Prior exposure to pathogens augments host heterogeneity in susceptibility and has key epidemiological consequences

Abstract

Abstract Pathogen epidemics are key threats to human and wildlife health. Across systems, host protection from pathogens following initial exposure is often incomplete, resulting in recurrent epidemics through partially-immune hosts. Variation in population-level protection has important consequences for epidemic dynamics, but whether acquired protection influences host heterogeneity in susceptibility and its epidemiological consequences remains unexplored. We experimentally investigated whether prior exposure (none, low-dose, or high-dose) to a bacterial pathogen alters host heterogeneity in susceptibility among songbirds. Hosts with no prior pathogen exposure had little variation in protection, but heterogeneity in susceptibility was significantly augmented by prior pathogen exposure, with the highest variability detected in hosts given high-dose prior exposure. An epidemiological model parameterized with experimental data found that heterogeneity in susceptibility from prior exposure more than halved epidemic sizes compared with a homogeneous population with identical mean protection. However, because infection-induced mortality was also greatly reduced in hosts with prior pathogen exposure, reductions in epidemic size were smaller than expected in hosts with prior exposure. These results highlight the importance of variable protection from prior exposure and/or vaccination in driving host heterogeneity and epidemiological dynamics. Author Summary Individuals in a population can be highly variable in terms of whether or not they get sick during a pathogen outbreak. This individual variability in susceptibility has important consequences for how widely a disease can spread in a population. Therefore, it is key to understand what drives such variability in susceptibility among individuals. One possibility is that variable levels of standing immunity in a population, whether from vaccination or previous infection, lead to variability in susceptibility among individuals. We tested whether acquired immunity creates more variability in susceptibility among individuals in a host population, using a songbird disease system as a model. We found that birds that had acquired immunity to a bacterial pathogen were far more variable in their susceptibility. We also show that this population-level variability in itself can strongly suppress disease outbreaks.