Linking parasitism to network centrality and the impact of sampling bias in its interpretation

Abstract Group living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission, because increased numbers or frequencies of social contacts is often associated with increased parasite abundance or diversity. The social structure of a group or population has been shown to be paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the social transmission of parasites in animals, and especially in primates, have only taken into account parts of the group (e.g., only adults or even only adult females), which is likely to impact the interpretation of any results linking sociality and parasitism. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a complete group of Japanese macaques ( Macaca fuscata ). We then tested the impact of missing parts of the group on this relationship. We aimed to test: (1) whether social network centrality – the number of partners (degree), frequency of interactions (strength) and level of social integration (eigenvector) – was linked to parasite infection intensity; and, (2) to what extent excluding all or portions of individuals within the group from the analyses might influence the observed relationship. We conducted social network analysis on data collected from one complete group of Japanese macaques over two months on Koshima Island, Japan, to relate metrics of network centrality to an index of parasite infection intensity (eggs per gram of feces: EPG). We then ran a series of knock-out simulations to test the effect(s) of accounting only for certain age-sex classes on the observed relationship. General linear mixed models showed that, in the complete network, centrality was positively associated with infection by the examined geohelminths ( Oesophagostomum aculeatum, Trichuris trichiura and Strongyloides fuelleborni ), but in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still positive - lost statistical significance. Our study indicates that sampling bias can impact the relationship that is observed between social interaction and parasitism. In addition to supporting earlier results linking geohelminths to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with applications to infectious disease epidemiology, population management, and health interventions.