Julie Morand-Ferron retrospective (1977–2022) for FACETS

Cauchoix M., Barragan Jason G., Biganzoli A., Briot J., Guiraud V., El Ksabi N., Lieuré D., Morand‐Ferron J., Chaine A.S.

Morand-Ferron J., Reichert M.S., Quinn J.L.

Behavioural flexibility allows animals to adjust to changes in their environment. Although the cognitive processes that explain flexibility have been relatively well studied in psychology, this is less true for animals in the wild. Here we use data collected automatically during self-administered discrimination-learning trials for two passerine species, and during four phases (habituation, initial learning, first reversal and second reversal) in order to decompose sources of consistent among-individual differences in reversal learning, a commonly used measure for cognitive flexibility. First, we found that, as expected, proactive interference was significantly repeatable and had a negative effect on reversal learning, confirming that individuals with poor ability to inhibit returning to a previously rewarded feeder were also slower to reversal learn. Second, to our knowledge for the first time in a natural population, we examined how sampling of non-rewarding options post-learning affected reversal-learning performance. Sampling quantity was moderately repeatable in blue tits but not great tits; sampling bias, the variance in the proportion of visits to each non-rewarded feeder, was not repeatable for either species. Sampling behaviour did not predict variation in reversal-learning speed to any significant extent. Finally, the repeatability of reversal learning was explained almost entirely by proactive interference for blue tits; in great tits, the effects of proactive interference and sampling bias on the repeatability of reversal learning were indistinguishable. Our results highlight the value of proactive interference as a more direct measurement of cognitive flexibility and shed light on how animals respond to changes in their environment.

Hermer E., Murphy B., Chaine A.S., Morand-Ferron J.

The causes of individual variation in memory are poorly understood in wild animals. Harsh environments with sparse or rapidly changing food resources are hypothesized to favour more accurate spatial memory to allow animals to return to previously visited patches when current patches are depleted. A potential cost of more accurate spatial memory is proactive interference, where accurate memories block the formation of new memories. This relationship between spatial memory, proactive interference, and harsh environments has only been studied in scatter-hoarding animals. We compare spatial memory accuracy and proactive interference performance of non-scatter hoarding great tits (Parus major) from high and low elevations where harshness increases with elevation. In contrast to studies of scatter-hoarders, we did not find a significant difference between high and low elevation birds in their spatial memory accuracy or proactive interference performance. Using a variance partitioning approach, we report the first among-individual trade-off between spatial memory and proactive interference, uncovering variation in memory at the individual level where selection may act. Although we have no evidence of harsh habitats affecting spatial memory, our results suggest that if elevation produced differences in spatial memory between elevations, we could see concurrent changes in how quickly birds can forget.

Poirier M., Kozlovsky D.Y., Morand-Ferron J., Careau V.

General intelligence has been a topic of high interest for over a century. Traditionally, research on general intelligence was based on principal component analyses and other dimensionality reduction approaches. The advent of high-speed computing has provided alternative statistical tools that have been used to test predictions of human general intelligence. In comparison, research on general intelligence in non-human animals is in its infancy and still relies mostly on factor-analytical procedures. Here, we argue that dimensionality reduction, when incorrectly applied, can lead to spurious results and limit our understanding of ecological and evolutionary causes of variation in animal cognition. Using a meta-analytical approach, we show, based on 555 bivariate correlations, that the average correlation among cognitive abilities is low ( r = 0.185; 95% CI: 0.087–0.287), suggesting relatively weak support for general intelligence in animals. We then use a case study with relatedness (genetic) data to demonstrate how analysing traits using mixed models, without dimensionality reduction, provides new insights into the structure of phenotypic variance among cognitive traits, and uncovers genetic associations that would be hidden otherwise. We hope this article will stimulate the use of alternative tools in the study of cognition and its evolution in animals.

Cyr A., Morand-Ferron J., Thériault F.

Spatial information can be valuable, but new environments may be perceived as risky and thus often evoke fear responses and risk-averse exploration strategies such as thigmotaxis or wall-following behavior. Individual differences in risk-taking (boldness) and thigmotaxis have been reported in natural taxa, which may benefit their survival. In neurorobotic, the common approach is to reproduce cognitive phenomena with multiple levels of bio-inspiration into robotic scenarios. Since autonomous robots may benefit from these different behaviors in exploration tasks, this study aims at simulating two exploration strategies in a virtual robot controlled by a spiking neural network. The experimental context consists in a visual learning task solved through an operant conditioning procedure. Results suggest that the proposed neural architecture sustains both behaviors, switching from one to the other by external cues. This original bio-inspired model could be used as a first step toward further investigations of neurorobotic personality modulated by learning and complex exploration contexts.

