Reciprocal selection promotes the specificity of host-pathogen associations and resistance polymorphisms in response to disease. However, plants and animals also vary in response to pathogen species not previously encountered in nature, with potential effects on new disease emergence. Using anther-smut disease, we show that resistance (measured as infection rates) to foreign pathogens can be correlated with standing variation in resistance to an endemic pathogen. In Silene vulgaris, genetic variation in resistance to its endemic anther-smut pathogen correlated positively with resistance variation to an anther-smut pathogen from another host, but the relationship was negative between anther-smut and a necrotrophic pathogen. We present models describing the genetic basis for assessing resistance relationships between endemic and foreign pathogens and for quantifying infection probabilities upon foreign pathogen introduction. We show that even when the foreign pathogen has a lower average infection ability than the endemic pathogen, infection outcomes are determined by the sign and strength of the regression of the host’s genetic variation in infection rates by a foreign pathogen on variation in infection rates by an endemic pathogen, and by resistance allele frequencies. Given that pre-invasion equilibria of resistance are determined by factors including resistance costs, we show that protection against foreign pathogens afforded by positively correlated resistances can be lessened or even result in elevated infection risk at the population level, depending on local dynamics. Therefore, a pathogen’s emergence potential could be influenced, not just by its average infection rate, but by resistance variation resulting from prior selection imposed by endemic diseases.

Seeds of Silene vulgaris were sampled from natural populations as 28 maternal half-sib families (seeds from a single maternal plant, but where multiple sires are possible), with two families from each of 14 localities.  The seed families were used for inoculation experiments, testing the relationship between infection rates (proportions that became diseased following exposure to the pathogen) for an endemic pathogen of S. vulgaris (the anther-smut pathogen Microbotryum silenes-inflatae) and a foreign pathogen (anther-smut pathogen Microbotryum lychnidis-dioicae that normally occurs on a different host, Silene latifolia) and a foreign necrotrophic pathogen (Stemphylium solani).  The endemic pathogen, M. silenes-inflatae, was collected as the spore contents of a diseased S. vulgaris flower from one of the populations (coordinates, 44.212, 7.672).  The foreign pathogen, M. lychnidis-dioicae, was collected from a diseased S. latifolia plant in Lamole, Italy (coordinates, 43.551, 11.358). The necrotrophic foliar pathogen, Stemphylium solani, was isolated from an S. vulgaris plant in the introduced range in Bernardston, MA (coordinates, 42.682, -72.544) and cultured on malt extract agar.  Its identity was confirmed by the DNA sequence of the internal transcribed spacer region of the ribosomal RNA (GenBank accession MN856663).  Data show the locations of the seed collections and the proportions of plants that became diseased following exposure to the pathogen or lesion size (cm²), also showing sample sizes.