Unexpected consequences of culling on the eradication of wildlife diseases: The role of virulence evolution

American Naturalist

Volumn 181, Issue 3, 2013, Pages 301-313

  Bolzoni, Luca ^a,b   De Leo, Giulio A ^b,c  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Adaptive dynamics; Culling; Disease control; Superinfection; Virulence evolution; Wildlife disease

Indexed keywords

ADAPTIVE RADIATION; CULLING; DISEASE CONTROL; DISEASE PREVALENCE; EVOLUTIONARILY STABLE STRATEGY; INFECTIVITY; LIVESTOCK; PATHOGEN; TIMESCALE; VIRULENCE; WILDLIFE MANAGEMENT;

ANIMAL; ANIMAL DISEASE; ARTICLE; BIOLOGICAL MODEL; DISEASE ERADICATION; EVOLUTION; GAME; METHODOLOGY; MORTALITY; SUPERINFECTION; VIRULENCE; WILD ANIMAL; ZOONOSIS;

ANIMAL DISEASES; ANIMALS; ANIMALS, WILD; BIOLOGICAL EVOLUTION; DISEASE ERADICATION; GAME THEORY; MODELS, BIOLOGICAL; SUPERINFECTION; VIRULENCE; ZOONOSES;

EID: 84874604370     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/669154     Document Type: Article

References (65)

