Sublethal costs of infection reduce performance of collective tasks in social insects: a modelling study

Group living confers benefits like higher efficiency of foraging, but social insects also face costs such as increased risk of parasitism. Infection can have sublethal effects on individual behaviours and can also alter social interactions among group members. These sublethal effects of infection could scale up to reduce the performance of collective tasks critical to group success, through reductions in individual performance, reduced social recruitment of new individuals to the task, and impaired information-sharing. Alternatively, learning from uninfected groupmates could mitigate individual infection costs and buffer impacts of infection on collective performance. However, we lack a mechanistic framework for quantifying how infection influences collective behaviors through direct and socially-mediated effects. We developed an agent-based model to investigate how infection influences collective foraging performance in a social insect (applied to the ant Temnothorax rugatulus ), where infection could affect individual performance through reduced motion capacity and ability to perceive and orient towards food, and social information transfer through the reduced probability of recruitment to join the foraging task. We varied the magnitude of these behavioral costs of infection in colonies experiencing low, intermediate or high levels of infection, and recorded the effects on colony performance, as well as the reciprocal effects of infected individuals on uninfected individual performance (and vice versa). We found that costs to individual performance caused larger decreases in collective performance the further upstream in the foraging task they occurred, while social costs to recruitment exacerbated these negative effects. Additionally, we found that infected and uninfected ants had reciprocal effects on each other’s performance that scale with infection prevalence, suggesting that social interactions are only likely to buffer reductions in colony performance when infection prevalence is low. Our study provides a mechanistic understanding of how infection-related changes in behaviour can impact groups, with important consequences for fitness of group living insects.