Understanding the Role of Naive Learners in Cultural Change.

AbstractA change to a population's social network is a change to the substrate of cultural transmission, affecting behavioral diversity and adaptive cultural evolution. While features of network structure such as population size and density have been well studied, less is understood about the influence of social processes such as population turnover-or the repeated replacement of individuals by naive individuals. Experimental data have led to the hypothesis that naive learners can drive cultural evolution by better assessing the relative value of behaviors, although this hypothesis has been expressed only verbally. We conducted a formal exploration of this hypothesis using a generative model that concurrently simulated its two key ingredients: social transmission and reinforcement learning. We simulated competition between high- and low-reward behaviors while varying turnover magnitude and tempo. Variation in turnover influenced changes in the distributions of cultural behaviors, irrespective of initial knowledge-state conditions. We found optimal turnover regimes that amplified the production of higher reward behaviors through two key mechanisms: repertoire composition and enhanced valuation by agents that knew both behaviors. These effects depended on network and learning parameters. Our model provides formal theoretical support for, and predictions about, the hypothesis that naive learners can shape cultural change through their enhanced sampling ability. By moving from experimental data to theory, we illuminate an underdiscussed generative process that can lead to changes in cultural behavior, arising from an interaction between social dynamics and learning.

Social demonstration of colour preference improves the learning of associated demonstrated actions.

We studied how different types of social demonstration improve house sparrows' (Passer domesticus) success in solving a foraging task that requires both operant learning (opening covers) and discrimination learning (preferring covers of the rewarding colour). We provided learners with either paired demonstration (of both cover opening and colour preference), action-only demonstration (of opening white covers only), or no demonstration (a companion bird eating without covers). We found that sparrows failed to learn the two tasks with no demonstration, and learned them best with a paired demonstration. Interestingly, the action of cover opening was learned faster with paired rather than action-only demonstration despite being equally demonstrated in both. We also found that only with paired demonstration, the speed of operant (action) learning was related to the demonstrator's level of activity. Colour preference (i.e. discrimination learning) was eventually acquired by all sparrows that learned to open covers, even without social demonstration of colour preference. Thus, adding a demonstration of colour preference was actually more important for operant learning, possibly as a result of increasing the similarity between the demonstrated and the learned tasks, thereby increasing the learner's attention to the actions of the demonstrator. Giving more attention to individuals in similar settings may be an adaptive strategy directing social learners to focus on ecologically relevant behaviours and on tasks that are likely to be learned successfully.

Manipulating actions: A selective two-option device for cognitive experiments in wild animals.

Advances in biologging technologies have significantly improved our ability to track individual animals' behaviour in their natural environment. Beyond observations, automation of data collection has revolutionized cognitive experiments in the wild. For example, radio-frequency identification (RFID) antennae embedded in 'puzzle box' devices have allowed for large-scale cognitive experiments where individuals tagged with passive integrated transponder (PIT) tags interact with puzzle boxes to gain a food reward, with devices logging both the identity and solving action of visitors. Here, we extended the scope of wild cognitive experiments by developing a fully automated selective two-option foraging device to specifically control which actions lead to a food reward and which remain unrewarded. Selective devices were based on a sliding-door foraging puzzle, and built using commercially available low-cost electronics. We tested it on two free-ranging PIT-tagged subpopulations of great tits Parus major as a proof of concept. We conducted a diffusion experiment where birds learned from trained demonstrators to get a food reward by sliding the door either to the left or right. We then restricted access of knowledgeable birds to their less preferred side and calculated the latency until birds produced solutions as a measure of behavioural flexibility. A total of 22 of 23 knowledgeable birds produced at least one solution on their less preferred side after being restricted, with higher-frequency solvers being faster at doing so. In addition, 18 of the 23 birds reached their solving rate from prior to the restriction on their less preferred side, with birds with stronger prior side preference taking longer to do so. We therefore introduce and successfully test a new selective two-option puzzle box, providing detailed instructions and freely available software that allows reproducibility. It extends the functionality of existing systems by allowing fine-scale manipulations of individuals' actions and opens a large range of possibilities to study cognitive processes in wild animal populations.

Social network analysis reveals context-dependent kin relationships in wild sulphur-crested cockatoos Cacatua galerita.

