High parasite diversity accelerates host adaptation and diversification

Abstract

Host-parasite species pairs are known to coevolve, but how multiple parasites coevolve with their host is unclear. By using experimental coevolution of a host bacterium and its viral parasites, we revealed that diverse parasite communities accelerated host evolution and altered coevolutionary dynamics to enhance host resistance and decrease parasite infectivity. Increases in parasite diversity drove shifts in the mode of selection from fluctuating (Red Queen) dynamics to predominately directional (arms race) dynamics. Arms race dynamics were characterized by selective sweeps of generalist resistance mutations in the genes for the host bacterium's cell surface lipopolysaccharide (a bacteriophage receptor), which caused faster molecular evolution within host populations and greater genetic divergence among populations. These results indicate that exposure to multiple parasites influences the rate and type of host-parasite coevolution.

Fig. 1. Ecological and Coevolutionary Dynamics of Host-Parasite Interactions.

(A) We tracked the population dynamics of hosts (solid lines) and parasites (dashed lines) for high (yellow), medium (blue) and low (black) diversity populations alongside the parasite free control (grey). All plotted points show the mean +/- standard error population density. Bacterial populations challenged with phage rapidly recovered their density. We did not observe cyclical oscillations in host and parasite densities. (B and C) To directly test for co-evolution, we used 13,500 time shift assays to measure changes in phage infectivity and bacterial resistance to phage. Lower levels or parasite infectivity (B) and higher levels of host resistance (C) evolve with increasing parasite diversity (F_2,85 =9.7, P < 0.001). Furthermore, hosts are more susceptible to parasites from their future than their contemporary parasites and they are most resistant to parasites from their past. Likewise future parasite are more infective than past or contemporary parasites (F_2,13044 =1766.21, P < 0.0001). Error bars show 1 standard error.

Fig. 2. Parasite diversity accelerates host evolution

(A) Host allele frequencies after 10 days of coevolution from the high (yellow), medium (blue) and low (black) parasite diversity treatments were used to calculate pairwise Euclidean distances between the ancestral sequence (grey) and each coevolved population. Increasing parasite diversity accelerated the rate of host evolution. (B) The genetic distances between coevolved populations were ordinated by non-metric multidimensional scaling. The ellipses represent a 95% confidence bubble around the means for the different treatments. We found evidence of divergence between populations within treatments (ANOSIM R = 0.11 P < 0.01), and the greatest within treatment diversification was observed in the high parasite diversity treatment.

Fig. 3

Red Queen coevolution more common in pairwise host-parasite interactions. We tested for Red Queen dynamics by regressing the change in host allele frequency from day 5 to day 10 (y-axis) with observed frequency on day 5 (x-axis). We found evidence for negative frequency dependent selection on host alleles under low (black) and medium (blue) parasite diversity, but not at high parasite diversity (yellow). The string of points forming a straight downward slope from zero in all three panels are alleles observed on day 5 that had subsequently decreased in frequency to below our ability to detect them at day 10.

Fig. 4. Parasite diversity leads to more Arms Race coevolutionary dynamics.

(A) To test for Arms Race Dynamics, we calculated FST for all host SNPs across the P. aeruginosa genome across the high (yellow), medium (blue) and low (black) parasite diversity treatments and the parasite free control (grey). Each plotted point in the panel represents a single SNP and host genes that are known parasite targets are shown in italics, including genes involved in LPS biosynthesis, Type IV pili biosynthesis, and the Ton-B dependent receptor. (B) We used a conservative FST cutoff to identify selective sweeps of SNPs per host population (+/- standard error), and we found that increasing parasite diversity increased the rate of fixation of SNPs (X²= 20, df = 3, P <0.001).