Demographic fluctuations and selection during host-parasite coevolution interactively increase genetic diversity.

Host-parasite interactions can cause strong demographic fluctuations accompanied by selective sweeps of resistance/infectivity alleles. Both demographic bottlenecks and frequent sweeps are expected to reduce the amount of segregating genetic variation and therefore might constrain adaptation during coevolution. Recent studies, however, suggest that the interaction of demographic and selective processes is a key component of coevolutionary dynamics and may rather positively affect levels of genetic diversity available for adaptation. Here, we provide direct experimental testing of this hypothesis by disentangling the effect of demography, selection, and of their interaction in an experimental host-parasite system. We grew 12 populations of a unicellular, asexually reproducing algae (Chlorella variabilis) that experienced either growth followed by constant population sizes (3 populations), demographic fluctuations (3 populations), selection induced by exposure to a virus (3 populations), or demographic fluctuations together with virus-induced selection (3 populations). After 50 days (approximately 50 generations), we conducted whole-genome sequencing of each algal host population. We observed more genetic diversity in populations that jointly experienced selection and demographic fluctuations than in populations where these processes were experimentally separated. In addition, in those 3 populations that jointly experienced selection and demographic fluctuations, experimentally measured diversity exceeds expected values of diversity that account for the cultures' population sizes. Our results suggest that eco-evolutionary feedbacks can positively affect genetic diversity and provide the necessary empirical measures to guide further improvements of theoretical models of adaptation during host-parasite coevolution

High parasite diversity maintained after an alga-virus coevolutionary arms race.

Arms race dynamics are a common outcome of host-parasite coevolution. While they can theoretically be maintained indefinitely, realistic arms races are expected to be finite. Once an arms race has ended, for example due to the evolution of a generalist resistant host, the system may transition into coevolutionary dynamics that favor long-term diversity. In microbial experiments, host-parasite arms races often transition into a stable coexistence of generalist resistant hosts, (semi-)susceptible hosts, and parasites. While long-term host diversity is implicit in these cases, parasite diversity is usually overlooked. In this study, we examined parasite diversity after the end of an experimental arms race between a unicellular alga (Chlorella variabilis) and its lytic virus (PBCV-1). First, we isolated virus genotypes from multiple time points from two replicate microcosms. A time-shift experiment confirmed that the virus isolates had escalating host ranges, i.e. that the arms races had occurred. We then examined the phenotypic and genetic diversity of virus isolates from the post-arms race phase. Post-arms race virus isolates had diverse host ranges, survival probabilities, and growth rates; they also clustered into distinct genetic groups. Importantly, host range diversity was maintained throughout the post-arms race phase, and the frequency of host range phenotypes fluctuated over time. We hypothesize that this dynamic polymorphism was maintained by a combination of fluctuating selection and demographic stochasticity. Together with previous work in prokaryotic systems, our results link experimental observations of arms races to natural observations of long-term host and parasite diversity

Correlations between residuals of morphological traits and residuals of squared maximum flow speed resistance.

<p>Correlations between residuals of morphological traits and residuals of squared maximum flow speed resistance.</p

Crab and wave ecotype <i>L</i>. <i>saxatilis</i> showing measurements of the shell.

<p>A) Typical “crab” ecotype with large size, thick shell, wide aperture, and an elongated spire, sampled at left (boulder) end of the transect shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0186901#pone.0186901.g002" target="_blank">Fig 2</a>. B) Typical “wave” ecotype with small size, thin shell, wide aperture and compressed spire, sampled ~10 m before the right (cliff) end of the transect in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0186901#pone.0186901.g002" target="_blank">Fig 2</a>). C) Shell measurements (aperture view) used in this study: Outer aperture area (OA, colored orange), inner aperture area (IA, colored yellow), Length 1 (L₁), Width 1 (W₁), Length 2 (L₂), Width 2 (W₂). D) Projection of the shell area (SA, colored gray) from the spire view.</p

Variation in morphology along the transect.

<p>Shell shapes 1 and 2 (S1 and S2, as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0186901#pone.0186901.g001" target="_blank">Fig 1</a>) estimate shell globosity and lateral compression, respectively, and foot area (FA), outer and inner-aperture areas (OA, IA, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0186901#pone.0186901.g001" target="_blank">Fig 1</a>) were scaled on the shell area (SA) to represent relative areas (RFA, ROA and RIA, respectively). Lines are the best fitting sigmoid functions describing the clines in the traits, with y values on the left of the graph. S1 filled purple squares, S2 empty brown circles, RFA filled red circles, ROA empty green squares, RIA empty black diamond. The best fitting cline for the squared flow resistance (SFR) is plotted as a bold black curve, with y values on the right of the graph. A black arrow marks the position of the transition from boulder to cliff habitat and a green arrow indicates the disappearance of <i>Fucus</i> sp.</p

Resistance to water speed in snails reared in a common garden.

<p>Number of snails that resisted various maximum water speeds (free stream velocity). Note that the x-axis is not a linear scale. A) Ten months old adults born and raised in the laboratory from parents sampled at each end of a crab-wave transect (island of Ramsökalv). B) Two week old juveniles born and raised in the laboratory from parents sampled at each end of a crab-wave transect (island of Saltö).</p