Abstract
Adaptation is conventionally regarded as occurring at the level of the individual organism, where it functions to maximize the individual’s inclusive fitness1,2,3. However, it has recently been argued that empirical studies on the evolution of parasite virulence in spatial populations show otherwise4,5,6,7. In particular, it has been claimed that the evolution of lower virulence in response to limited parasite dispersal8,9 provides proof of Wynne-Edwards’s10 idea of adaptation at the group level. Although previous theoretical work has shown that limited dispersal can favour lower virulence, it has not clarified why, with five different suggestions having been given6,8,11,12,13,14,15. Here we show that the effect of dispersal on parasite virulence can be understood entirely within the framework of inclusive fitness theory. Limited parasite dispersal favours lower parasite growth rates and, hence, reduced virulence because it (1) decreases the direct benefit of producing offspring (dispersers are worth more than non-dispersers, because they can go to patches with no or fewer parasites), and (2) increases the competition for hosts experienced by both the focal individual (‘self-shading’) and their relatives (‘kin shading’). This demonstrates that reduced virulence can be understood as an individual-level adaptation by the parasite to maximize its inclusive fitness, and clarifies the links with virulence theory more generally16.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Hamilton, W. D. The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52 (1964)
Grafen, A. Optimization of inclusive fitness. J. Theor. Biol. 238, 541–563 (2006)
Grafen, A. The formal Darwinism project: a mid-term report. J. Evol. Biol. 20, 1243–1254 (2007)
Sober, E. & Wilson, D. S. Unto Others: The Evolution and Psychology of Unselfish Behavior (Harvard Univ. Press, 1998)
Wilson, D. S. & Wilson, E. O. Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327–348 (2007)
Wilson, D. S. Social semantics: towards a genuine pluralism in the study of social behaviour. J. Evol. Biol. 21, 368–373 (2008)
Hölldobler, B. & Wilson, E. O. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies (Norton, 2008)
Kerr, B., Neuhauser, C., Bohannan, J. M. & Dean, A. M. Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons’. Nature 442, 75–78 (2006)
Boots, M. & Mealor, M. Local interactions select for lower pathogen infectivity. Science 315, 1284–1286 (2007)
Wynne-Edwards, V. C. Animal Dispersion in Relation to Social Behaviour (Oliver & Boyd, 1962)
Haraguchi, Y. & Sasaki, A. Host-parasite arms race in mutation modifications: indefinite escalation despite a heavy load. J. Theor. Biol. 183, 121–137 (1996)
Boots, M. & Sasaki, A. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. Lond. B 266, 1933–1938 (1999)
O’Keefe, K. J. & Antonovics, J. Playing by different rules: the evolution of virulence in sterilizing pathogens. Am. Nat. 159, 597–605 (2002)
Boots, M., Hudson, P. J. & Sasaki, A. Large shifts in pathogen virulence relate to host population structure. Science 303, 842–844 (2004)
Lion, S. & van Baalen, M. Self-structuring in spatial evolutionary ecology. Ecol. Lett. 11, 277–295 (2008)
Frank, S. A. Models of parasite virulence. Q. Rev. Biol. 71, 37–78 (1996)
Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, 1930)
Hamilton, W. D. Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218–1220 (1970)
Stearns, S. C. Evolution of Life Histories (Oxford Univ. Press, 1992)
Krebs, J. R. & Davies, N. B. An Introduction to Behavioural Ecology 3rd edn (Blackwell Scientific, 1993)
Rousset, F. & Ronce, O. Inclusive fitness for traits affecting metapopulation demography. Theor. Popul. Biol. 65, 127–141 (2004)
Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982)
Day, T. & Gandon, S. Applying population-genetic models in theoretical evolutionary epidemiology. Ecol. Lett. 10, 876–888 (2007)
Rousset, F. Genetic Structure and Selection in Subdivided Populations (Princeton Univ. Press, 2004)
Goodnight, C. et al. Evolution in spatial predator–prey models and the “prudent predator”: the inadequacy of steady-state organism fitness and the concept of individual and group selection. Complexity 13, 23–44 (2008)
Lehmann, L. & Keller, L. The evolution of cooperation and altruism – a general framework and a classification of models. J. Evol. Biol. 19, 1365–1376 (2006)
West, S. A., Griffin, A. S. & Gardner, A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (2007)
Gardner, A. & Grafen, A. Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659–671 (2009)
Frank, S. A. Hierarchical selection theory and sex ratios. I. General solutions for structured populations. Theor. Popul. Biol. 29, 312–342 (1986)
Queller, D. C. Quantitative genetics, inclusive fitness, and group selection. Am. Nat. 139, 540–558 (1992)
Acknowledgements
We thank M. Boots, S. Brown, A. Buckling, A. Fernandes, S. Gandon, A. Griffin and S. Lion for discussions, and the Natural Sciences and Engineering Research Council of Canada, the UK Natural Environmental Research Council, the Royal Society, the Leverhulme Trust, and the European Research Council for funding.
Author Contributions All authors contributed equally to this work.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Supplementary Information
This file contains Supplementary Data, Supplementary References, Supplementary Tables S1-S2 and Supplementary Figures S1-S2 with Legends. (PDF 1077 kb)
PowerPoint slides
Rights and permissions
About this article
Cite this article
Wild, G., Gardner, A. & West, S. Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986 (2009). https://doi.org/10.1038/nature08071
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature08071
This article is cited by
-
The scale of competition impacts parasite virulence evolution
Evolutionary Ecology (2023)
-
Shoaling guppies evade predation but have deadlier parasites
Nature Ecology & Evolution (2022)
-
The dynamics of evolutionary rescue from a novel pathogen threat in a host metapopulation
Scientific Reports (2021)
-
Low spatial structure and selection against secreted virulence factors attenuates pathogenicity in Pseudomonas aeruginosa
The ISME Journal (2018)
-
Ecological and evolutionary approaches to managing honeybee disease
Nature Ecology & Evolution (2017)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.