Evolutionary dynamics of pathogen resistance and tolerance

Host organisms can respond to the threat of disease either through resistan ce defenses (which inhibit or limit infection) or through tolerance strateg ies (which do not limit infection, but reduce or offset its fitness consequ ences). Here we show that resistance and tolerance can have fundamentally d ifferent evolutionary outcomes, even when they have equivalent short-term b enefit for the host. As a gene conferring disease resistance spreads throug h a population, the incidence of infection declines, reducing the fitness a dvantage of carrying the resistance gene. Thus genes conferring complete re sistance cannot become fixed (i.e., universal) by selection in a host popul ation, and diseases cannot be eliminated solely by natural selection for ho st resistance. By contrast, as a gene conferring disease tolerance spreads through a population, disease incidence rises, increasing the evolutionary advantage of carrying the tolerance gene. Therefore, any tolerance gene tha t can invade a host population will tend to be driven to fixation by select ion. As predicted, field studies of diverse plant species infected by rust fungi confirm that resistance traits tend to be polymorphic and tolerance t raits tend to be fixed. These observations suggest a new mechanism for the evolution of mutualism from parasitism, and they help to explain the ubiqui ty of disease.