Resistance Correlations Influence Infection by Foreign Pathogens

AbstractReciprocal 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 on 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 as well as by resistance allele frequencies. Given that preinvasion 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 only by its average infection rate but also by resistance variation resulting from prior selection imposed by endemic diseases.