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.