Questioning the sustainability of quantitative physiological resistance : epidemiological and evolutionary responses of foliar fungal pathogens to changes in wheat plant traits

Crop pathogens are known to rapidly adapt to agricultural practices. Although cultivar resistance breakdown and resistance to pesticides have been broadly studied, little is known about the adaptation of crop pathogens to more quantitative traits such as quantitative resistance. Quantitative resistance could be more sustainable than gene for gene resistance because it exerts a lower selective pressure on pathogens and relies on a variety of plant traits (and probably genes) rather than on a single one. Using a modelling approach, in this study we address the epidemiological and evolutionary responses of the pathogen to changes in several plant traits that impact epidemic development. With the model, we study life history evolution of biotrophic fungal pathogens of wheat. We focus on a single pathogen life history trait, the latent period, which directly determines the amount of resource allocated to growth and reproduction alongside the speed of canopy colonization. We investigate the evolutionary response of pathogens to changing several plant traits such as leaf metabolite concentration, leaf dimension and leaf lifespan. These plant traits impact epidemic development: disease severity is predicted to increase with metabolite content and leaf lifespan. We compare predictions of latent period evolution based on different “empirical” fitness measures such as annual spore production or within-season exponential growth rate, with predictions based on the more rigorous concept of invasion fitness from adaptive dynamics theory. For each of the studied plant traits, we use pairwise invisibility plots to identify evolutionarily stable strategies of the latent period (ESS). The ESS latent period responds differently to the different plant traits: it is longer on plants with long-lasting leaves and shorter on plants with bigger leaves leading to denser canopies. Our results further reveal that early canopy colonization during crop development might be a critical factor determining the issue of between-strain competition and shaping pathogen adaptation in the context of plant quantitative resistance. Finally, we argue that landscape-level heterogeneity may induce maladaptation of the pathogen that may be useful in stalling the evolutionary breakdown of quantitative resistance