Maximising fitness in the face of parasites: a review of host tolerance

Abstract

Tolerance, the ability of a host to limit the negative fitness effects of a given parasite load, is now recognised as an important host defence strategy in animals. Together with resistance, the ability of a host to limit parasite load, these two host strategies represent two disparate host responses to parasites, each with different predicted evolutionary consequences: resistance is predicted to reduce parasite prevalence, whereas tolerance could be neutral towards, or increase, parasite prevalence in a population. The distinction between these two strategies might have far-reaching epidemiological consequences. Classically, a reaction norm defines host tolerance because it depicts the change in host fitness as a function of parasite load, where a shallow negative slope indicates that host fitness slowly deteriorates as parasite load increases (i.e., high tolerance). Despite the fact that tolerance was only recently acknowledged to be an important component in an animal's immune repertoire, it is frequently referenced, so our aim is to emphasise the current advances on the topic. We begin by summarising the ways in which biologists measure the two components of tolerance, parasite load and fitness, as well as the ways in which the concept has been defined (i.e., point and range tolerance). It is common to test for variation in host tolerance according to intrinsic, innate factors, where variation exists among populations, genders or genotypes. Such variation in tolerance is pervasive across animal taxa, and we briefly review some of the mechanistic bases of variation that have recently begun to be explored. Three further novel advancements in the tolerance field are the appreciation of the role of extrinsic, environmental factors on tolerance, host tolerance in multi-host-parasite systems and individual-based approaches to tolerance measures. We explore these topics using recent examples and suggest some future perspectives. It is becoming increasingly clear that an appreciation of tolerance as a defence strategy can provide significant insights into how hosts coexist with parasites.

Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association

“…In global warming scenarios, increased host fitness costs due to predicted higher parasite life-cycle completion and dispersal rates [46], could be compensated for, at least to some extent by host tolerance. There is an increasing appreciation of the importance of abiotic factors on host tolerance [24]. Recently, it was described that Drosophila melanogaster infected with a fungus seek cooler temperatures, under which they were able to increase resistance to the fungal infection and increase their late life reproductive output [59].…”

“…Parasite weight was included as a continuous predictor variable in each model and all possible interactions were included up to three-way. A significant interaction between any of the factors and parasite weight would reveal that this factor affects host tolerance [19, 24]. Tolerance is illustrated as the slope of the relationship between host health or fecundity, and parasite weight, where steeper positive slopes indicate greater tolerance.…”

“…We considered including the quadratic term of parasite weight into our tolerance models to account for non-linear relationships [19–21, 24, 27, 57]. Only including the linear term for parasite weight plus all other factors and interactions up to three-way, meant testing the effects of 25 parameters in total.…”

“…better at minimising the negative fitness effect of an increasing infection intensity, than a population with a steeper negative slope [19, 20]. A number of studies have shown that hosts use tolerance to mitigate fitness losses during infections with microparasites [19, 21–24]. Given that macroparasites can also dramatically reduce host fitness [12, 25, 26], tolerance might be expected to be an important host strategy [27].…”

“…Both parameters are hypothesised to be affected by the growing S. solidus since the parasite drains substantial amounts of nutrients from its host [8, 10, 11]. Although local adaptation for resistance has been shown, evidence of local adaptation for tolerance has not been found to date [21, 22, 24]. In a mesocosm experiment, lake and stream stickleback ecotypes were similarly non-tolerant to an ectoparasite ( Gyrodactylus sp.…”