Behavioral Correlates of Parasite Risk Among Humans, Primates, and Other Mammals: Social Contact, Exploratory Tendency, and the Foundations of Culture

Abstract

Social learning and innovation are the behavioral processes that together create the emergent phenomenon of culture, which allows organisms to behaviorally adapt to and thrive in new environments. However, these processes can be difficult to quantify in practice. Instead, social contact and environmental exploration are two measurable behavior patterns that underlie the processes of social learning and innovation, respectively. The benefits afforded by these behavior patterns are many, but they also have their costs. Specifically, I test the hypothesis that the social and exploratory behaviors of animals influence their infection by parasites. To better understand the association between cultural behavior and parasitism, I utilize three complementary analytical approaches in this dissertation, each with different study systems, and each focusing on distinct facets of this association. In the first study, I utilized phylogenetic comparative methods among 127 primate species to investigate two competing hypotheses about the broad associations between cultural behavior and parasitism: that cultural behaviors increase exposure to parasites, or that parasite infection drives the emergence of cultural behaviors as compensatory mechanisms. I investigated these hypotheses by assembling datasets on parasite richness and recorded instances of social learning, innovation, and exploration. Bayesian Markov Chain Monte Carlo Phylogenetic Generalized Least Squares (PGLS) analyses indicated that the variety of social learning behaviors covaried positively with richness of socially transmitted parasites, but not with richness of environmentally transmitted parasites. Conversely, the variety of innovative and exploratory behaviors for a primate species covaried positively with environmentally transmitted parasite richness but not with socially transmitted parasite richness. This provided support for the hypothesis that cultural behaviors increase exposure to parasites. Delving further into the social facet of cultural behavior and parasite exposure, my second study employed stochastic simulations of parasite transmission across theoretical populations to investigate how patterns of social contact within groups can impact parasitism. Simple group size indices have proven to be poor predictors of disease risk within a group, and so more complex metrics of social contact merit investigating. By simulating disease transmission through social networks, I developed a novel method for simultaneously accounting for the effects of the structure and size of groups, with respect to disease outbreaks. This structure-standardized group size, which I called “effective network size” was then used in PGLS analyses of 22 primate species for which social network structures had been published to determine whether effective network size was a better predictor than group size of parasite risk, measured by parasite species richness. I found that effective network size performed no better than raw group size, but that the approach has promise for further applications. In my third study, which focused on the exploratory facet of behavior and parasite risk, I designed a longitudinal field study to investigate how exploratory tendencies in a model taxa, rodents, affected their parasite infections as well as their likelihood of associating with humans, which may ultimately affect human exposure to rodent-borne diseases. I predicted that more exploratory rodents, which are expected to interact with their environments more intensely and to venture more often into new environments, would have a greater richness and intensity of parasites and would be found more often in homes (commensal) than less exploratory rodents. I captured rodents in homes and wildlife conservancies in central Kenya and assessed the exploratory tendencies of each captured rodent. I also collected gastrointestinal and ectoparasites from them. As expected, commensal rodents were more exploratory than wild rodents, and these more exploratory individuals had greater intensities of ectoparasites and gastrointestinal parasites. However, contrary to my prediction, commensal rodents had a lower average richness of gastrointestinal parasites. Thus, exploratory behaviors were predictive of parasite infection intensity but not richness. These more heavily burdened animals in human homes may also play an important role in transmitting their parasites to humans. As my three complementary studies show, the social and exploratory behaviors that form the foundations of human and animal culture can have significant impacts on parasitism. These increases in parasite diversity and infection intensity may be most apparent in humans, a species which is undoubtedly dependent on culture for their success and livelihood, from hunter-gatherers to farmers.