Parasite exposure and host susceptibility jointly drive the emergence of epidemics

Parasite transmission is thought to depend on both parasite exposure and
host susceptibility to infection; however, the relative contribution of
these two factors to epidemics remains unclear. We used interactions
between an aquatic host and its fungal parasite to evaluate how parasite
exposure and host susceptibility interact to drive epidemics. In six
lakes, we tracked the following factors from pre-epidemic to epidemic
emergence: 1) parasite exposure (measured observationally as fungal spores
attacking wild-caught hosts), 2) host susceptibility (measured
experimentally as the number of fungal spores required to produce terminal
infection), 3) host susceptibility traits (barrier resistance and internal
clearance, both quantified with experimental assays), and 4) parasite
prevalence (measured observationally from wild-caught hosts). Tracking
these factors over six months and in almost 7,000 wild-caught hosts
provided key information on the drivers of epidemics. We found that
epidemics depended critically on the interaction of exposure and
susceptibility; epidemics only emerged when a host population’s level of
exposure exceeded its individuals’ capacity for recovery. Additionally, we
found that host internal clearance traits (the hemocyte response) were
critical in regulating epidemics. Our study provides an empirical
demonstration of how parasite exposure and host susceptibility interact to
inhibit or drive disease in natural systems and demonstrates that
epidemics can be delayed by asynchronicity in the two processes. Finally,
our results highlight how individual host traits can scale up to influence
broad epidemiological patterns.