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.

Keywords: coevolution; frequency‐dependent selection; plant disease; plant breeding; fungi; disease resistance; polymorphism; fitness

Figure 1. Resistance level and cost required to maintain resistance polymorphism, under different host lifespans. Resistance level shows the relative difference in transmission between resistant and susceptible genotypes, where 1 is the most resistant and 0 is no resistance. Cost shows the relative difference in reproductive rate between susceptible and resistant genotypes, with 1 being the highest cost and 0 no cost. Dark grey area – resistance sweeps to fixation, white area – resistance is lost, striped area – stable polymorphism. (a) Host lifespan is 2 years, (b) 5 years, (c) 10 years, (d) 20 years. Reproduced with permission from Bruns et al. (2015) © John Wiley and Sons.
Figure 2. A gene‐for‐gene interaction illustrated by barley powdery mildew. The plant has a resistance (RES) gene which is effective only against parasites with an avirulence (AVR) gene (meaning that the parasite cannot cause disease on a host plant with the corresponding RES gene). If the plant has the susceptibility allele (res) of the resistance gene, it cannot recognise the parasite, whether it is avirulent or virulent, and if the parasite has the virulence allele (avr) of the avirulence gene, it cannot be detected by the host. In either case, the host's resistance mechanism fails to detect parasite avirulence and induce effective defences, which results in the plant becoming diseased.
Figure 3. Natural selection in a coevolving host–parasite interaction.
Figure 4. Dynamics of gene‐for‐gene coevolution. (a) A simple model, lacking direct frequency‐dependent selection, in which the graph of allele frequencies spirals outwards from an unstable equilibrium point. (b) A model in which direct frequency‐dependent selection is generated by disease being polycyclic; the graph of allele frequencies spirals inwards towards a stable equilibrium.
Figure 5. Forces acting on frequencies of resistance and virulence. An increased cost of resistance reduces the frequency of resistance, which reduces selection for virulence. The increased frequency of virulence reduces selection against resistance, so raising the frequency of resistance to its original value; the net outcome is a reduced frequency of virulence but no change in that of resistance. An increased cost of virulence reduces the frequency of virulence, which increases selection for resistance. The increased frequency of resistance increases selection for virulence, so raising the frequency of virulence to its original level; the net outcome is a higher frequency of resistance but no change in that of virulence.
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How to Cite close
Bruns, Emme(Feb 2016) Fitness Costs of Plant Disease Resistance. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020094.pub2]