A paradox of parasite resistance: Disease-driven trophic cascades increase the cost of resistance, selecting for lower resistance with parasites than without them

Abstract

Most evolutionary theory predicts that, during epidemics, hosts will evolve higher resistance to parasites that kill them. Here, we provide an alternative to that typical expectation, with an explanation centered on resource feedbacks. When resistance is costly, hosts evolve decreasing resistance without parasites, as expected. But with parasites, hosts can evolve lower resistance than they would in the absence of parasites. This outcome arises in an eco-evolutionary model when four conditions are met: first, resistance has a fecundity cost (here, via decreased foraging/exposure rate); second, resources increase during epidemics via trophic cascades; third, increased resources magnify the benefit of maintaining a fast foraging rate, thereby magnifying the cost of evolving a slower foraging/exposure rate (i.e., resistance); fourth, that amplification of the cost outweighs the benefit of resistance. When these conditions are met, hosts evolve lower resistance than without parasites. This phenomenon was previously observed in a mesocosm experiment with fungal parasites, zooplankton hosts, and algal resources. Re-analyzing this experiment produced evidence for our model’s mechanism. Thus, both model and experiment indicate that, via resource feedbacks, parasites can counterintuitively select against resistance.

Host genetic variation in feeding rate mediates a fecundity cost of parasite resistance in aDaphnia-parasite system

“…However, in environments where environmentally-transmitted parasites are either common or virulent, rapid feeders could pay a fitness cost in that they are more likely to encounter infectious parasite transmission stages and suffer the fitness implications of disease (Auld et al, 2013). Theory tells us that this simple trade-off tell us about the relative strength of competition and parasitism as ecological forces of selection, and could potentially explain the persistence of parasite-susceptible genotypes (Hall et al, 2010; Walsman et al, 2022); indeed, when competition is particularly strong, rapid feeding and higher susceptibility can be favoured by selection even when parasites are prevalent.…”

“…and references within). Moreover, in systems where infection induced anorexia occurs, an increase in parasite prevalence can result in greater food availability for the uninfected fraction of the host population, thus reducing intra-specific competition and potentially mitigating any cost of resistance (Walsman et al, 2022).…”