Contrasting parasite‐mediated reductions in fitness within versus between patches of a nematode host

Host and parasites interact across spatial scales, but parasite‐mediated fitness effects are typically measured only at local scales. Recent work suggests that parasites can reduce host fitness during dispersal between patches, highlighting the potential for both within‐ and between‐patch effects to contribute to the net fitness consequences of parasitism. Building on this work, we measured the contribution of the dispersal phase to parasite‐mediated reductions in host fitness. We used the nematode Caenorhabditis elegans and its natural microsporidian parasite Nematocida parisii to quantify the fitness consequences of parasitism at the individual, population, and metapopulation level. Nematocida parisii reduced individual fecundity and population growth but had its greatest fitness impact at the dispersal stage: parasitism reduced the fitness of dispersing larvae by 62%–100%. These results indicate that the cost of parasitism in this system is greatly underestimated if the metapopulation level is not taken into account. We also found that the effects of N. parisii vary with host genotype, and the relative advantage of the most resistant genotype increases with inclusion of the dispersal stage. Taken together, our findings demonstrate that host‐parasite interactions at the dispersal stage can magnify selection for parasite resistance.