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.
Highlights
What Controls Virulence?Evolutionary biologists define the virulence of a parasite as the reduction in host fitness caused by infection
When this reduction in host fitness is due to an increased mortality rate, the consequences for parasite evolution are clear; host death means parasite death [1]
Virulence may be viewed as resulting from the density of parasites within a host (I) and the degree of damage caused by each parasite (a, the per-parasite virulence): Virulence~I a ð1Þ
Summary
Evolutionary biologists define the virulence of a parasite as the reduction in host fitness caused by infection. The study of host-controlled a has been described as the study of tolerance: the ability of hosts to limit the damage caused by a given parasite burden, which is essentially the ability to minimize per-parasite virulence It has been studied as a mean, i.e., where two genotypes carry the same parasite burden, but one genotype achieves higher fitness. If we are to draw general conclusions about tolerance evolution, we need to resolve when empirical studies of point tolerance (e.g., [19]) should be freely compared with studies of range tolerance (e.g., [14]), and when either can inform theory that uses yet other definitions (e.g., [33]; see [21]) Both in terms of measurement and the evolutionary inferences that are possible. Host–parasite coevolution is about two interacting organisms gaining fitness at each other’s expense, and a more holistic approach could unite a large range of perspectives on the evolutionary ecology of attack, defence, and commensalism
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