Simultaneous evolution of host resistance and tolerance to parasitism

Abstract

Tolerance and resistance are two modes of defence mechanisms used by hosts when faced with parasites. Here, we assume tolerance reduces infection‐induced mortality rate and resistance reduces the susceptibility of getting infected. Importantly, a negative association between these two strategies has often been found experimentally. We study the simultaneous evolution of resistance and tolerance in a host population where they are related by such a trade‐off. Using evolutionary invasion theory, we examine the patterns of optimal investment in each defence strategy, under different ecological scenarios. Our focus is on predicting which of the two strategies is favoured under various epidemiological and ecological conditions. Our key findings surround the impact of recovery and sterility of infected hosts. As the rate at which infected hosts recover from the infection, that is the recovery rate increases, the investment in tolerance increases (resistance decreases) when infected hosts are sterile, but this pattern reverses when infected hosts can reproduce. We further found that a change in the parameter determining the intraspecies competition for resources leading to a reduction in birth rate, that is the crowding factor affects investments in tolerance and resistance only when infected hosts can reproduce. These results emphasize the role of fecundity in driving the evolutionary dynamics of a host. We also find that disease prevalence can increase or decrease depending on whether or not the host evolves: prevalence is highest at low recovery rates when the host does not evolve, but the feedback of a change in tolerance and resistance reverses this pattern, leading to lower prevalence at low recovery rates as host evolves.

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

“…Alternatively, hosts can increase their tolerance (i.e. limit the damage caused by a parasite/ virulence without affecting parasite fitness) by modifying fitness-related lifehistory traits [5][6][7]. Therefore, the evolution of both parasite resistance and parasite tolerance can influence population dynamics and parasite virulence, which poses an important challenge for epidemiological theory [8].…”

A sterility–mortality tolerance trade-off leads to within-population variation in host tolerance

“…The allocation to different tolerance mechanisms of the host depends upon the cost and how virulent/deadly the parasite is. For instance, when resistance (via reduced transmission) is traded-off with mortality tolerance, hosts infected with low virulent parasites experience selection for greater mortality tolerance than those infected by highly virulent parasites (Singh and Best, 2021). Similarly, mortality tolerance evolves in an experimental system with a ‘protected’ treatment in which virulence is low, whereas fecundity tolerance evolves in an unprotected treatment in which virulence is high (Rafaluk-Mohr et al, 2022).…”

“…The theoretical literature is largely based on the assumption that evolving defense is costly, suggesting trade-offs between defence strategies and other host fitness attributes (Boots and Haraguchi, 1999; Restif and Koella, 2003, 2004; Donnelly et al, 2015). Nonetheless, there is evidence of trade-offs between mechanisms of resistance and tolerance as well (Fineblum and Rausher, 1995; Pilson, 2000; Agrawal et al, 2004; Råberg et al, 2007; Baucom and Mauricio, 2008; Mikaberidze and Mc-Donald, 2020), but there has been a less theoretical investigation of such a scenario (Restif and Koella, 2004; Best et al, 2008, 2017; Singh and Best, 2021). Investment in sterility tolerance has previously been assumed to be bought at the cost of host characteristics such as increased natural death rate (Best et al, 2008, 2010a) or reduced intrinsic birth rate (Restif and Koella, 2004).…”

Evolutionary consequences of vector-borne transmission: how using vectors shapes host, vector and pathogen evolution

“…host capability to limit pathogen proliferation) or tolerance (i.e. host capability to reduce pathogenic effects of infection without controlling pathogen load/burden) depending on the cost of infection (Singh and Best, 2021 ). Indeed, introduction of the avian malaria parasite Plasmodium relictum has seemingly driven evolution of the Hawaiian honeycreeper amakihi Chlorodrepanis virens by selecting resistant/tolerant populations due to the strong selective pressure exerted by the parasite (Atkinson et al ., 2013 ).…”