A preference to associate with kin facilitates inclusive fitness benefits, and increased tolerance or cooperation between kin may be an added benefit of group living. Many species exhibit preferred associations with kin; however, it is often hard to disentangle active preferences from passive overlap, for example caused by limited dispersal or inheritance of social position. Many parrots exhibit social systems consisting of pair-bonded individuals foraging in variably sized fission-fusion flocks within larger communal roosts of hundreds of individuals. Previous work has shown that, despite these fission-fusion dynamics, individuals can exhibit long-term preferred foraging associations outside their pair bonds. Yet the underlying drivers of these social preferences remain largely unknown. In this study, we use a network approach to examine the influence of kinship on social associations and interactions in wild, communally roosting sulphur-crested cockatoos, Cacatua galerita. We recorded roost co-membership, social associations and interactions in 561 individually marked birds across three neighbouring roosts. We then collected genetic samples from 205 cockatoos, and conducted a relationship analysis to construct a kinship network. Finally, we tested correlations between kinship and four social networks: association, affiliative, low-intensity aggression and high-intensity aggression. Our result showed that while roosting groups were clearly defined, they showed little genetic differentiation or kin structuring. Between roost movement was high, with juveniles, especially females, repeatedly moving between roosts. Both within roosting communities, and when visiting different roosts, individuals preferentially associated with kin. Supporting this, individuals were also more likely to allopreen kin. However, contrary to expectation, individuals preferred to direct aggression towards kin, with this effect only observed when individuals shared roost membership. By measuring social networks within and between large roosting groups, we could remove potential effects of passive spatial overlap on kin structuring. Our study reveals that sulphur-crested cockatoos actively prefer to associate with kin, both within and between roosting groups. By examining this across different interaction types, we further demonstrate that sulphur-crested cockatoos exhibit behavioural and context-dependent interaction rules towards kin. Our results help reveal the drivers of social association in this species, while adding to the evidence for social complexity in parrots.

Cultural diffusion dynamics depend on behavioural production rules.

Culture is an outcome of both the acquisition of knowledge about behaviour through social transmission, and its subsequent production by individuals. Acquisition and production are often discussed or modelled interchangeably, yet to date no study has explored the consequences of their interaction for cultural diffusions. We present a generative model that integrates the two, and ask how variation in production rules might influence diffusion dynamics. Agents make behavioural choices that change as they learn from their productions. Their repertoires may also change, and the acquisition of behaviour is conditioned on its frequency. We analyse the diffusion of a novel behaviour through social networks, yielding generalizable predictions of how individual-level behavioural production rules influence population-level diffusion dynamics. We then investigate how linking acquisition and production might affect the performance of two commonly used inferential models for social learning; network-based diffusion analysis, and experience-weighted attraction models. We find that the influence that production rules have on diffusion dynamics has consequences for how inferential methods are applied to empirical data. Our model illuminates the differences between social learning and social influence, demonstrates the overlooked role of reinforcement learning in cultural diffusions, and allows for clearer discussions about social learning strategies.

Coevolution of relative brain size and life expectancy in parrots.

Previous studies have demonstrated a correlation between longevity and brain size in a variety of taxa. Little research has been devoted to understanding this link in parrots; yet parrots are well-known for both their exceptionally long lives and cognitive complexity. We employed a large-scale comparative analysis that investigated the influence of brain size and life-history variables on longevity in parrots. Specifically, we addressed two hypotheses for evolutionary drivers of longevity: the cognitivebuffer hypothesis, which proposes that increased cognitive abilities enable longer lifespans, and the expensive brain hypothesis, which holds that increases in lifespan are caused by prolonged developmental time of, and increased parental investment in, large-brained offspring. We estimated life expectancy from detailed zoo records for 133 818 individuals across 244 parrot species. Using a principled Bayesian approach that addresses data uncertainty and imputation of missing values, we found a consistent correlation between relative brain size and life expectancy in parrots. This correlation was best explained by a direct effect of relative brain size. Notably, we found no effects of developmental time, clutch size or age at first reproduction. Our results suggest that selection for enhanced cognitive abilities in parrots has in turn promoted longer lifespans.

Social network architecture and the tempo of cumulative cultural evolution.

The ability to build upon previous knowledge-cumulative cultural evolution-is a hallmark of human societies. While cumulative cultural evolution depends on the interaction between social systems, cognition and the environment, there is increasing evidence that cumulative cultural evolution is facilitated by larger and more structured societies. However, such effects may be interlinked with patterns of social wiring, thus the relative importance of social network architecture as an additional factor shaping cumulative cultural evolution remains unclear. By simulating innovation and diffusion of cultural traits in populations with stereotyped social structures, we disentangle the relative contributions of network architecture from those of population size and connectivity. We demonstrate that while more structured networks, such as those found in multilevel societies, can promote the recombination of cultural traits into high-value products, they also hinder spread and make products more likely to go extinct. We find that transmission mechanisms are therefore critical in determining the outcomes of cumulative cultural evolution. Our results highlight the complex interaction between population size, structure and transmission mechanisms, with important implications for future research.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

A citizen science approach reveals long-term social network structure in an urban parrot, Cacatua galerita.

