Julie Morand-Ferron

Experimentally induced innovations lead to persistent culture via conformity in wild birds

In human societies, cultural norms arise when behaviours are transmitted through social networks via high-fidelity social learning. 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 populations. 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 humans. 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.

Social networks predict patch discovery in a wild population of songbirds

Animals use social information in a wide variety of contexts. Its extensive use by individuals to locate food patches has been documented in a number of species, and various mechanisms of discovery have been identified. However, less is known about whether individuals differ in their access to, and use of, social information to find food. We measured the social network of a wild population of three sympatric tit species (family Paridae) and then recorded individual discovery of novel food patches. By using recently developed methods for network-based diffusion analysis, we show that order of arrival at new food patches was predicted by social associations. Models based only on group searching did not explain this relationship. Furthermore, network position was correlated with likelihood of patch discovery, with central individuals more likely to locate and use novel foraging patches than those with limited social connections. These results demonstrate the utility of social network analysis as a method to investigate social information use, and suggest that the greater probability of receiving social information about new foraging patches confers a benefit on more socially connected individuals.

Technical innovations drive the relationship between innovativeness and residual brain size in birds

The hypothesis that large brains allow animals to produce novel behaviour patterns is supported by the correlation between brain size, corrected for body size, and the frequency of foraging innovations reported in the literature for both birds and primates. In birds, foraging innovations have been observed in over 800 species, and include behaviours that range from eating a novel food to using tools. Previous comparative studies have quantified innovativeness by summing all reports of innovative behaviour, regardless of the nature of the innovation. Here, we use the variety of foraging innovations recorded for birds to see which of two classic hypotheses best accounts for the relationship between innovativeness and brain size: the technical intelligence hypothesis or the opportunistic-generalism intelligence hypothesis. We classified 2182 innovation cases into 12 categories to quantify the diversity of innovations performed by each of 76 avian families. We found that families with larger brains had a greater repertoire of innovations, and that innovation diversity was a stronger predictor of residual brain size than was total number of innovations. Furthermore, the diversity of technical innovations displayed by bird families was a much better predictor of residual brain size than was the number of food type innovations, providing support for the technical intelligence hypothesis. Our results suggest that the cognitive capacity required to perform a wide variety of novel foraging techniques underpins the positive relationship between innovativeness and brain size in birds. We include a summary of innovation data for 803 species as Supplementary Material.

Cognitive Ability Influences Reproductive Life History Variation in the Wild

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].

Larger groups of passerines are more efficient problem solvers in the wild

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.

Milk bottles revisited: Social learning and individual variation in the blue tit, Cyanistes caeruleus

Blue tits are famous for the ‘milk bottle’ innovation, which emerged at numerous sites across Britain in the early 20th century. However, overall we still know little about the factors that foster or hinder the spread of innovations, or of the impact of individual differences in behaviour on social transmission. We used a two-action and control experimental design to study the diffusion of innovation in groups of wild-caught blue tits, and found strong evidence that individuals can use social learning to acquire novel foraging skills. We then measured six individual characteristics, including innovative problem solving, to investigate potential correlates of individual social-learning tendency. Consistent with a hypothesis of common mechanisms underlying both processes, we found evidence for a relationship between social learning and innovativeness. In addition, we observed significant age- and sex-biased social learning, with juvenile females twice as likely to acquire the novel skill as other birds. Social learning was also more likely in subordinate males than dominant males. Our results identify individual variation and transmission biases that have potential implications for the diffusion of innovations in natural populations.

Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges

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.

Food stealing in birds : brain or brawn?

Kleptoparasitism, the stealing of food items already procured by others, is a widespread foraging strategy in animals, yet the reasons why some taxa have evolved this strategy and others have not remain unresolved. It has been hypothesized that kleptoparasitism should be more profitable, and hence have more often evolved, in lineages featuring certain characteristics, such as a large body mass, an enlarged brain or a dependence on vertebrate prey. Alternatively, the evolution of kleptoparasitism could have been facilitated in certain ecological contexts, such as open habitats or mixed-species foraging groups. Here, we test these hypotheses for the evolution of food stealing with a comparative analysis in birds, using information on 856 field reports of interspecific kleptoparasitism from all over the world. In multivariate analyses controlling for common ancestry, the probability that a family uses kleptoparasitism was positively associated with residual size of the brain, habitat openness and the presence of vertebrate prey in the diet, but showed no association with body size or participation in mixed-species foraging groups. The conclusion that kleptoparasitism is associated more closely with cognition than with aggression is further supported by the finding that kleptoparasites have a larger residual brain size than their respective hosts, while their body size is not significantly larger. By emphasizing the central role of cognitive abilities in avian kleptoparasitism, our results offer a novel perception of avian food stealing, which in the past was primarily seen in terms of ‘brawn’ rather than ‘brains’.

Learning in a game context: strategy choice by some keeps learning from evolving in others

Behavioural decisions in a social context commonly have frequency-dependent outcomes and so require analysis using evolutionary game theory. Learning provides a mechanism for tracking changing conditions and it has frequently been predicted to supplant fixed behaviour in shifting environments; yet few studies have examined the evolution of learning specifically in a game-theoretic context. We present a model that examines the evolution of learning in a frequency-dependent context created by a producer–scrounger game, where producers search for their own resources and scroungers usurp the discoveries of producers. We ask whether a learning mutant that can optimize its use of producer and scrounger to local conditions can invade a population of non-learning individuals that play producer and scrounger with fixed probabilities. We find that learning provides an initial advantage but never evolves to fixation. Once a stable equilibrium is attained, the population is always made up of a majority of fixed players and a minority of learning individuals. This result is robust to variation in the initial proportion of fixed individuals, the rate of within- and between-generation environmental change, and population size. Such learning polymorphisms will manifest themselves in a wide range of contexts, providing an important element leading to behavioural syndromes.

Dunking behaviour in Carib grackles

Dunking behaviour, the dipping of food in water, has been anecdotally observed in more than 25 species of birds in the wild, but its function and ecology have not been systematically studied. In experiments conducted in the field and in captivity on Carib grackles, Quiscalus lugubris, in Barbados, we showed that: (1) dunking rate in the field was influenced by food type and that moistening dry food seems to be one of the major benefits of dunking; (2) most dunking observed in the field was performed by a minority of individuals, but the vast majority (86%) of grackles tested in captivity were capable of dunking; (3) a higher density of conspecifics at a water source was associated with a lower dunking rate and an increased risk of kleptoparasitism when dunking; and (4) there were consistent individual differences in dunking and stealing frequency. We conclude that dunking is part of the normal behavioural repertoire of Carib grackles in Barbados, and that the low frequency of the behaviour in the field did not result from the inability of some individuals to perform the technique, but more likely from the balance of costs and benefits affecting its expression.