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 favour 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 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.

Demographic fluctuations and selection during host-parasite co-evolution 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 co-evolution. Recent studies, however, suggest that the interaction of demographic and selective processes is a key component of co-evolutionary 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 effects of demography, selection and 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 (three populations), demographic fluctuations (three populations), selection induced by exposure to a virus (three populations), or demographic fluctuations together with virus-induced selection (three populations). After 50 days (~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 three 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 co-evolution.

Adaptation to dislodgement risk on wave-swept rocky shores in the snail Littorina saxatilis.

The periwinkle Littorina saxatilis has repeatedly evolved both a small, fragile and globose "wave ecotype" confined to wave-swept shores and a large, robust and elongated "crab ecotype" found in nearby crab-rich but less-exposed shores. This phenotypic divergence is assumed to reflect, in some part, local adaptation to wave exposure, but this hypothesis has received incomplete experimental testing. Here, we report a test of the prediction that the wave ecotype has a higher capacity to resist water flow than the crab ecotype. We sampled snails along a crab-wave transect and measured their resistance to dislodgement in a high-speed water flume with water speeds that match those of breaking waves in a range of relevant field conditions. Snails from the wave environment were consistently more resistant to water flow than snails from the crab environment and high resistance was positively correlated with the surface area of the foot and the area of the outer aperture contour both relative to shell size, and to the extent of lateral shell compression. In a separate experiment, we found that snails raised in still water in a common garden showed higher resistance to water flow if originating from a wave environment than from a crab environment, and this was true both at juvenile (2 weeks) and adult (10 months) developmental stages. This result suggests genetic control of a distinct "wave adapted" phenotype, likely to be maintained under strong divergent selection between the two adjacent habitats.