Parrots are often referenced in discussions of social and cognitive complexity, yet relatively little is known of their social organization in the wild. In particular, the presence of long-lasting social ties has been highlighted as a hallmark of social complexity; however, the presence of such ties can be masked in fission-fusion systems like that exhibited by most parrot species. Social network analysis has the potential to elucidate such multi-level dynamics. While most parrot species are tropical canopy dwellers, a subset has successfully colonized urban habitats, where they are often the focus of much public interest. Our study takes advantage of this to use citizen science to collect observations of wing-tagged sulphur-crested cockatoos in central Sydney and record their social associations over multiple years. Using a specifically designed mobile phone application 'Wingtags', we collected over >27,000 citizen science reports of wing-tagged cockatoos, and built social networks from spatial-temporal co-occurrences in observations for 130 tagged birds. To validate this novel methodology, we GPS-tagged a subset of wing-tagged birds and compared networks built from both data collection methods. We then examined correlates of social network structure before exploring the temporal dynamics of network structure and social associations. Social networks constructed from GPS data and citizen science data were highly correlated, suggesting that this novel methodology is robust. Network structure exhibited little seasonal variability and was largely driven by roost site choice; however, individuals also showed a surprising degree of mixing between roosts in their foraging associations. Finally, within this larger fission-fusion system, individuals tended to maintain specific social ties for long periods of time. There was an effect of age on these temporal dynamics, with aging individuals increasing both social stability and longevity of associations. Our findings highlight the utility of citizen science to measure social networks in urban species, and add to the evidence that long-lasting social associations can persist in fission-fusion social systems such as those observed in wild sulphur-crested cockatoos.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

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.

Conformity does not perpetuate suboptimal traditions in a wild population of songbirds.

Social learning is important to the life history of many animals, helping individuals to acquire new adaptive behavior. However despite long-running debate, it remains an open question whether a reliance on social learning can also lead to mismatched or maladaptive behavior. In a previous study, we experimentally induced traditions for opening a bidirectional door puzzle box in replicate subpopulations of the great tit Parus major Individuals were conformist social learners, resulting in stable cultural behaviors. Here, we vary the rewards gained by these techniques to ask to what extent established behaviors are flexible to changing conditions. When subpopulations with established foraging traditions for one technique were subjected to a reduced foraging payoff, 49% of birds switched their behavior to a higher-payoff foraging technique after only 14 days, with younger individuals showing a faster rate of change. We elucidated the decision-making process for each individual, using a mechanistic learning model to demonstrate that, perhaps surprisingly, this population-level change was achieved without significant asocial exploration and without any evidence for payoff-biased copying. Rather, by combining conformist social learning with payoff-sensitive individual reinforcement (updating of experience), individuals and populations could both acquire adaptive behavior and track environmental change.

Movement and conformity interact to establish local behavioural traditions in animal populations.

The social transmission of information is critical to the emergence of animal culture. Two processes are predicted to play key roles in how socially-transmitted information spreads in animal populations: the movement of individuals across the landscape and conformist social learning. We develop a model that, for the first time, explicitly integrates these processes to investigate their impacts on the spread of behavioural preferences. Our results reveal a strong interplay between movement and conformity in determining whether locally-variable traditions establish across a landscape or whether a single preference dominates the whole population. The model is able to replicate a real-world cultural diffusion experiment in great tits Parus major, but also allows for a range of predictions for the emergence of animal culture under various initial conditions, habitat structure and strength of conformist bias to be made. Integrating social behaviour with ecological variation will be important for understanding the stability and diversity of culture in animals.

Social tipping points in animal societies.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.

Wild birds respond to flockmate loss by increasing their social network associations to others.

Understanding the consequences of losing individuals from wild populations is a current and pressing issue, yet how such loss influences the social behaviour of the remaining animals is largely unexplored. Through combining the automated tracking of winter flocks of over 500 wild great tits (Parus major) with removal experiments, we assessed how individuals' social network positions responded to the loss of their social associates. We found that the extent of flockmate loss that individuals experienced correlated positively with subsequent increases in the number of their social associations, the average strength of their bonds and their overall connectedness within the social network (defined as summed edge weights). Increased social connectivity was not driven by general disturbance or changes in foraging behaviour, but by modifications to fine-scale social network connections in response to losing their associates. Therefore, the reduction in social connectedness expected by individual loss may be mitigated by increases in social associations between remaining individuals. Given that these findings demonstrate rapid adjustment of social network associations in response to the loss of previous social ties, future research should examine the generality of the compensatory adjustment of social relations in ways that maintain the structure of social organization.

Interspecific social networks promote information transmission in wild songbirds.