1. Adler, F. R., and J. L. Mosquera. 2002. Super- and coinfection: filling the range. Pages 138-149 in U. Dieckmann, J. A. J. Metz, M. W. Sabelis, and K. Sigmund, eds. Adaptive dynamics of infectionus diseases: in pursuit of virulence management. Cambridge University Press, Cambridge.
2. Alizon, S., and M. van Baalen. 2008. Multiple infections, immune dynamics, and the evolution of virulence. American Naturalist 172: E150-E168.
3. Anderson, R. M., H. C. Jackson, R. M. May, and A. M. Smith. 1981. Population dynamics of rabies in Europe. Nature 289:765-771.
4. Anderson, R. M., and R. M. May. 1979. Population biology of infectious diseases: part I. Nature 280:361-367.
5. Anderson, R. M., and R. M. May. 1982. Coevolution of hosts and parasites. Parasitology 85: 411-426.
6. Antia, R., and M. Lipsitch. 1997. Mathematical models of parasite responses to host immune defences. Parasitology 115:A155-A167.
7. Aubert, M., M. Picard, E Fouquet, J. Conde, C. Cruciere, R. Ferry, E. Albina, J. Barrat, and F. Vedeau. 1994. Classical swine fever in wild boar. Annales de Medicine Veterinaire 138:239-247.
8. Begon, M., S. M. Hazel, D. Baxby, K. Bown, R. Cavanagh, J. Chantrey, T. Jones, M. Bennett. 1999. Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society B: Biological Sciences 266:1939-1945.
9. Björkman, A., and P. A. Phillips-Howard. 1990. The epidemiology of drug resistance malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 84:177-180.
10. Boldin, B. and O. Diekmann. 2008. Superinfections can induce evolutionarily stable coexistence of pathogens. Journal of Mathematical Biology 56:635-672.
11. Bolzoni, L., L. Real, and G. A. De Leo. 2007. Transmission heterogeneity and control strategies for infectious disease emergence. PLoS ONE 2:e747.
12. Bolzoni, L., and G. A. De Leo. 2007. A cost analysis of alternative culling strategies for the eradication of classical swine fever in wildlife. Environment and Development Economics 12:653-671.
13. Bremermann, H., and H. Thieme. 1989. A competitive exclusion principle for pathogen virulence. Journal of Mathematical Biology 27:179-190.
14. Brown, C. R., and M. B. Brown. 2004. Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85:1619-1626.
15. Casagrandi, R., L. Bolzoni, S. A. Levin, and V. Andreasen. 2006. The SIRC model and influenza A. Mathematical Biosciences 200:152-169.
16. Castillo-Chavez, C., and J. X. Velasco-Hernandez. 1998. On the relationship between evolution of virulence and host demography. Journal of Theoretical Biology 192:326-333.
17. Choisy, M., and P. Rohani. 2006. Harvesting can increase severity of wildlife disease epidemics. Proceedings of the Royal Society B: Biological Sciences 273:2025-2034.
18. Coyne, M. J., G. Smith, and F. E. McAllister. 1989. Mathematical model for the population biology of rabies in raccoons in the mid-Atlantic states. American Journal of Veterinary Research 50:2148-2154.
19. Day, T., and S. R. Proulx. 2004. A general theory for the evolutionary dynamics of virulence. American Naturalist 163:E40-E62.
20. De Leo, G. A., and L. Bolzoni. 2012. Getting a free ride on poultry farms: how highly pathogenic avian influenza may persist in spite of its virulence. Theoretical Ecology 5:23-25.
21. de Jong, M. C. M., O. Diekmann, J. A. P. Heesterbeek. 1995. How does transmission of infection depend on population size? Pages 84-94 in D. Mollison, ed. Epidemic models: their structure and relation to data. Cambridge University Press, Cambridge.
22. Dieckmann, U., J. A. J. Metz, M. W. Sabelis, and K. Sigmund. 2002. Adaptive dynamics of infectionus diseases: in pursuit of virulence management. Cambridge University Press, Cambridge.
23. Donnelly, C. A., R. Woodroffe, D. R. Cox, J. Bourne, C. L. Cheeseman, R. S. Clifton-Hadley, G. Wei, et al. 2006. Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439:843-846.
24. Dushoff, J. 1996. Incorporating immunological ideas in epidemiological models. Journal of Theoretical Biology 180:181-187.
25. Dwyer, G., S. A. Levin, and L. Buttel. 1990. A simulation model of the population dynamics and evolution of myxomatosis. Ecological Monograph 60:423-447.
26. Ebert, D., and K. L. Mangin. 1997. The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51:1828-1837.
27. Eshel, I. 1977. On the founder effect and the evolution of altruistic traits: an ecogenetical approach. Theoretical Population Biology 11:410-424.
28. Fenner, F., and F. N. Ratcliff. 1965. Myxomatosis. Cambridge University Press, Cambridge.
29. Frank, S. A. 1996. Models of parasite virulence. Quarterly Review of Biology 71:37-78.
30. Galvani, A. P. 2003. Epidemiology meets evolutionary ecology. Trends in Ecology and Evolution 18:132-139.
31. Gandon, S., V. A. A. Jansen, and M. van Baalen. 2001a. Host life history and the evolution of parasite virulence, Evolution 55:1056-1062.
32. Gandon, S., M. J. Mackinnon, S. Nee, and A. F. Read. 2001b. Imperfect vaccines and the evolution of pathogen virulence. Nature 414:751-756.
33. Grenfell, B. T. 2001. Dynamics and epidemiological impact of microparasites. Pages 33-52 in G. L. Smith, W. L. Irving, J. W. McCauley, D. J. Rowlands, eds. New challenges to health: the threat of virus infection. Cambridge University Press, Cambridge.
34. Guberti, V. 1991. Fauna e patologie a denuncia obbligatoria: il caso della peste Suina Classica nel cinghiale in Toscana. Supplemento alle Ricerche di Biologia e della Selvaggina 19:393-403.
35. Guberti, V., D. Rutili, G. Ferrari, G. C. Patta, and A. Oggiano. 1998. Estimate of the threshold abundance for the persistence of the classical swine fever in the wild boar population of eastern Sardinia, Italy. Pages 54-61 in document VI/7196/98-AL. Measure to control classical swine fever in European wild boar. Commission of the European Communities, Perugia, Italy.
