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Antagonistic coevolution accelerates molecular evolution

Nature volume 464, pages 275–278 (2010)Cite this article

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Abstract

The Red Queen hypothesis proposes that coevolution of interacting species (such as hosts and parasites) should drive molecular evolution through continual natural selection for adaptation and counter-adaptation1,2,3. Although the divergence observed at some host-resistance4,5,6 and parasite-infectivity7,8,9 genes is consistent with this, the long time periods typically required to study coevolution have so far prevented any direct empirical test. Here we show, using experimental populations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage Φ2 (refs 10, 11), that the rate of molecular evolution in the phage was far higher when both bacterium and phage coevolved with each other than when phage evolved against a constant host genotype. Coevolution also resulted in far greater genetic divergence between replicate populations, which was correlated with the range of hosts that coevolved phage were able to infect. Consistent with this, the most rapidly evolving phage genes under coevolution were those involved in host infection. These results demonstrate, at both the genomic and phenotypic level, that antagonistic coevolution is a cause of rapid and divergent evolution, and is likely to be a major driver of evolutionary change within species.

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Figure 1: Genetic and phenotypic responses to selection.
Figure 2: Patterns of molecular evolution in the Φ2 genome.

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EMBL/GenBank/DDBJ

Data deposits

The ancestral genome sequence of phage Φ2 has been submitted to the EMBL Nucleotide Sequence Database under accession number FN594518.

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Acknowledgements

We are grateful to M. Begon and G. Hurst for comments on previous drafts of this manuscript. We acknowledge funding from the Natural Environment Research Council, the Wellcome Trust, the Leverhulme Trust and the European Research Council. We are grateful for technical assistance from staff at the Centre for Genomic Research, University of Liverpool.

Author Contributions M.A.B. and S.P. conceived and designed the study; T.V. performed selection experiments, infectivity assays and prepared samples for population genomic sequencing; B.L. and M.A.B. performed further assays; R.B. prepared samples for ancestral genome sequencing; N.R.T., M.Q., F.S. and D.W. performed ancestral genome sequencing and assembly; A.J.S. and N.R.T. performed genome annotation; S.P., T.V. and M.A.B. analysed the data; M.A.B., S.P., A.B., A.J.S. and N.R.T. wrote the manuscript; T.V. and N.H. commented on the manuscript; M.A.B., A.F. and S.P. supervised the research; S.P., N.H., A.B. and M.A.B. obtained funding.

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Author notes

  1. Steve Paterson, Tom Vogwill and Michael A. Brockhurst: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Biological Sciences, Biosciences Building, University of Liverpool, Crown Street, Liverpool L69 7ZB, UK ,

    Steve Paterson, Tom Vogwill, Ben Libberton, Andrew Fenton, Neil Hall & Michael A. Brockhurst

  2. Zoology Department, University of Oxford, South Parks Road, Oxford OX1 3PS, UK,

    Angus Buckling & Rebecca Benmayor

  3. SIMBIOS Centre, Level 5 Kydd Building, University of Abertay Dundee, Bell Street, Dundee DD1 1HG, UK ,

    Andrew J. Spiers

  4. Pathogen Genomics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK ,

    Nicholas R. Thomson, Mike Quail, Frances Smith & Danielle Walker

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  1. Steve Paterson
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Corresponding author

Correspondence to Michael A. Brockhurst.

Supplementary information

Supplementary Information

This file contains Supplementary Figures S1-S2 with Legends, Supplementary Table S1, a Supplementary Discussion and Supplementary References. (PDF 297 kb)

Supplementary Table 2

This table contains the genome annotation for phage Φ2, and the full gene-by-gene statistical analysis of the genome re-sequencing data. (XLS 75 kb)

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Paterson, S., Vogwill, T., Buckling, A. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010). https://doi.org/10.1038/nature08798

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