Spatially structured host genetic diversity leads to the evolution of local specialization

Host heterogeneity and spatial population structure each influence parasite evolution and may interact when space structures contacts between host types. Here, we experimentally evolve granulosis virus in microcosms of its natural Plodia interpunctella (Indian meal moth) host that differ in both spatial structure and host genetic diversity. We control spatial structure by manipulating the viscosity of the food that the larvae live within and host genetic diversity by adding larvae from either one or two non-evolving inbred lines to opposite microcosm ends. We preserve spatial structure across passages and assay virus from different positions within the microcosm on both host genotypes. We find that the lower contact rates between host genotypes resulting from spatial structure can lead to the evolution of locally specialized virus, even when the host population is genetically diverse overall. We also find that spatial structure changes how viruses specialize: viruses evolved in well-mixed environments had lower exploitation rates (proportion infected x virions) on the host they evolved with, while those in spatially structured environments exhibited higher exploitation of familiar hosts. These results demonstrate that spatial structure and host heterogeneity interact to shape pathogen specialization and that the evolutionary consequences of host diversity depend on population structure.