Careau V., Beauchamp P.P., Bouchard S., Morand-Ferron J.

Standard metabolic rate (SMR) is known to be highly variable across levels of biological organisation (e.g., species, populations, among individuals, within individuals). Some of the variation in SMR can be attributed to factors such as diet, temperature, and body mass, yet much of the residual variation in SMR remains unexplained. Intuitively, we can expect SMR to co-vary with "personality", but the rapidly accumulating empirical evidence on this topic remains equivocal. The goal of this study was to test for a link between SMR and a behavioural syndrome at the among-individual level in wild-caught fall field crickets (Gryllus pennsylvanicus). Paired measurements of SMR and two behavioural traits were repeatedly taken over a two-month period, thus allowing to estimate the among-individual correlations (rind) separately from the residual (within-individual) correlations. The two behavioural traits (latency to exit a refuge in a novel environment and "freezing" time following a stressful stimulus) were significantly and moderately repeatable and were found to be part of a syndrome, as indicated by a strong and positive among-individual correlation (rind = 0.82 ± 0.27). Yet, only latency to exit was significantly and positively correlated with SMR (rind = 0.45 ± 0.21), suggesting that the link between boldness and SMR may be driven by individual differences in responses to novelty and not to simulated predatory cues. Since we found that bold individuals (short latency to exit) consistently had a lower SMR than shy individuals (long latency to exit), our results go against the pace-of-life syndrome hypothesis. Instead, our results suggest the presence of constrains in the energy budgets of crickets, which generated an allocation trade-off between energy spent on physical activity vs. maintenance costs (SMR).

Boogert N.J., Madden J.R., Morand-Ferron J., Thornton A.

Individuals vary in their cognitive performance. While this variation forms the foundation of the study of human psychometrics, its broader importance is only recently being recognized. Explicitly acknowledging this individual variation found in both humans and non-human animals provides a novel opportunity to understand the mechanisms, development and evolution of cognition. The papers in this special issue highlight the growing emphasis on individual cognitive differences from fields as diverse as neurobiology, experimental psychology and evolutionary biology. Here, we synthesize this body of work. We consider the distinct challenges in quantifying individual differences in cognition and provide concrete methodological recommendations. In particular, future studies would benefit from using multiple task variants to ensure they target specific, clearly defined cognitive traits and from conducting repeated testing to assess individual consistency. We then consider how neural, genetic, developmental and behavioural factors may generate individual differences in cognition. Finally, we discuss the potential fitness consequences of individual cognitive variation and place these into an evolutionary framework with testable hypotheses. We intend for this special issue to stimulate researchers to position individual variation at the centre of the cognitive sciences. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

Cauchoix M., Chow P.K., van Horik J.O., Atance C.M., Barbeau E.J., Barragan-Jason G., Bize P., Boussard A., Buechel S.D., Cabirol A., Cauchard L., Claidière N., Dalesman S., Devaud J.M., Didic M., et. al.

Behavioural and cognitive processes play important roles in mediating an individual's interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability ( R ) in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether R estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean R estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

Hermer E., Cauchoix M., Chaine A.S., Morand-Ferron J.

Environments characterized by scarce and variable food supply, termed “harsh environments,” have been hypothesized to favor cognitive abilities that aid an animal in finding food, remembering where it is located, or predicting its availability. Most studies of the “harsh environment” hypothesis have found that scatter hoarders from harsher environments have better spatial memory abilities, but few studies have looked at this hypothesis in nonscatter hoarders. Here, we present the first comparison of performance on a serial reversal learning task in a nonscatter hoarder from 2 elevations that differ in harshness. Serial reversal learning tasks measure a suite of cognitive abilities that are believed to allow an animal to adjust its foraging behavior to match changes in the availability of food over time. Therefore, performance on this task is predicted to increase with elevation. There was no significant difference between the high and low elevation great tits in initial reversal learning accuracy. While both high and low elevation birds were able to improve their reversal learning accuracy, they did not differ in their rate of improvement over reversals. However, we found that lower elevation birds had higher accuracy across all reversals. Contrary to the “harsh environment” hypothesis, our findings suggest that birds from the less harsh environment at low elevation performed more accurately on the reversal learning task. Overall, our results suggest that the study of the relationship between harshness and cognition in nonhoarders would benefit from taking into account other environmental factors, and trade-offs with other cognitive abilities.