36. Hochberg, M. E., and R. D. Holt. 1990. The coexistence of competing parasites. I. The role of cross-species infection. American Naturalist 136:517-541.
37. Iannelli, M., M. Martcheva, and X.-Z. Li. 2005. Strain replacement in an epidemic model with super-infection and perfect vaccination. Mathematical Biosciences 195:23-46.
38. Kaden, V., H. Steyer, J. Schnabel, and W. Bruer. 2005. Classical swine fever (CSF) in wild boar: the role of the transplacental infection in the perpetuation of CSF. Journal of Veterinary Medicine B 52: 161-164.
39. Kermack, W. O., and A. G. McKendrick. 1927. Contributions to the mathematical theory of epidemics. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences 115:700-721.
40. Khibnik, A. I., Y. A. Kuznetsov, V. V. Levitin, and E. V. Nikolaev. 1993. Continuation techniques and interactive software for bifurcation analysis of ODEs and iterated maps. Physica D 62:360-371.
41. Koelle, K., S. Cobey, B. Grenfell, and M. Pascual. 2006. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314:1898-1903.
42. Kosmidou, A., R. Buttner, and G. Meyers. 1998. Isolation and characterization of cytopathogenic classical swine fever virus (CSFV). Archives of Virology 143:1295-1309.
43. Laddomada, A. 2000. Incidence and control of CSF in wild boar in Europe. Veterinary Microbiology 73:121-130.
44. Lafferty, K. D., A. M. Kuris. 2009. Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25:564-572.
45. Lipsitch, M., E. A. Herre, and M. A. Nowak. 1995. Host population structure and the evolution of virulence: a "law of diminishing returns." Evolution 49:743-748.
46. Lloyd-Smith, J. O., P. C. Cross, C. J. Briggs, M. Daugherty, W. M. Getz, J. Latto, M. S. Sanchez, A. B. Smith, and A. Swei. 2005. Should we expect population thresholds for wildlife disease? Trends Ecology and Evolution 20:511-519.
47. McLean, A. R. 1995. Vaccination, evolution and changes in efficacy of vaccines: a theoretical framework. Proceedings of the Royal Society B: Biological Sciences 261:389-393.
48. Messinger, S. M., and A. Ostling. 2009. The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. American Naturalist 174:441-454.
49. Metz, J. A. J., S. A. H. Geritz, G. Meszena, F. J. A. Jacobs, and J. S. van Heerwaarden. 1996. Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction. Pages 183-231 in S. van Strien and S. V. Lunel, eds. Stochastic and spatial structures of dynamical systems. North-Holland, Amsterdam.
50. Mosquera, J. and F. R. Adler. 1998. Evolution of virulence: a unified framework for coinfection and superinfection. Journal of Theoretical Biology 195:293-313.
51. Nowak, M. A., and R. M. May. 1994. Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society B: Biological Sciences 255:81-89.
52. Olsen, B., V. J. Munster, A. Wallensten, J. Waldenstrom, A. D. M. E. Osterhaus, and R. A. M. Fouchier. 2006. Global patterns of influenza A virus in wild birds. Science 312:384-388.
53. Porco, T. C., J. O. Lloyd-Smith, K. L. Gross, and A. P. Galvani. 2005. The effect of treatment on pathogen virulence. Journal of Theoretical Biology 233:91-102.
54. Pugliese, A. 2002. On the evolutionary coexistence of parasite strains. Mathematical Biosciences 177:355-375.
55. Ramsey, D., N. Spencer, P. Caley, M. Efford, K. Hansen, M. Lam, and D. Cooper. 2002. The effects of reducing population density on contact rates between brushtail possums: implications for transmission of bovine tuberculosis. Journal of Applied Ecology 39: 806-818.
56. Smith, D. L., S. A. Levin, and R. Laxminarayan. 2005. Strategic interactions in multi-institutional epidemics of antibiotic resistance. Proceedings of the National Academy of Sciences of the USA 102: 3153-3158.
57. Spackman, E., J. Gelb, L. A. Preskenis, B. S. Ladman, C. R. Pope, M. J. Pantin-Jackwood, and E. T. Mckinley. 2010. The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virology Journal 7:331-340.
58. Stadejek, T., S. Vilcek, J. P. Lowings, A. Ballagi-Pordany, D. J. Paton, and S. Belak. 1997. Genetic heterogeneity of classical swine fever virus in central Europe. Virus Research 52:195-204.
59. Tolari, F. 1994 Principali malattie infettive soggette ad eradicazione comuni ad animali domestici e selvatici. Pages 21-33 in Atti del XIII Convegno Nazionale Patologia della Selvaggina. March 17-19, Volterra, Italy.
60. Twiddy, S. S., J. J. Farrar, N. V. Chau, B. Wills, E. A. Gould, T. Gritsun, G. Lloyd, and E. C. Holmes. 2002. Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology 298:63-72.
61. van Baalen, M. 2002. Dilemmas in virulence management. Pages 60-69 in U. Dieckmann, J. A. J. Metz, M. W. Sabelis, and K. Sigmund, eds. Adaptive dynamics of infectionus diseases: in pursuit of virulence management. Cambridge University Press, Cambridge.
62. van Gennip, H. G. P., A. C. Vlot, M. M. Hulst, A. J. de Smit, and R. J. M. Moormann. 2004. Determinants of virulence of classical swine fever virus strain Brescia. Journal of Virology 78:8812-8823.
63. Vilcek, S., and S. Belak. 1998. Classical swine fever virus: discrimination between vaccine strains and European field viruses by restriction endonuclease cleavage of PCR amplicons. Acta Veterinaria Scandinavica 39:395-400.
64. Woodroffe, R., S. Cleaveland, O. Courtenay, M. K. Laurenson, and M. Artois. 2004. Infectious disease in the management and conservation of wild canids. Pages 124-142 in D. W. Macdonald and C. Sillero-Zubiri, eds. The biology and conservation of wild canids. Oxford University Press, Oxford.
65. Xu, C., M. S. Boyce, and D. J. Daley. 2005. Harvesting in seasonal environments. Journal of Mathematical Biology 50:663-682.