic correlations driven by a shared selective pressure for increased social competence. Furthermore, these components may be domain‐specific or of general‐domain across social and non‐social contexts. Here, we used zebrafish to test if the motivational and cognitive components of social behavior are phenotypically linked and if they are domain specific or of general domain. The behavioral phenotyping of zebrafish in social and equivalent non‐social tests shows that the motivational (preference) and cognitive (memory) components of sociality: (1) are independent from each other, hence not supporting the occurrence of a sociality syndrome; and (2) are phenotypically linked to non‐social traits, forming two general behavioral modules, suggesting that sociality traits have been co‐opted from general‐domain motivational and cognitive traits. Moreover, the study of the association between single nucleotide polymorphisms (SNPs) and each behavioral module further supports this view, since several SNPs from a list of candidate “social” genes, are statistically associated with the motivational, but not with the cognitive, behavioral module. Together, these results support the occurrence of general‐domain motivational and cognitive behavioral modules in zebrafish, which have been co‐opted for the social domain.
Kyriacos Kareklas, Hansjoerg P. Kunc, and Gareth Arnott
Springer Science and Business Media LLC
Abstract Background Competition is considered to rely on the value attributed to resources by animals, but the influence of extrinsic stressors on this value remains unexplored. Although natural or anthropogenic environmental stress often drives decreased competition, assumptions that this relies on resource devaluation are without formal evidence. According to theory, physiological or perceptual effects may influence contest behaviour directly, but motivational changes due to resource value are expected to manifest as behavioural adjustments only in interaction with attainment costs and resource benefits. Thus, we hypothesise that stressor-induced resource devaluations will impose greater effects when attainment costs are high, but not when resource benefits are higher. Noise may elicit such effects because it impacts the acoustic environment and imposes physiological and behavioural costs to animals. Therefore, we manipulated the acoustic environment using playbacks of artificial noise to test our hypotheses in the territorial male Siamese fighting fish, Betta splendens. Results Compared to a no-playback control, noise reduced defense motivation only when territory owners faced comparatively bigger opponents that impose greater injury costs, but not when territories also contained bubble nests that offer reproductive benefits. In turn, nest-size decreases were noted only after contests under noise treatment, but temporal nest-size changes relied on cross-contest variation in noise and comparative opponent size. Thus, the combined effects of noise are conditional on added attainment costs and offset by exceeding resource benefits. Conclusion Our findings provide support for the hypothesised modulation of resource value under extrinsic stress and suggest implications for competition under increasing anthropogenic activity.
Kyriacos Kareklas, Rebekah McMurray, and Gareth Arnott
Elsevier BV
Kyriacos Kareklas, James Wilson, Hansjoerg P. Kunc, and Gareth Arnott
The Royal Society
Contestants use displays to signal their aggressive intent and settle disputes before they escalate. For birds, this is often in the form of song, which can vary in structural complexity. The role of song complexity in signalling aggressive intent has not been fully established, and its efficacy could be influenced by background noise levels. Using playback experiments, we found that in European robins, Erithacus rubecula, song complexity signalled sender aggression and affected receiver response. However, increased noise impacted the ability of contestants to adjust response based on opponent song complexity. These findings provide new evidence regarding the use of acoustic signal complexity for assessing opponent aggression and that noise can influence contest behaviour by interrupting this process, which could impose fitness consequences.
Kyriacos Kareklas, Gareth Arnott, Robert W. Elwood, and Richard A. Holland
Elsevier BV
Kyriacos Kareklas, Robert W. Elwood, and Richard A. Holland
Elsevier BV
Kyriacos Kareklas, Robert W. Elwood, and Richard A. Holland
The Company of Biologists
We tested zebrafish shoals to examine whether groups exhibit collective spatial learning and whether this relates to the personality of group members. To do this we trained shoals to associate a collective spatial decision to a reward and tested whether shoals could reorient to the learned location from a new starting point. There were strong indications of collective learning and collective reorienting, most likely by memorising distal cues, but these processes were unrelated to personality differences within shoals. However, there was evidence that group decisions require agreement between differing personalities. Notably, shoals with more boldness variation were more likely to split during training trials and took longer to reach a collective decision. Thus cognitive tasks, such as learning and cue memorisation, may be exhibited collectively, but the ability to reach collective decisions is affected by the personality composition of the group. A likely outcome of the splitting of groups with very disparate personalities is the formation of groups with members more similar in their personality.
Kyriacos Kareklas, Robert W. Elwood, and Richard A. Holland
Wiley
AbstractRecent research has explored links between cognition and personality, with prominent hypotheses proposing that personality drives consistent individual differences in cognitive function. These hypotheses particularly expect bolder individuals to be faster, but less accurate, as a trade‐off in cognitive function. However, cognitive processes are typically interconnected and defined in more complex terms than simply speed and accuracy. Here, we present evidence that personality‐based differences in learning rates are a result of differences in decision‐making during training in a two‐alternative forced‐choice spatial memory task. This was examined in the mormyrid fish Gnathonemus petersii in the presence of light, where both vision and the electric sense are available, and in the dark, where visibility is limited and fish rely mostly on electrosensing. The species is adapted for the dark to avoid visual predators; thus, the presence of light can induce high‐risk and the dark low‐risk. We show that light conditions had little effect on learning, with bolder fish learning faster both in the light and in the dark conditions. Yet the relationship between learning rates and error rates indicates that the effect on learning is indirectly influenced by accuracy during training. Speed‐accuracy trade‐offs were not found in decision‐making, with bolder individuals deciding faster and more accurately both in the light and in the dark. Only learning strategy was affected by light conditions, with significantly more fish preferring response to place learning in the dark than in the light, where distal cues were not visible. We conclude that other than effects from the integration of visual information, bolder individuals show a consistently greater tendency to explore and find food rewards during training. This affects their decision‐making and in turn their learning performance. We highlight the complexity by which personality‐based effects are exhibited in spatial associative learning.
Kyriacos Kareklas, Gareth Arnott, Robert W. Elwood, and Richard A. Holland
Springer Science and Business Media LLC
Kyriacos Kareklas, Daniel Nettle, and Tom V. Smulders
The Royal Society
Upon continued submersion in water, the glabrous skin on human hands and feet forms wrinkles. The formation of these wrinkles is known to be an active process, controlled by the autonomic nervous system. Such an active control suggests that these wrinkles may have an important function, but this function has not been clear. In this study, we show that submerged objects are handled more quickly with wrinkled fingers than with unwrinkled fingers, whereas wrinkles make no difference to manipulating dry objects. These findings support the hypothesis that water-induced finger wrinkles improve handling submerged objects and suggest that they may be an adaptation for handling objects in wet conditions.