Morand-Ferron J., Hamblin S., Cole E.F., Aplin L.M., Quinn J.L.

Associative learning is essential for resource acquisition, predator avoidance and reproduction in a wide diversity of species, and is therefore a key target for evolutionary and comparative cognition research. Automated operant devices can greatly enhance the study of associative learning and yet their use has been mainly restricted to laboratory conditions. We developed a portable, weatherproof, battery-operated operant device and conducted the first fully automated colour-associative learning experiment using free-ranging individuals in the wild. We used the device to run a colour discrimination task in a monitored population of tits (Paridae). Over two winter months, 80 individuals from four species recorded a total of 5,128 trials. Great tits (Parus major) were more likely than other species to visit the devices and engage in trials, but there were no sex or personality biases in the sample of great tits landing at the devices and registering key pecks. Juveniles were more likely than adults to visit the devices and to register trials. Individuals that were successful at solving a novel technical problem in captivity (lever-pulling) learned faster than non-solvers when at the operant devices in the wild, suggesting cross-contextual consistency in learning performance in very different tasks. There was no significant effect of personality or sex on learning rate, but juveniles’ choice accuracy tended to improve at a faster rate than adults. We discuss how customisable automated operant devices, such as the one described here, could prove to be a powerful tool in evolutionary ecology studies of cognitive traits, especially among inquisitive species such as great tits.

Morand-Ferron J., Cole E.F., Quinn J.L.

Cognition is defined as the processes by which animals collect, retain and use information from their environment to guide their behaviour. Thus cognition is essential in a wide range of behaviours, including foraging, avoiding predators and mating. Despite this pivotal role, the evolutionary processes shaping variation in cognitive performance among individuals in wild populations remain very poorly understood. Selection experiments in captivity suggest that cognitive traits can have substantial heritability and can undergo rapid evolution. However only a handful of studies have attempted to explore how cognition influences life-history variation and fitness in the wild, and direct evidence for the action of natural or sexual selection on cognition is still lacking, reasons for which are diverse. Here we review the current literature with a view to: (i) highlighting the key practical and conceptual challenges faced by the field; (ii) describing how to define and measure cognitive traits in natural populations, and suggesting which species, populations and cognitive traits might be examined to greatest effect; emphasis is placed on selecting traits that are linked to functional behaviour; (iii) discussing how to deal with confounding factors such as personality and motivation in field as well as captive studies; (iv) describing how to measure and interpret relationships between cognitive performance, functional behaviour and fitness, offering some suggestions as to when and what kind of selection might be predicted; and (v) showing how an evolutionary ecological framework, more generally, along with innovative technologies has the potential to revolutionise the study of cognition in the wild. We conclude that the evolutionary ecology of cognition in wild populations is a rapidly expanding interdisciplinary field providing many opportunities for advancing the understanding of how cognitive abilities have evolved.

Aplin L.M., Farine D.R., Morand-Ferron J., Cockburn A., Thornton A., Sheldon B.C.

How socially transmitted behaviours spread and persist is shown in a wild animal population, revealing an effect of social conformity. Although socially transmitted behaviours have been observed in several different species of birds and mammals, little is known about how such behaviours spread and persist. This paper demonstrates a remarkably strong effect of social conformity in wild birds, and elucidates its role in maintaining persistent foraging traditions. Lucy Aplin et al. taught two small groups of wild great tits a different novel foraging strategy and then tracked the spread of the strategy in wild populations when the trained birds were released back into their respective population groups. From just two trained birds, the strategy spread to 75% of the population, with sub-populations heavily biased to perform the technique trained in their group across at least two generations. Birds that had encountered both strategies adopted the local variant. In human societies, cultural norms arise when behaviours are transmitted through social networks via high-fidelity social learning1. However, a paucity of experimental studies has meant that there is no comparable understanding of the process by which socially transmitted behaviours might spread and persist in animal populations2,3. Here we show experimental evidence of the establishment of foraging traditions in a wild bird population. We introduced alternative novel foraging techniques into replicated wild sub-populations of great tits (Parus major) and used automated tracking to map the diffusion, establishment and long-term persistence of the seeded innovations. Furthermore, we used social network analysis to examine the social factors that influenced diffusion dynamics. From only two trained birds in each sub-population, the information spread rapidly through social network ties, to reach an average of 75% of individuals, with a total of 414 knowledgeable individuals performing 57,909 solutions over all replicates. The sub-populations were heavily biased towards using the technique that was originally introduced, resulting in established local traditions that were stable over two generations, despite a high population turnover. Finally, we demonstrate a strong effect of social conformity, with individuals disproportionately adopting the most frequent local variant when first acquiring an innovation, and continuing to favour social information over personal information. Cultural conformity is thought to be a key factor in the evolution of complex culture in humans4,5,6,7. In providing the first experimental demonstration of conformity in a wild non-primate, and of cultural norms in foraging techniques in any wild animal, our results suggest a much broader taxonomic occurrence of such an apparently complex cultural behaviour.

