Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution1,2. However, direct empirical evidence of long-term host–parasite coevolution, in particular ‘Red Queen’ dynamics—in which antagonistic biotic interactions such as host–parasite interactions can lead to reciprocal evolutionary dynamics—is rare3,4,5, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process6. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host–parasite system, corroborated these experimental results. In line with the idea of continuing host–parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.
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We thank R. L. Burks, B. Jansen, T. Huyse, T. J. Little, J. Mergeay, D. J. Mikolajewski, R. Ortells, F. Van de Meutter, J. Vanoverbeke and G. Verbeke for discussion and advice; J. Vandekerkhove, D. Verreydt, H. Michels and A. Wollebrants for technical help; and S. Sweizig for linguistic corrections. We acknowledge constructive comments by A. Read and Y. Michalakis. This research was supported by grants from the KULeuven Research Fund to E.D., the Fonds voor Wetenschappelijk Onderzoek – Vlaanderen (F.W.O) to E.D. and J.A.M.R., the KULeuven Research Fund to L.D.M., INRA and the Swiss Nationalfonds to S.G., and the Swiss Nationalfonds to D.E.
The Supplementary Information contains five parts: SI1 shows a figure on the dormant egg profile in the sediment cores; SI2 explains the clone depth x time shift interaction in the logistic regression of Table 1; SI3 gives information on the genetic continuity of the host population based on neutral markers; SI4 describes the coevolutionary model that we designed to capture our experimental study and study organism with four additional figures. SI5 gives additional references referred to in the Supplementary Information.
About this article
Nature Reviews Immunology (2017)