Evolution of Disease Virulence

by

Samuel Alizon

• LAST REVIEWED: 13 January 2014
• LAST MODIFIED: 13 January 2014
• DOI: 10.1093/obo/9780199941728-0018

Introduction

Understanding why parasites harm their host has long puzzled evolutionary biologists. For most micro- and macroparasite species, keeping the host alive and in good shape seems to ensure longer transmission. However, this general evolution toward avirulence is not supported by the data. That parasites remain virulent over long time periods suggests that virulence confers an advantage to the parasite either at the between-host level (if being virulent improves the number of secondary infections) or at the within-host level (if being virulent improves host exploitation). This adaptive vision of virulence has been criticized as an elegant hypothesis that lacks empirical support. However, it is now firmly rooted in data. Understanding virulence evolution has generated many studies based on experimental and field data, but also many mathematical models. These numerous studies usually revolve around two questions: “How do virulent strains persist?” and “Given that virulence can be adaptive, how will the optimal level of virulence be affected by ecological and epidemiological factors (such as host density or spatial structure)?” Understanding why parasites harm their host raises general issues in evolutionary biology, such as the evolution of a system with two (or more) actors with multilevel selective pressures (within-host and between-host). It also has important public health implications, such as avoiding selecting for more virulent strains or (hopefully) controlling virulence evolution.

General Overviews

One could argue that virulence evolution is a field in which there almost are more reviews than research articles. The place to start is probably Ewald 1994, which summarizes the author’s view on adaptiveness for virulence. However, Zimmer 2003 is accessible to a wider audience. Some reviews offer a focus on specific aspects; Bull 1994, for example, discusses virulence from the point of view of a molecular biologist, whereas Ebert and Herre 1996 focuses on transmission model and genetic constraints. Frank 1996 stands out as one of the first reviews of mathematical models for virulence evolution. Frank also discusses kin selection issues, a topic also raised in Chao, et al. 2000, but from a more experimental side. Mackinnon and Read 2004 is interesting because it analyses virulence evolution through works performed on a single parasite, Plasmodium. Finally, Schmid-Hempel 2011 is very detailed and contains a rich bibliography on the topic. In fact, many of the topics dealt with in this review are also discussed by Schmid-Hempel.

• Bull, J. J. 1994. Virulence. Evolution 48.5: 1423–1437.

  DOI: 10.2307/2410237

  This general review detail the various explanations as to why pathogens harm their host, with a special emphasis on levels of selection. Available online for purchase or by subscription.

• Chao, L., K. A. Hanley, C. L. Burch, C. Dahlberg, and P. E. Turner. 2000. Kin selection and parasite evolution: Higher and lower virulence with hard and soft selection. Quarterly Review of Biology 75.3: 261–275.

  DOI: 10.1086/393499

  A review that focuses more specifically on how kin selection can help us understand virulence evolution, particularly the context of genetically diverse infections, where the relatedness among coinfecting parasites can vary. Available online for purchase or by subscription.

• Ebert, D., and E. A. Herre. 1996. The evolution of parasitic diseases. Parasitology Today 12.3: 96–101.

  DOI: 10.1016/0169-4758(96)80668-5

  A general review on virulence evolution, with a particular emphasis on genetic constraints and vertical transmission. Available online for purchase or by subscription.

• Ewald, P. W. 1994. Evolution of infectious disease. Oxford: Oxford Univ. Press.

  This book is one of the most accessible publications on the topic. Paul Ewald advocates his idea that virulence evolution can be understood and directed. The fact that this is a single-author book makes it easier to read. Note that a shorter version of his argument was published in 1993 in Scientific American.

• Frank, S. A. 1996. Models of parasite virulence. Quarterly Review of Biology 71.1: 37–78.

  DOI: 10.1086/419267

  This long review puts a special emphasis on mathematical approaches to virulence evolution, especially that based on kin selection theory. It also provides the reader with a detailed overview of the theory, and remains one of the most informative reviews. Available online for purchase or by subscription.

• Mackinnon, M. J., and A. F. Read. 2004. Virulence in malaria: An evolutionary viewpoint. Philosophical Transactions of the Royal Society B: Biological Sciences 359.1446: 965–986.

  DOI: 10.1098/rstb.2003.1414

  A review focused on the case of malaria, which is one of the most studied organisms in this context. It illustrates how these general questions on virulence evolution can be applied to the case of a specific parasite.

• Schmid-Hempel, P. 2011. Evolutionary parasitology: The integrated study of infections, immunology, ecology, and genetics. Oxford: Oxford Univ. Press.

  A recent book focused on parasite evolution. Virulence evolution has a central place in it, and the chapter is very pedagogical, with helpful boxes. This is probably the first place to look for a detailed, recent, and clear overview of the topic. It is also the best place to find an extensive bibliography on the topic.

• Zimmer, C. 2003. Taming pathogens: An elegant idea, but does it work? Science 300.5624: 1362–1364.

  DOI: 10.1126/science.300.5624.1362

  An article by science writer Carl Zimmer about the feasibility of controlling virulence evolution. An entertaining reading for a wide audience. Available online for purchase or by subscription.