Fine-Scale Spatial Covariation between Infection Prevalence and Susceptibility in a Natural Population

The prevalence of infection varies dramatically on a fine spatial scale. Many evolutionary hypotheses are founded on the assumption that this variation is due to host genetics, such that sites with a high frequency of alleles conferring susceptibility are associated with higher infection prevalence. This assumption is largely untested and may be compromised at finer spatial scales where gene flow between sites is high. We put this assumption to the test in a natural snail-trematode interaction in which host susceptibility is known to have a strong genetic basis. A decade of field sampling revealed substantial spatial variation in infection prevalence between 13 sites around a small lake. Laboratory assays replicated over 3 years demonstrate striking variation in host susceptibility among sites in spite of high levels of gene flow between sites. We find that mean susceptibility can explain more than one-third of the observed variation in mean infection prevalence among sites. We estimate that variation in susceptibility and exposure together can explain the majority of variation in prevalence. Overall, our findings in this natural host-parasite system argue that spatial variation in infection prevalence covaries strongly with variation in the distribution of genetically based susceptibility, even at a fine spatial scale.