High parasite diversity accelerates host adaptation and diversification

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Science  25 May 2018:
Vol. 360, Issue 6391, pp. 907-911
DOI: 10.1126/science.aam9974
  • 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-, medium-, and low-diversity populations alongside the parasite-free control. All plotted points show the mean population density ± SE. Bacterial populations challenged with phage rapidly recovered their density. We did not observe cyclical oscillations in host and parasite densities. CFU, colony-forming units; PFU, plaque-forming units. (B and C) To directly test for coevolution, we used 13,500 time-shift assays to measure changes in phage infectivity and bacterial resistance to phage. Lower levels of parasite infectivity (B) and higher levels of host resistance (C) evolved with increasing parasite diversity (F2,85 = 9.7, P < 0.001). Furthermore, hosts were more susceptible to parasites from the future than to contemporary parasites, and they were most resistant to parasites from the past. Likewise, future parasites were more infective than past or contemporary parasites (F2,13044 = 1766.21, P < 0.0001). Error bars show 1 SE.

  • Fig. 2 Parasite diversity accelerates host evolution.

    (A) Host allele frequencies after 10 days of coevolution with the high-, medium-, and low-parasite-diversity treatments were used to calculate pairwise Euclidean distances between the ancestral sequence (ANC) and each coevolved population. Increasing parasite diversity accelerated the rate of host evolution. (B) The genetic distances between coevolved populations were ordinated by nonmetric multidimensional scaling (MDS1 and MDS2). 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 is 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 the observed frequency (%) on day 5 (x axis). We found evidence for negative frequency-dependent selection on host alleles under low and medium parasite diversity, but not at high parasite diversity. The string of points forming a straight downward slope from zero in all three panels represents 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 for the high-, medium-, and low-parasite-diversity treatments and the parasite-free control. Each plotted point in the panel represents a single SNP, and host genes that are known parasite targets, including genes involved in LPS biosynthesis, type IV pilus biosynthesis, and the Ton-B–dependent receptor, are shown in italics. (B) We used a conservative FST cutoff to identify selective sweeps of SNPs per host population (± SE), and we found that increasing parasite diversity increased the rate of fixation of SNPs (χ2 = 20, df = 3, P < 0.001).

Supplementary Materials

  • High parasite diversity accelerates host adaptation and diversification

    A. Betts, C. Gray, M. Zelek, R. C. MacLean, K. C. King

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