Decomposing health: tolerance and resistance to parasites in animals

Abstract

Plant biologists have long recognized that host defence against parasites and pathogens can be divided into two conceptually different components: the ability to limit parasite burden (resistance) and the ability to limit the harm caused by a given burden (tolerance). Together these two components determine how well a host is protected against the effects of parasitism. This distinction is useful because it recognizes that hosts that are best at controlling parasite burdens are not necessarily the healthiest. Moreover, resistance and tolerance can be expected to have different effects on the epidemiology of infectious diseases and host-parasite coevolution. However, studies of defence in animals have to date focused on resistance, whereas the possibility of tolerance and its implications have been largely overlooked. The aim of our review is to (i) describe the statistical framework for analysis of tolerance developed in plant science and how this can be applied to animals, (ii) review evidence of genetic and environmental variation for tolerance in animals, and studies indicating which mechanisms could contribute to this variation, and (iii) outline avenues for future research on this topic.

Figure 1

Reaction norms for fitness of two host genotypes (A and B) across a parasite burden range. The dots represent individual hosts of genotype A (unfilled) or B (filled). (a) Host genotypes differ in tolerance; A is more tolerant. (b) Host genotypes differ in ‘general vigour’, but not in tolerance.

Figure 2

Inbred strains of laboratory mice differ in tolerance to the rodent malaria parasite P. chabaudi. (a) Tolerance measured as the slope of minimum red blood cell (RBC) density (log-transformed) against peak parasite density. (b) Tolerance measured as the slope of minimum weight (log-transformed) against peak parasite density. In the case of both minimum RBC density and weight, ANCOVAs revealed highly significant interactions between mouse strain and parasite density. The ranking of the slopes for minimum RBC density and weight is the same, indicating that the two forms of tolerance are positively correlated (r_s=1.0, p<0.05). From Råberg et al. (2007). Up triangles, DBA/1 mice; down triangles, NIH; circles, A/J; pluses, CBA; crosses, C57.

Figure 3

(a) Reaction norms of different host genotypes (A and B) differ in shape, that is, there is a statistical interaction between host genotype and the quadratic infection intensity term. In such cases, it may be difficult to rank the tolerance of different host types. For illustration purposes, we show an extreme example where one host genotype has a convex reaction norm while the other has a concave norm; more subtle differences are perhaps more likely in reality. (b) If the range of parasite burdens differs between host genotypes (A and B), and the overall reaction norm (dashed curve) is nonlinear, an analysis that only considers linear relationships may yield the incorrect conclusion that host genotypes vary in tolerance (in this case that B is more tolerant than A) (Tiffin & Inouye 2000).

Figure 4

Schematic of different types of costs of tolerance. (a) Tolerance is costly in the sense that a more tolerant genotype (A) has lower fitness at low or zero parasite burdens. (b) Tolerance is costly in the sense that a more tolerant genotype (A) has lower resistance.