Ecological and Evolutionary Stabilities of Biotrophism, Necrotrophism, and Saprotrophism.

Fungi have multiple trophic behaviors, including biotrophism (parasitism on living hosts), necrotrophism (parasitism through killing host tissues), and saprotrophism (feeding on decaying organic matter). Historical classifications of plant pathogens are based on many different axes, including their trophic dependence on living and dead plants, their pathogenicity and mutualistic relationship to host plants, and their transmission pathways and infection mechanisms. Such diverse classifications sometimes conflict with each other. Clarifying the delineations among these groups would promote synthesis of fungal biology with current ecological and evolutionary concepts. To ask when biotrophic, necrotrophic, or saprotrophic fungi are maintained and favored by selection, we constructed an epidemiological model that describes the transitions between four states of host plants: susceptible living plant (S), infected living plant (I), uninfected dead plant (D), and infected dead plant, or plant residue (R). States S and D represent two kinds of resource-living and dead plant tissues-for fungal inocula (I and R). We obtained values for the basic reproductive number (R0), which defines the persistence criteria of fungi. On the basis of our results, we propose four types of ecological groups, corresponding to the patterns of dependence on nutrient resources: (1) parasitism-dependent fungi, characterized by their critical dependence on living plants; (2) saprotrophism-dependent fungi, characterized by their critical dependence on dead plants; (3) facultatively dependent fungi, which are neither parasitism nor saprotrophism dependent; and (4) doubly dependent fungi, which are neither wholly parasitism dependent nor wholly saprotrophism dependent. This grouping can be used to suggest principles for effective pest control. Our model also reveals simple conditions for the evolution of fungal trophic behaviors. We found that, in the absence of a trade-off between virulence and other life-history parameters, milder fungal virulence in living plants is always selected for if plant-fungus population dynamics are stable. However, with sufficiently strong necrotrophic transmission, the host population densities show sustained cycles, which promote the evolution of higher virulence. Epidemiological synthesis of diverse trophism in plant-fungi relationship in our model thus opens the way to discuss the evolution of fungal lifestyles as a function of ecological conditions.