Immunity in a variable world

Abstract

Immune function is likely to be a critical determinant of an organism's fitness, yet most natural animal and plant populations exhibit tremendous genetic variation for immune traits. Accumulating evidence suggests that environmental heterogeneity may retard the long-term efficiency of natural selection and even maintain polymorphism, provided alternative host genotypes are favoured under different environmental conditions. 'Environment' in this context refers to abiotic factors such as ambient temperature or availability of nutrient resources, genetic diversity of pathogens or competing physiological demands on the host. These factors are generally controlled in laboratory experiments measuring immune performance, but variation in them is likely to be very important in the evolution of resistance to infection. Here, we review some of the literature emphasizing the complexity of natural selection on immunity. Our aim is to describe how environmental and genetic heterogeneities, often excluded from experimentation as 'noise', may determine the evolutionary potential of populations or the potential for interacting species to coevolve.

Figure 1

G×E and local adaptation can be illustrated by imagining two environments (A and B) and one gene with two alleles (symbolized by circles and diamonds), each affecting the same trait. (a) G×E interactions maintain polymorphism when one allele gives the highest fitness in environment A, but the other allele is fitter in environment B. G×E refers to the general case where environments may vary in time or space, while local adaptation refers to the specific case where the environments are different locales. (b) The maintenance of polymorphism by G×E can occur in two ways. (i) In the first example, the phenotype produced by each allele has environment-specific values and the phenotype is positively correlated with fitness. In this case, alternative genotypes yield higher fitness in the two environments. (ii) The phenotype produced by an allele may be constant across environments, but different phenotypes are favoured in different environments, such that the correlation between phenotype and fitness changes from negative to positive depending on the environment. In this case, there is no G×E for the direct phenotype measured, but there is G×E for fitness. This latter scenario is reasonable, as many traits will have varied relationships with fitness. For example, small size might be favoured in some environments, but large size in others. (c) Pleiotropy occurs when one gene with two alleles codes for two traits (X and Y). (ii) Both traits may be under selection for larger values, but one of the two alleles codes for high phenotypic values of trait X and low values of trait Y, while the other allelic form of the gene codes for high values of trait Y. (i) Under this scenario, the overall fitness conferred by each allele is identical due to the balanced effects on both traits, so natural selection does not eliminate either of them.