Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality

Abstract

Evolutionary diversification can occur in allopatry or sympatry, can be driven by selection or unselected, and can be phenotypically manifested immediately or remain latent until manifested in a newly encountered environment. Diversification of host-parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host-parasite interaction phenotypes to diversify latently during parasite-blind host evolution is rarely considered. Here, we use a social bacterium experimentally adapted to several environments in the absence of phage to analyse allopatric diversification of host quality-the degree to which a host population supports a viral epidemic. Phage-blind evolution reduced host quality overall, with some bacteria becoming completely resistant to growth suppression by phage. Selective-environment differences generated only mild divergence in host quality. However, selective environments nonetheless played a major role in shaping evolution by determining the degree of stochastic diversification among replicate populations within treatments. Ancestral motility genotype was also found to strongly shape patterns of latent host-quality evolution and diversification. These outcomes show that (i) adaptive landscapes can differ in how they constrain stochastic diversification of a latent phenotype and (ii) major effects of selection on biological diversification can be missed by focusing on trait means. Collectively, our findings suggest that latent-phenotype evolution should inform host-parasite evolution theory and that diversification should be conceived broadly to include latent phenotypes.

Keywords: adaptive landscape; bacteriophages; byproduct evolution; cryptic genetic variation; phenotypic plasticity; pleiotropy.

Figure 1.

Diversification of latent host quality during phage-blind evolution occurred predominantly within rather than between selective environments. Cross-replicate means of host-quality measurements (grey circles) for ancestors and all evolved populations (a) and evolved populations categorized by evolution environment (b) with corresponding overall category means (black circles) and 95% confidence intervals. HA and SA indicate hard and soft agar environments, respectively. Host quality is measured as Mx1 phage population size 24 h after initial infection of bacterial populations (log-transformed data). The dashed line corresponds to average phage population size after growth on the experimental ancestors GJV1 and GJV2. The asterisks indicate statistically significant differences: two-sample two-sided t-test ((a) ***p < 0.001) and the one pairwise comparison in which treatment means differ significantly ((b) post hoc Tukey test, mixed linear model, *p < 0.05).

Figure 2.

Selective environments differentially constrained stochastic diversification of host quality within treatments. (a) Within-treatment coefficients of variation (CVs) of phage population size 24 h post infection. Small and large circles represent within-replicate-assay CV estimates across evolved populations and cross-replicate-assay means for each treatment, respectively. HA and SA differentiate hard and soft agar environments, respectively. Error bars show 95% confidence intervals. For comparison, the dashed line indicates the between-treatment CV (i.e. the cross-replicate-assay average of the CV among host-quality means for each treatment). Grey shaded area is the corresponding 95% confidence interval. (b) Host quality of evolved populations from the least (upper panel) and most (lower panel) evolutionarily diversified treatments. Grey circles are the means across four biological replicates (open circles) and error bars represent 95% confidence intervals.

Figure 3.

Diversity of evolved bacterial resistance to growth suppression by phage. Growth of the ancestors and of MyxoEE-3 populations evolved on low-nutrient soft agar (P65-P72) in the presence (red) and absence (blue) of phage. Data points show optical density (OD_{595 nm}) measurements over time for four temporally separate biological replicates, trendlines track conditional mean values of locally weighted regressions and shaded areas represent 95% confidence intervals of the fit. The asterisks indicate significant differences to the ancestors (Dunnett test, mixed linear model, **p < 0.01 and ***p < 0.001).

Figure 4.

Ancestral motility genotype determined both degree of trait mean evolution and degree of stochastic diversification for host quality. Phage population size 24 h after infection of ancestors and evolved populations with both motility systems intact (A+S+) or lacking either system (A-S+ or A+S-). Each data point represents the mean of four biological replicates. Colours show the difference between evolved populations and their respective ancestors (open circles: non-significant difference, black circles: significant difference; Dunnett test, mixed linear model).