Adaptation and the evolution of parasite virulence in a connected world

• Published in: Nature (London) Vol. 459; no. 7249; pp. 983 - 986
• Main Authors: Wild, Geoff, Gardner, Andy, West, Stuart A.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 18.06.2009; Nature Publishing Group
• Subjects: Adaptation; Adaptation (Biology); Adaptation, Physiological; Analysis; Animals; Biological and medical sciences; Biological Evolution; Competition; Distribution; Fundamental and applied biological sciences. Psychology; Genetics of eukaryotes. Biological and molecular evolution; Geography; Humanities and Social Sciences; Insect viruses; Kin selection (Evolution); letter; Models, Biological; Mortality; multidisciplinary; Natural history; Natural selection; Observations; Parasites; Parasites - pathogenicity; Science; Selection, Genetic; Study and teaching; Theory; Virulence; Virulence (Microbiology); World; Canada; Pathogenicity; Biological evolution; Virulence; Parasite; Mathematical model; Epidemiology; Dispersion
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature08071

They are all individuals The conventional view of adaptation is that it operates at the level of the individual organism, but recent observations of the evolution of virulence in viruses infecting moths and bacteria in spatially structured populations (where dispersal is limited) have been interpreted as examples of group selection. Wild et al . here extend previous models mathematically to show that the effect of dispersal on parasite virulence can be understood as an individual-level adaptation by the parasite entirely within the context of kin selection theory. The evolution of lowered virulence in spatially structured populations with limited dispersal has been suggested to be an example of adaptation at the group level. The extension of previous models now shows that the effect of dispersal can be understood within the framework of inclusive fitness theory, demonstrating that reduced virulence could be due to individual-level adaptation by the parasite. Adaptation is conventionally regarded as occurring at the level of the individual organism, where it functions to maximize the individual’s inclusive fitness 1 , 2 , 3 . However, it has recently been argued that empirical studies on the evolution of parasite virulence in spatial populations show otherwise 4 , 5 , 6 , 7 . In particular, it has been claimed that the evolution of lower virulence in response to limited parasite dispersal 8 , 9 provides proof of Wynne-Edwards’s 10 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 given 6 , 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 generally 16 .