The central role of host reproduction in determining the evolution of virulence in spatially structured populations

A substantial body of work has shown that local transmission selects for less acute, ‘prudent’ parasites that have lower virulence and transmission rates. This is because parasite strains with higher transmission rates ‘self-shade’ due to a combination of genetic correlations (self: clustered related parasite strains compete for susceptible individuals) and ecological correlations (shade: infected individuals clustering and blocking transmission). However, the interaction of ecological and genetic correlations alongside higher order ecological effects such as patch extinctions means that spatial evolutionary effects can be nuanced; theory has predicted that a relatively small proportion of local infection can select for highest virulence, such that there is a humped relationship between the degree of local infection and the harm that parasites are selected to cause. Here, we examine the separate roles of the interaction scales of reproduction and infection in the context of different degrees of pathogenic castration in determining virulence evolution outcomes. Our key result is that, as long as there is significant reproduction from infected individuals, local infection always selects for lower virulence, and that the prediction that a small proportion of local infection can select for higher virulence only occurs for highly castrating pathogens. The results emphasize the importance of demography for evolutionary outcomes in spatially structured populations, but also show that the core prediction that parasites are prudent in space is reasonable for the vast majority of host-parasite interactions and mixing patterns in nature.