An epi-evolutionary model for predicting the adaptation of spore-producing pathogens to quantitative resistance in heterogeneous environments

Abstract

We have modeled the evolutionary epidemiology of spore-producing plant pathogens in heterogeneous environments sown with several cultivars carrying quantitative resistances. The model explicitly tracks the infection-age structure and genetic composition of the pathogen population. Each strain is characterized by pathogenicity traits determining its infection efficiency and a time-varying sporulation curve taking into account lesion aging. We first derived a general expression of the basic reproduction number $R_0$ for fungal pathogens in heterogeneous environments. We show that the evolutionary attractors of the model coincide with local maxima of $R_0$ only if the infection efficiency is the same on all host types. We then studied the contribution of three basic resistance characteristics (the pathogenicity trait targeted, resistance effectiveness, and adaptation cost), in interaction with the deployment strategy (proportion of fields sown with a resistant cultivar), to (i) pathogen diversification at equilibrium and (ii) the shaping of transient dynamics from evolutionary and epidemiological perspectives. We show that quantitative resistance affecting only the sporulation curve will always lead to a monomorphic population, whereas dimorphism (i.e., pathogen diversification) can occur if resistance alters infection efficiency, notably with high adaptation costs and proportions of the resistant cultivar. Accordingly, the choice of the quantitative resistance genes operated by plant breeders is a driver of pathogen diversification. From an evolutionary perspective, the time to emergence of the evolutionary attractor best adapted to the resistant cultivar tends to be shorter when resistance affects infection efficiency than when it affects sporulation. Conversely, from an epidemiological perspective, epidemiological control is always greater when the resistance affects infection efficiency. This highlights the difficulty of defining deployment strategies for quantitative resistance simultaneously maximizing epidemiological and evolutionary outcomes.

Keywords: adaptive dynamics; basic reproduction number; integro‐differential equations; quantitative resistance; resistance durability; spore‐producing pathogens.