Antagonistic coevolution accelerates molecular evolution

Steve Paterson, Tom Vogwill, Angus Buckling, Rebecca Benmayor, Andrew J. Spiers, Nicholas R. Thomson, Mike Quail, Frances Smith, Danielle Walker, Ben Libberton, Andrew Fenton, Neil Hall, Michael A. Brockhurst

Research output: Contribution to journalLetter

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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-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity 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, 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.
Original languageEnglish
Pages (from-to)275-278
Number of pages3
JournalNature
Volume464
DOIs
StatePublished - 11 Mar 2010

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Molecular Evolution
Bacteriophages
Parasites
Bacteria
Genes
Pseudomonas fluorescens
Host Specificity
Genotype
Infection

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Paterson, S., Vogwill, T., Buckling, A., Benmayor, R., Spiers, A. J., Thomson, N. R., ... Brockhurst, M. A. (2010). Antagonistic coevolution accelerates molecular evolution. Nature, 464, 275-278. DOI: 10.1038/nature08798

Paterson, Steve; Vogwill, Tom; Buckling, Angus; Benmayor, Rebecca; Spiers, Andrew J.; Thomson, Nicholas R.; Quail, Mike; Smith, Frances; Walker, Danielle; Libberton, Ben; Fenton, Andrew; Hall, Neil; Brockhurst, Michael A. / Antagonistic coevolution accelerates molecular evolution.

In: Nature, Vol. 464, 11.03.2010, p. 275-278.

Research output: Contribution to journalLetter

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title = "Antagonistic coevolution accelerates molecular evolution",
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-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity 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, 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.",
author = "Steve Paterson and Tom Vogwill and Angus Buckling and Rebecca Benmayor and Spiers, {Andrew J.} and Thomson, {Nicholas R.} and Mike Quail and Frances Smith and Danielle Walker and Ben Libberton and Andrew Fenton and Neil Hall and Brockhurst, {Michael A.}",
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Paterson, S, Vogwill, T, Buckling, A, Benmayor, R, Spiers, AJ, Thomson, NR, Quail, M, Smith, F, Walker, D, Libberton, B, Fenton, A, Hall, N & Brockhurst, MA 2010, 'Antagonistic coevolution accelerates molecular evolution' Nature, vol 464, pp. 275-278. DOI: 10.1038/nature08798

Antagonistic coevolution accelerates molecular evolution. / Paterson, Steve; Vogwill, Tom; Buckling, Angus; Benmayor, Rebecca; Spiers, Andrew J.; Thomson, Nicholas R.; Quail, Mike; Smith, Frances; Walker, Danielle; Libberton, Ben; Fenton, Andrew; Hall, Neil; Brockhurst, Michael A.

In: Nature, Vol. 464, 11.03.2010, p. 275-278.

Research output: Contribution to journalLetter

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T1 - Antagonistic coevolution accelerates molecular evolution

AU - Paterson,Steve

AU - Vogwill,Tom

AU - Buckling,Angus

AU - Benmayor,Rebecca

AU - Spiers,Andrew J.

AU - Thomson,Nicholas R.

AU - Quail,Mike

AU - Smith,Frances

AU - Walker,Danielle

AU - Libberton,Ben

AU - Fenton,Andrew

AU - Hall,Neil

AU - Brockhurst,Michael A.

PY - 2010/3/11

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N2 - 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-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity 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, 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.

AB - 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-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity 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, 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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Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR et al. Antagonistic coevolution accelerates molecular evolution. Nature. 2010 Mar 11;464:275-278. Available from, DOI: 10.1038/nature08798