Cole E., Morand-Ferron J., Hinks A., Quinn J.

Cognition has been studied intensively for several decades, but the evolutionary processes that shape individual variation in cognitive traits remain elusive [1-3]. For instance, the strength of selection on a cognitive trait has never been estimated in a natural population, and the possibility that positive links with life history variation [1-5] are mitigated by costs [6] or confounded by ecological factors remains unexplored in the wild. We assessed novel problem-solving performance in 468 wild great tits Parus major temporarily taken into captivity and subsequently followed up their reproductive performance in the wild. Problem-solver females produced larger clutches than nonsolvers. This benefit did not arise because solvers timed their breeding better, occupied better habitats, or compromised offspring quality or their own survival. Instead, foraging range size and day length were relatively small and short, respectively, for solvers, suggesting that they were more efficient at exploiting their environment. In contrast to the positive effect on clutch size, problem solvers deserted their nests more often, leading to little or no overall selection on problem-solving performance. Our results are consistent with the idea that variation in cognitive ability is shaped by contrasting effects on different life history traits directly linked to fitness [1, 3].

Morand-Ferron J., Wu G., Giraldeau L.

Consistent individual differences in behaviour have now been documented in a broad range of organisms over a variety of contexts. However, individual differences in social contexts have received less attention. We explored the consistency and temporal persistence of individual differences in tactic use in a producer–scrounger foraging game using two sets of flocks of wild-caught nutmeg mannikins, Lonchura punctulata. With both sets of birds, we observed significant individual differences in tactic use that persisted under different food distributions and when flock members were reunited at a 6-month interval with the same flockmates but not when flock members were different. In another experiment, in which birds with high-scrounging profiles were made to forage in the same flock, the corporate frequency of scrounging was no higher, and the intake rate no lower than in flocks made up of intermediate- or low-frequency scroungers. Taken together our experiments suggest that persistent individual differences can arise from dynamics that are peculiar to the group in which they occur, underlining the importance of companions’ identity in determining tactic use in this game. Behavioural plasticity can erase idiosyncratic individual differences in games with frequency-dependent payoffs when group composition changes.

Morand-Ferron J., Quinn J.L.

Group living commonly helps organisms face challenging environmental conditions. Although a known phenomenon in humans, recent findings suggest that a benefit of group living in animals generally might be increased innovative problem-solving efficiency. This benefit has never been demonstrated in a natural context, however, and the mechanisms underlying improved efficiency are largely unknown. We examined the problem-solving performance of great and blue tits at automated devices and found that efficiency increased with flock size. This relationship held when restricting the analysis to naive individuals, demonstrating that larger groups increased innovation efficiency. In addition to this effect of naive flock size, the presence of at least one experienced bird increased the frequency of solving, and larger flocks were more likely to contain experienced birds. These findings provide empirical evidence for the “pool of competence” hypothesis in nonhuman animals. The probability of success also differed consistently between individuals, a necessary condition for the pool of competence hypothesis. Solvers had a higher probability of success when foraging with a larger number of companions and when using devices located near rather than further from protective tree cover, suggesting a role for reduced predation risk on problem-solving efficiency. In contrast to traditional group living theory, individuals joining larger flocks benefited from a higher seed intake, suggesting that group living facilitated exploitation of a novel food source through improved problem-solving efficiency. Together our results suggest that both ecological and social factors, through reduced predation risk and increased pool of competence, mediate innovation in natural populations.