An experimental test of parasite adaptation to common versus rare host genotypes

Abstract

A core hypothesis in coevolutionary theory proposes that parasites adapt to specifically infect common host genotypes. Under this hypothesis, parasites function as agents of negative frequency-dependent selection, favouring rare host genotypes. This parasite-mediated advantage of rarity is key to the idea that parasites maintain genetic variation and select for outcrossing in host populations. Here, we report the results of an experimental test of parasite adaptation to common versus rare host genotypes. We selected the bacterial parasite Serratia marcescens to kill Caenorhabdiis elegans hosts in uneven mixtures of host genotypes. To examine the effect of commonness itself, independent of host identity, each of four host genotypes was represented as common or rare in experimental host mixtures. After experimental selection, we evaluated a parasite line's change in virulence—the selected fitness trait—on its rare and common host genotypes. Our results were consistent with a slight advantage for rare host genotypes: on average, parasites lost virulence against rare genotypes but not against common genotypes. The response varied substantially, however, with distinct patterns across host genotype mixtures. These findings support the potential for parasites to impose negative frequency-dependent selection, while emphasizing that the cost of being common may vary with host genotype.

Antagonistic Coevolution Limits the Range of Host Defense in C. elegans Populations

“…Specifically, the amount of evolutionary reciprocity within the interaction can influence the effective range of host defenses, with increased reciprocity resulting in more narrow ranges (Figures 2, 3). This aligns with research showing that parasites evolved with homogenous host populations exhibited more narrow host ranges (White et al, 2020;Gibson et al, 2020a;Gibson et al, 2020b). Therefore, host and parasite populations with an immediate evolutionary history of coevolution may often be constrained in genotypic space, pigeonholed by combinations of alleles that were previously advantageous but are contemporarily unfavorable.…”

The impact of host heterogeneity on pathogen evolution depends on spatial structure

“…Our results have implications for broader ecological and evolutionary theory on how specialization can support diversity. The fact that pathogens in our experiment can have (presumably) maladaptively high virulence on foreign hosts demonstrates that rare host genotypes may not always have a fitness advantage [65][66][67][68]. This has previously been considered in cases of species invasions (i.e.…”

“…A large portion of ecological and evolutionary theory on how host-parasite coevolution can result in biotic diversity depends on specialist interactions and assumes that pathogens have the highest exploitation rates on their familiar or locally common host so that rare hosts have a fitness advantage [6,15,79,80]. This is partially because most of these models focus only on the infectivity component of pathogen specialization and do not consider post-infection processes like replication and virulence where high levels might be expected to lower fitness [81].…”