Abstract
Many of the major human infectious diseases, including some now confined to humans and absent from animals, are ‘new’ ones that arose only after the origins of agriculture. Where did they come from? Why are they overwhelmingly of Old World origins? Here we show that answers to these questions are different for tropical and temperate diseases; for instance, in the relative importance of domestic animals and wild primates as sources. We identify five intermediate stages through which a pathogen exclusively infecting animals may become transformed into a pathogen exclusively infecting humans. We propose an initiative to resolve disputed origins of major diseases, and a global early warning system to monitor pathogens infecting individuals exposed to wild animals.
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References
- 1.
Diamond, J. Guns, Germs, and Steel: the Fates of Human Societies (Norton, New York, 1997)
- 2.
Dobson, A. P. & Carper, E. R. Infectious diseases and human population history. Bioscience 46, 115–126 (1996)
- 3.
Diamond, J. & Panosian, C. in When Disease Makes History: Epidemics and Great Historical Turning Points (ed. Hämäläinen, P.) 17–44 (Helsinki Univ. Press, 2006)
- 4.
McNeill, W. H. Plagues and Peoples (Anchor, Garden City, 1976)
- 5.
Crosby, A. W. Ecological Imperialism: the Biological Expansion of Europe 900–1900 (Cambridge Univ. Press, Cambridge, UK, 1986)
- 6.
Ramenofsky, A. Vectors of Death: the Archaeology of European Contact (New Mexico Press, Albuquerque, 1987)
- 7.
Anderson, R. M. & May, R. M. Infectious Diseases of Humans: Dynamics and Control (Oxford Univ. Press, Oxford, UK, 1991)
- 8.
Lopez, A. D., Mathers, C. D., Ezzati, N., Jamison, D. T. & Murray, C. J. L. (eds) Global Burden of Disease and Risk Factors (Oxford Univ. Press, New York, 2006)
- 9.
Bellwood, P. First Farmers: the Origins of Agriculture Societies (Blackwell, Oxford, 2005)
- 10.
Diamond, J. Evolution, consequences, and future of plant and animal domestication. Nature 418, 34–41 (2002)
- 11.
McNeill, J. R. in When Disease Makes History: Epidemics and Great Historical Turning Points (ed. Hämäläinen, P.) 81–111 (Helsinki Univ. Press, Helsinki, 2006)
- 12.
Waters, A. P., Higgins, D. G. & McCutchan, T. F. Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc. Natl Acad. Sci. USA 88, 3140–3144 (1991)
- 13.
Ayala, F. J., Escalante, A. A. & Rich, S. M. Evolution of Plasmodium and the recent origin of the world populations of Plasmodium falciparum. Parassitologia 41, 55–68 (1999)
- 14.
Van Heuverswyn, F. et al. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444, 164 (2006)
- 15.
Wolfe, N. D. et al. Naturally acquired simian retrovirus infections in central African hunters. Lancet 363, 932–937 (2004)
- 16.
Kuiken, T. et al. Pathogen surveillance in animals. Science 309, 1680–1681 (2005)
- 17.
Wang, D. et al. Viral discovery and sequence recovery using DNA microarrays. PLoS Biol. 1, E2 (2003)
- 18.
Jones, M. S. et al. New DNA viruses identified in patients with acute viral infection syndrome. J. Virol. 79, 8230–8236 (2005)
- 19.
Switzer, W. M. et al. Ancient co-speciation of simian foamy viruses and primates. Nature 434, 376–380 (2005)
- 20.
Taylor, L. H., Latham, S. M. & Woolhouse, M. E. Risk factors for human disease emergence. Phil. Trans. R. Soc. Lond. B 356, 983–989 (2001)
- 21.
Moya, A., Holmes, E. C. & Gonzalez-Candelas, F. The population genetics and evolutionary epidemiology of RNA viruses. Nature Rev. Microbiol. 2, 279–288 (2004)
- 22.
Antia, R., Regoes, R. H., Koella, J. C. & Bergstrom, C. T. The role of evolution in the emergence of infectious diseases. Nature 426, 658–661 (2003)
- 23.
May, R. M., Gupta, S. & McLean, A. R. Infectious disease dynamics: what characterizes a successful invader? Phil. Trans. R. Soc. Lond. B 356, 901–910 (2001)
- 24.
Morens, D. M., Folkers, G. K. & Fauci, A. S. The challenge of emerging and re-emerging infectious diseases. Nature 430, 242–249 (2004)
- 25.
Morse, S. S. Factors in the emergence of infectious diseases. Emerg. Infect. Dis. 1, 7–15 (1995)
- 26.
Wilson, M. E. Travel and the emergence of infectious diseases. Emerg. Infect. Dis. 1, 39–46 (1995)
- 27.
Weiss, R. A. & McMichael, A. J. Social and environmental risk factors in the emergence of infectious diseases. Nature Med. 10, S70–S76 (2004)
Acknowledgements
We thank L. Krain for assistance with Supplementary Note S10; M. Antolin, D. Burke, L. Fleisher, E. Holmes, L. Real, A. Rimoin, R. Weiss and M. Woolhouse for comments; and many other colleagues for providing information. This work was supported by an NIH Director’s Pioneer Award and Fogarty International Center IRSDA Award (to N.D.W.), a W. W. Smith Foundation award (to N.D.W.), and National Geographic Society awards (to J.D. and N.D.W.).
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Affiliations
Department of Epidemiology, School of Public Health, University of California, Los Angeles 90095-1772, USA
- Nathan D. Wolfe
Division of Infectious Diseases, David Geffen School of Medicine, University of California, Los Angeles 90095-1688, USA
- Claire Panosian Dunavan
Departments of Geography and of Environmental Health Sciences, University of California, Los Angeles 90095-1524, USA
- Jared Diamond
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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
Corresponding authors
Correspondence to Nathan D. Wolfe or Jared Diamond.
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