Understanding the functional links between social structure and population processes is a central aim of evolutionary ecology. Multiple types of interactions can be represented by networks drawn for the same population, such as kinship, dominance or affiliative networks, but the relative importance of alternative networks in modulating population processes may not be clear. We illustrate this problem, and a solution, by developing a framework for testing the importance of different types of association in facilitating the transmission of information. We apply this framework to experimental data from wild songbirds that form mixed-species flocks, recording the arrival (patch discovery) of individuals to novel foraging sites. We tested whether intraspecific and interspecific social networks predicted the spread of information about novel food sites, and found that both contributed to transmission. The likelihood of acquiring information per unit of connection to knowledgeable individuals increased 22-fold for conspecifics, and 12-fold for heterospecifics. We also found that species varied in how much information they produced, suggesting that some species play a keystone role in winter foraging flocks. More generally, these analyses demonstrate that this method provides a powerful approach, using social networks to quantify the relative transmission rates across different social relationships.

Individual-level personality influences social foraging and collective behaviour in wild birds.

There is increasing evidence that animal groups can maintain coordinated behaviour and make collective decisions based on simple interaction rules. Effective collective action may be further facilitated by individual variation within groups, particularly through leader-follower polymorphisms. Recent studies have suggested that individual-level personality traits influence the degree to which individuals use social information, are attracted to conspecifics, or act as leaders/followers. However, evidence is equivocal and largely limited to laboratory studies. We use an automated data-collection system to conduct an experiment testing the relationship between personality and collective decision-making in the wild. First, we report that foraging flocks of great tits (Parus major) show strikingly synchronous behaviour. A predictive model of collective decision-making replicates patterns well, suggesting simple interaction rules are sufficient to explain the observed social behaviour. Second, within groups, individuals with more reactive personalities behave more collectively, moving to within-flock areas of higher density. By contrast, proactive individuals tend to move to and feed at spatial periphery of flocks. Finally, comparing alternative simulations of flocking with empirical data, we demonstrate that variation in personality promotes within-patch movement while maintaining group cohesion. Our results illustrate the importance of incorporating individual variability in models of social behaviour.

The ontogeny of social networks in wild great tits (Parus major).

Sociality impacts many biological processes and can be tightly linked to an individual's fitness. To maximize the advantages of group living, many social animals prefer to associate with individuals that provide the most benefits, such as kin, familiar individuals, or those of similar phenotypes. Such social strategies are not necessarily stable over time but can vary with changing selection pressures. In particular, young individuals transitioning to independence should continuously adjust their social behavior in light of developmental changes. However, social strategies exhibited during adolescence in animals are understudied, and the factors underlying social network formation during ontogeny remain elusive. Here, we tracked associations of wild great tits (Parus major) during the transition to independence and across their first year of life. Both spatial and social factors predicted dyadic associations. During the transition to independence in spring, fledglings initially preferred to associate with siblings and peers over non-parent adults. We found no evidence for preferred associations among juveniles of similar age or fledge weight during that time but weak evidence for some potential inheritance of the parental social network. By autumn, after juveniles had reached full independence, they exhibited social strategies similar to those of adults by establishing stable social ties based on familiarity that persisted through winter into the next spring. Overall, this research demonstrates dynamic changes in social networks during ontogeny in a species with a fast life history and limited parental care, which likely reflect changes in selective pressures. It further highlights the importance of long-term social bonds based on familiarity in this species.

Multilevel Bayesian analysis of monk parakeet contact calls shows dialects between European cities.

Geographic differences in vocalizations provide strong evidence for animal culture, with patterns likely arising from generations of social learning and transmission. Most studies on the evolution of avian vocal variation have predominantly focused on fixed repertoire, territorial song in passerine birds. The study of vocal communication in open-ended learners and in contexts where vocalizations serve other functions is therefore necessary for a more comprehensive understanding of vocal dialect evolution. Parrots are open-ended vocal production learners that use vocalizations for social contact and coordination. Geographic variation in parrot vocalizations typically take the form of either distinct regional variations known as dialects or graded variation based on geographic distance known as clinal variation. In this study, we recorded monk parakeets (Myiopsitta monachus) across multiple spatial scales (i.e., parks and cities) in their European invasive range. We then compared calls using a multilevel Bayesian model and sensitivity analysis, with this novel approach allowing us to explicitly compare vocalizations at multiple spatial scales. We found support for founder effects and/or cultural drift at the city level, consistent with passive cultural processes leading to large-scale dialect differences. We did not find a strong signal for dialect or clinal differences between parks within cities, suggesting that birds did not actively converge on a group level signal, as expected under the group membership hypothesis. We demonstrate the robustness of our findings and offer an explanation that unifies the results of prior monk parakeet vocalization studies.