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.

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.

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.

The performance of field sampling for parasite detection in a wild passerine.

Parasites can impact the behavior of animals and alter the interplay with ecological factors in their environment. Studying the effects that parasites have on animals thus requires accurate estimates of infections in individuals. However, quantifying parasites can be challenging due to several factors. Laboratory techniques, physiological fluctuations, methodological constraints, and environmental influences can introduce measurement errors, in particular when screening individuals in the wild. These issues are pervasive in ecological studies where it is common to sample study subjects only once. Such factors should be carefully considered when choosing a sampling strategy, yet presently there is little guidance covering the major sources of error. In this study, we estimate the reliability and sensitivity of different sampling practices at detecting two internal parasites-Serratospiculoides amaculata and Isospora sp.-in a model organism, the great tit Parus major. We combine field and captive sampling to assess whether individual parasite infection status and load can be estimated from single field samples, using different laboratory techniques-McMaster and mini-FLOTAC. We test whether they vary in their performance, and quantify how sample processing affects parasite detection rates. We found that single field samples had elevated rates of false negatives. By contrast, samples collected from captivity over 24 h were highly reliable (few false negatives) and accurate (repeatable in the intensity of infection). In terms of methods, we found that the McMaster technique provided more repeatable estimates than the mini-FLOTAC for S. amaculata eggs, and both techniques were largely equally suitable for Isospora oocysts. Our study shows that field samples are likely to be unreliable in accurately detecting the presence of parasites and, in particular, for estimating parasite loads in songbirds. We highlight important considerations for those designing host-parasite studies in captive or wild systems giving guidance that can help select suitable methods, minimize biases, and acknowledge possible limitations.

Population turnover facilitates cultural selection for efficiency in birds.

Culture, defined as socially transmitted information and behaviors that are shared in groups and persist over time, is increasingly accepted to occur across a wide range of taxa and behavioral domains.1 While persistent, cultural traits are not necessarily static, and their distribution can change in frequency and type in response to selective pressures, analogous to that of genetic alleles. This has led to the treatment of culture as an evolutionary process, with cultural evolutionary theory arguing that culture exhibits the three fundamental components of Darwinian evolution: variation, competition, and inheritance.2-5 Selection for more efficient behaviors over alternatives is a crucial component of cumulative cultural evolution,6 yet our understanding of how and when such cultural selection occurs in non-human animals is limited. We performed a cultural diffusion experiment using 18 captive populations of wild-caught great tits (Parus major) to ask whether more efficient foraging traditions are selected for, and whether this process is affected by a fundamental demographic process-population turnover. Our results showed that gradual replacement of individuals with naive immigrants greatly increased the probability that a more efficient behavior invaded a population's cultural repertoire and outcompeted an established inefficient behavior. Fine-scale, automated behavioral tracking revealed that turnover did not increase innovation rates, but instead acted on adoption rates, as immigrants disproportionately sampled novel, efficient behaviors relative to available social information. These results provide strong evidence for cultural selection for efficiency in animals, and highlight the mechanism that links population turnover to this process.

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.