Fitness Costs of Plant Disease Resistance

Abstract

Disease is a major agent of evolution by natural selection because infection by a parasite reduces the fitness of its host. Plant populations have evolved many different mechanisms of resistance in response to disease, but, curiously, resistant genotypes rarely supplant susceptible genotypes. Instead, many plant populations are polymorphic at resistance gene loci, meaning that both resistant and susceptible genotypes coexist within a population. The maintenance of polymorphism can be explained if host resistance to disease is most beneficial when most plants are susceptible, and if resistance reduces a plant's fitness in the absence of the parasite. Fitness costs of disease resistance and pathogen virulence are critically important to the maintenance of polymorphism and the direction of host–pathogen coevolution. Costs in conjuncture with host and pathogen life history traits can drive populations towards an ever‐escalating coevolutionary ‘arms‐race’ or can maintain polymorphism through frequency‐dependent selection. Fitness costs of disease resistance may arise in several ways: physiological and metabolic costs of defence against parasites, developmental traits which allow plants to escape disease but are suboptimal for seed production, and trade‐offs between resistance and responses to other microbes. Fitness costs can have important evolutionary consequences in both natural plant populations and in agricultural contexts. Key Concepts Fitness costs of resistance are necessary for the long‐term maintenance of polymorphism, but their presence alone does not guarantee stable polymorphism. Host and pathogen life‐history traits and epidemiology interact with fitness costs of resistance to maintain polymorphism. When polymorphism is stable, the magnitude of costs determines the frequency of host resistance and pathogen virulence. Plants defend themselves in multiple ways and these carry different types of costs. Traits that reduce disease exposure by changing plant growth and phenology tend to be costly. Fitness costs of resistance can be constitutive or induced. Resistance to one type of pathogen can come at the cost of increased susceptibility to another type of pathogen. Costs of resistance and virulence play a role in coevolutionary dynamics in natural populations. In agricultural populations, costs of resistance and virulence can affect resistance breeding and the durability of resistance.

Resistance Genes Affect How Pathogens Maintain Plant Abundance and Diversity

“…Also, if there is a difference between parents and nonparents, one should test whether this effect can be attributed to pathogens (as most previous results did not identify the source of mortality). Finally, we are not aware of any study showing a cost of R-genes in species other than Arabidopsis thaliana (Bruns 2016).…”

The evolution of age-specific resistance to infectious disease

“…Yet the nature of age-specific immunity varies widely, with adults better protected than juveniles in many [5][6][7][8][9][10][12][13][14][15][16][17] but not all cases [4,11,12,18]. Differences in age-related patterns of host immunity exist both within and between species [19][20][21][22], but the reasons behind these diverse patterns are not always well understood. In particular, we lack a detailed understanding of the factors affecting differences in selection for host defences against infectious disease at different host life stages.…”

“…Trivially, physiological constraints may constrain juvenile defences in some species, preventing juveniles from evolving stronger protection against parasitism or herbivory [33,34]. Although this may provide a partial explanation for supressed juvenile defences, artificial selection for increased innate immunity [35][36][37] and evidence of polymorphism in the level of immunity in natural populations [19][20][21][22][38][39][40] have shown that many hosts do not possess the maximum possible level of juvenile immunity. Hence physiological constraints on juvenile defences do not provide a full explanation.…”

The evolution of age-specific resistance to infectious disease

“…Trivially, physiological constraints may constrain juvenile defences in some species, preventing juveniles from evolving stronger protection against parasitism or herbivory [33,34]. Although this may provide a partial explanation for supressed juvenile defences, artificial selection for increased innate immunity [35][36][37] and evidence of polymorphism in the level of immunity in natural populations [19][20][21][22][38][39][40] have shown that many hosts do not possess the maximum possible level of juvenile immunity. Hence physiological constraints on juvenile defences do not provide a full explanation.…”