The Coevolution of Virulence: Tolerance in Perspective

Abstract

Coevolutionary interactions, such as those between host and parasite, predator and prey, or plant and pollinator, evolve subject to the genes of both interactors. It is clear, for example, that the evolution of pollination strategies can only be understood with knowledge of both the pollinator and the pollinated. Studies of the evolution of virulence, the reduction in host fitness due to infection, have nonetheless tended to focus on parasite evolution. Host-centric approaches have also been proposed—for example, under the rubric of “tolerance”, the ability of hosts to minimize virulence without necessarily minimizing parasite density. Within the tolerance framework, however, there is room for more comprehensive measures of host fitness traits, and for fuller consideration of the consequences of coevolution. For example, the evolution of tolerance can result in changed selection on parasite populations, which should provoke parasite evolution despite the fact that tolerance is not directly antagonistic to parasite fitness. As a result, consideration of the potential for parasite counter-adaptation to host tolerance—whether evolved or medially manipulated—is essential to the emergence of a cohesive theory of biotic partnerships and robust disease control strategies.

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

“…First, 'range tolerance' is defined as the slope of the relationship between a trait capturing host fitness (e.g. growth rate or survivorship) and parasite burden [7,11]. The use of 'range tolerance' is particularly appropriate when the fitness proxy examined is affected by factors other than parasite burden [3].…”

“…Unlike resistance, host tolerance does not limit infection, but reduces or compensates parasite-induced damages through reduced immunopathology, increased wound repair mechanisms and a greater resilience to tissue injuries [3][4][5][6]. The expression of both defence responses results from the interactions between the host and parasite genomes and the environment [7,8].…”

“…By contrast, because tolerance does not reduce parasite fitness, its evolution is expected to result in a positive feedback whereby parasite infection selects for tolerant hosts, which in turn increases parasite prevalence. As a result, most theoretical models predict the maintenance of genetic variation in resistance but the fixation of tolerance along the course of host-parasite coevolution [2,7,9] (but see [10]). …”

An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow

“…Tolerance in its restricted meaning (i.e., mechanisms that reduce the host fitness costs of infection, Roy and Kirchner 2000;Simms 2000) has been the subject of a growing interest as a potentially more stable defense component than true resistance since it was considered to place little or no selective pressure on the pathogen (Schafer 1971;Ney et al 2013;Ennos 2015). Tolerance, however, is in nearly all cases expected to impose positive feedbacks leading to more prevalent and/or more virulent pathogens (Little et al 2010;Miller, White, and Boots 2006;Roy and Kirchner 2000). Therefore, introducing tolerant hosts to a population, through breeding for example, has the potential to increase pathogen pressure overall (Restif and Koella 2004).…”

Ecology and Epidemiology of Nematode Infection in Japanese Macaques:

“…And of course the flip side of parasite resistance, the ability to limit infection, is parasite tolerance, which instead reflects an organism' s ability to reduce the harm caused by parasites, though the latter has received considerably less attention (Råberg et al 2009;Little et al 2010;Ayres & Schneider 2012). There are few empirical studies in animals that have investigated variation in tolerance (Leuciscus leuciscus: Blanchet et al 2010;Bufo americanus, Rana clamitans: Rohr et al 2010;Danaus plexippus: Lefèvre et al 2011), but the concept, at least, is relatively simple: tolerance represents a change in reactivity to some threat such as a parasite or other invading organism, and can be examined in a dose-response framework.…”