The Evolution of Parasites in Response to Tolerance in Their Hosts: The Good, the Bad, and Apparent Commensalism

Abstract

Tolerance to parasites reduces the harm that infection causes the host (virulence). Here we investigate the evolution of parasites in response to host tolerance. We show that parasites may evolve either higher or lower within-host growth rates depending on the nature of the tolerance mechanism. If tolerance reduces virulence by a constant factor, the parasite is always selected to increase its growth rate. Alternatively, if tolerance reduces virulence in a nonlinear manner such that it is less effective at reducing the damage caused by higher growth rates, this may select for faster or slower replicating parasites. If the host is able to completely tolerate pathogen damage up to a certain replication rate, this may result in apparent commensalism, whereby infection causes no apparent virulence but the original evolution of tolerance has been costly. Tolerance tends to increase disease prevalence and may therefore lead to more, rather than less, disease-induced mortality. If the parasite is selected, even a highly efficient tolerance mechanism may result in more individuals in total dying from disease. However, the evolution of tolerance often, although not always, reduces the individual risk of dying from infection.

Decomposing health: tolerance and resistance to parasites in animals

“…If tolerance is heritable, what prevents hosts from evolving perfect tolerance (so that bZ0 in equation (2.1))? One factor that could constrain the evolution of tolerance is if it has not only fitness benefits, but also costs to the host (Strauss & Agrawal 1999;Stowe et al 2000;Fornoni et al 2004;Miller et al 2006). In principle, such costs could come about in several different ways.…”

“…One could imagine that evolution of tolerance may impose selection on the parasite after all, because tolerance reduces the chances a virulent strain will truncate its infectious period by killing its host. Assuming virulence is correlated with transmission rate, which it often is (Mackinnon et al 2008), tolerance should therefore favour more virulent parasites (Miller et al 2006). More virulent parasites could, in turn, select for further increases in tolerance.…”

The role of ecological feedbacks in the evolution of host defence: what does theory tell us?

“…They show that resistance is maximal at an intermediate parasite replication rate, as is tolerance (in fact, there is no investment in tolerance if the parasite has either too low or too high a replication rate). Miller et al (2006) investigated the evolution of parasites once host tolerance had become fixed in the population. They also assumed that the virulence experienced by an infected host is determined by both the host and the parasite.…”

Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species

“…Host defence strategies against parasites, such as tolerance and resistance, are often condition‐dependent and regulated by resource availability (Cotter, Simpson, Raubenheimer, & Wilson, ; Howick & Lazzaro, ; Knutie, Wilkinson, Wu, Ortega, & Rohr, ; Lee, Cory, Wilson, Raubenheimer, & Simpson, ; Sternberg et al, ). Tolerance mechanisms, such as tissue repair or compensation for energy loss, reduce the damage that parasites cause without reducing parasite fitness (Medzhitov, Schneider, & Soares, ; Miller, White, & Boots, ; Råberg, Sim, & Read, ; Read, Graham, & Råberg, ). For example, avian parents from parasite‐infested nests reduce the cost of parasitism by feeding their offspring more than parents from non‐parasitized nests (Christe, Richner, & Oppliger, ; Knutie et al, ; Tripet & Richner, ).…”