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Coevolution in multidimensional trait space favours escape from parasites and pathogens

Abstract

Almost all species are subject to continuous attack by parasites and pathogens. Because parasites and pathogens tend to have shorter generation times1,2 and often experience stronger selection due to interaction than their victims do3,4, it is frequently argued that they should evolve more rapidly and thus maintain an advantage in the evolutionary race between defence and counter-defence1,5. This prediction generates an apparent paradox: how do victim species survive and even thrive in the face of a continuous onslaught of more rapidly evolving enemies5? One potential explanation is that defence is physiologically, mechanically or behaviourally easier than attack, so that evolution is less constrained for victims than for parasites or pathogens6. Another possible explanation is that parasites and pathogens have enemies themselves and that victim species persist because parasites and pathogens are regulated from the top down and thus generally have only modest demographic impacts on victim populations7,8. Here we explore a third possibility: that victim species are not as evolutionarily impotent as conventional wisdom holds, but instead have unique evolutionary advantages that help to level the playing field. We use quantitative genetic analysis and individual-based simulations to show that victims can achieve such an advantage when coevolution involves multiple traits in both the host and the parasite.

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Figure 1: Percentage victim wins as a function of the number of traits n and the mean magnitude of correlations between traits.
Figure 2: Interaction probabilities and population densities in representative numerical simulations.

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Acknowledgements

We thank A. R. Ives and F. Débarre for comments. R.T.G. and D.C.J. are postdoctoral fellows at the National Institute for Mathematical and Biological Synthesis (NIMBioS). NIMBioS is sponsored by the National Science Foundation (NSF), the US Department of Homeland Security and the US Department of Agriculture through NSF award no. EF-0832858, with support from The University of Tennessee, Knoxville. Additional support for this research was provided by NSF grants DMS 0540392 and DEB 1118947 to S.L.N.

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R.T.G. and S.L.N. conceived the study and derived the analytical results. R.T.G. coded and ran numerical simulations and analysed output data. R.T.G. and D.C.J. derived proofs 1–3. R.T.G. and S.L.N. prepared the manuscript.

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Correspondence to R. Tucker Gilman.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary References, Supplementary Data 1-3, Supplementary Box 1, Supplementary Tables 1-6 and Supplementary Figures 1-5. (PDF 1956 kb)

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Gilman, R., Nuismer, S. & Jhwueng, DC. Coevolution in multidimensional trait space favours escape from parasites and pathogens. Nature 483, 328–330 (2012). https://doi.org/10.1038/nature10853

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