Infectious disease, behavioural flexibility and the evolution of culture in primates

Abstract

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.

Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates

“…Culturally acquired knowledge is typically adaptive and may often promote growth and survival of both learners and their dependent young, and thereby extend lifespans (25-27) via a cognitive buffer effect whereby social learning allows individuals to adapt behaviorally to challenging environments (41,42). These benefits may be sufficient to compensate for negative fitness consequences associated with reliance on social learning, such as increased risk of social transmission of parasites (39). Although hypotheses for the coevolution of lifespan and culture propose that increases in both juvenile period and overall lifespan are related to reliance on culturally transmitted knowledge (e.g., ref.…”

“…Second, our social learning measure is largely based on observational reports, not controlled experimental tests, whereas social learning is challenging to identify from observation alone (21,25). However, this approach provides a more naturalistic comparative measure of social learning in comparison with those based on experimental tests, representing a far broader range of primate behavioral diversity, necessary for large-scale comparative investigations (21,25,32,39,60). Results based on patterns of observational accounts of social learning across species should be valuable in informing and directing future, larger scale comparative experimental investigations of variation in social learning abilities across species (21,39,61).…”

“…Instances of social learning were identified using keywords (e.g., "social learning," "cultural transmission," and "traditional") to minimize subjectivity in the collation of reports from the literature (21,25). Although identifying social learning from literature reports of nonhuman primate behavior is inherently challenging, this approach allows for a quantitative behavioral measure of social learning across a large sample of diverse primate species, supporting far larger scale comparative analyses than would be possible using data from controlled experiments alone (21,25,32,39,60). Experimental approaches to measuring social learning across species are associated with their own particular challenges, especially in comparability and ecological validity of behavioral tests, and limited statistical power due to smaller sample sizes (21,25,61).…”

The coevolution of innovation and technical intelligence in primates

“…For example, comparative analysis of observational reports of innovation across primate species reveal that innovation rate covaries together with other observational measures thought to indicate general cognitive ability, such as rates of social learning, tool use and tactical deception [18,19], as well as with experimental tests of learning and problem-solving [20][21][22]. Similarly, experimentally induced and other novel behaviour in corvids [23,24] supports the idea that innovations appear when existing, domain-general abilities are applied to a novel problem.…”

“…Similarly, experimentally induced and other novel behaviour in corvids [23,24] supports the idea that innovations appear when existing, domain-general abilities are applied to a novel problem. However, there is some evidence that innovation may carry specific costs, such as exposure to environmentally transmitted parasites [19]. Behaviour patterns described as innovations encompass a huge range of behaviour, likely involving multiple psychological processes [25,26].…”