Host heterogeneity mitigates virulence evolution

Abstract

Parasites often infect genetically diverse host populations, and the evolutionary trajectories of parasite populations may be shaped by levels of host heterogeneity. Mixed genotype host populations, compared to homogeneous host populations, can reduce parasite prevalence and potentially reduce rates of parasite adaptation due to trade-offs associated with adapting to specific host genotypes. Here, we used experimental evolution to select for increased virulence in populations of the bacterial parasite Serratia marcescens exposed to either heterogeneous or homogeneous populations of Caenorhabditis elegans. We found that parasites exposed to heterogeneous host populations evolved significantly less virulence than parasites exposed to homogeneous host populations over several hundred bacterial generations. Thus, host heterogeneity impeded parasite adaptation to host populations. While we detected trade-offs in virulence evolution, parasite adaptation to two specific host genotypes also resulted in modestly increased virulence against the reciprocal host genotypes. These results suggest that parasite adaptation to heterogeneous host populations may be impeded by both trade-offs and a reduction in the efficacy of selection as different host genotypes exert different selective pressures on a parasite population.

Keywords: Caenorhabditis elegans; Serratia marcescens; host heterogeneity; monoculture; parasite evolution; virulence.

Figure 1.

(a,b) Mean change in host mortality rate relative to the ancestral parasites in C. elegans host strains CB4856 (a) and ewIR 68 (b). All experimental populations shared a common ancestor, and thus, any change from the ancestral data is indicative of relative virulence. Parasites were evolved in heterogeneous host populations, homogeneous host populations or in vitro (no hosts), and then tested for changes in virulence. The heterogeneous populations, from left to right, are 75–25, 50–50 and 25–75. Circles represent the mean change within each technical replicate (18–36 each). Bars represent ± s.e.m. (Online version in colour.)

Figure 2.

Each dot represents the treatment's average change in mortality rate of all populations and replicates relative to ancestral parasites. All experimental populations shared a common ancestor, and thus, any change from the ancestral data is indicative of relative virulence. The x-axis shows the type of host infected: either familiar to the parasite or novel. The p-value is based on a post-GLM Tukey contrast test between all familiar hosts (left panel) and all novel hosts (right panel) (χ² = 6.04, p = 0.01). In both cases, although all treatments had an increased mortality rate relative to the ancestor, novel hosts had a lower mortality rate than do the familiar hosts. Bars around mean represent s.e.m. (Online version in colour.)