Transient virulence of emerging pathogens

Journal of the Royal Society Interface

Volumn 7, Issue 46, 2010, Pages 811-822

  Bolker, Benjamin M ^a   Nanda, Arjun ^b   Shah, Dharmini ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Emerging disease; Epidemiology; Evolution; Virulence

Indexed keywords

EPIDEMIOLOGY; GENES; VIRUSES;

DAPHNIA; EMERGING DISEASE; ESTIMATES OF PARAMETERS; EVOLUTIONARY DYNAMICS; EVOLVABLE; GENETIC VARIANCE; GENETIC VARIATION; GROWTH CONDITIONS; HIGH TRANSMISSION RATE; INFECTIOUS PERIOD; PARASITE-; PHASE SELECTION; SEVERE ACUTE RESPIRATORY SYNDROME; SIMPLE MODEL; TRADE-OFF CURVES; WEST NILE VIRUS;

PATHOGENS;

ANALYTICAL PARAMETERS; ARTICLE; CLINICAL ASSESSMENT; DAPHNIA; EPIDEMIC; EVOLUTION; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR DYNAMICS; MYXOMATOSIS; NONHUMAN; PATHOGENESIS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRULENCE; WEST NILE FLAVIVIRUS;

DAPHNIA; WEST NILE VIRUS;

EID: 77951689042     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0384     Document Type: Article

References (71)

1. Abrams, P. A. 2001 Modelling the adaptive dynamics of traits involved in inter- and intraspecific interactions: an assessment of three methods. Ecol. Lett. 4, 166-175. (doi:10.1046/j.1461-0248.2001.00199.x)
2. Alizon, S. & van Baalen, M. 2005 Emergence of a convex trade-off between transmission and virulence. Am. Nat. 165, E155-E167. (doi:10.1086/430053)
3. Alizon, S., Hurford, A., Mideo, N. & van Baalen, M. 2009 Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245-259. (doi:10.1111/j.1420-9101.2008.01658.x)
4. Anderson, R. M., Fraser, C., Ghani, A. C., Donnelly, C. A., Riley, S., Ferguson, N. M., Leung, G. M., Lam, T. H. & Hedley, A. J. 2004 Epidemiology, transmission dynamics, and control of SARS: the 2002-2003 epidemic. Phil. Trans. R. Soc. Lond. B 359, 1091-1105. (doi:10.1098/ rstb.2004.1490)
5. André, J. B. & Gandon, S. 2006 Vaccination, within-host dynamics, and virulence evolution. Evolution 60, 13-23. (doi:10.1111/j.0014- 3820.2006.tb01077.x) (Pubitemid 44795595)
6. André, J. B. & Godelle, B. 2006 Within-host evolution and virulence in microparasites. J. Theor. Biol. 241, 402-409. (doi:10.1016/j.jtbi. 2005.12.011)
7. André, J. & Hochberg, M. E. 2005 Virulence evolution in emerging infectious diseases. Evolution 59, 1406-1412. (doi:10.1111/j.0014-3820. 2005.tb01791.x) (Pubitemid 41098434)
8. Antia, R. & Lipsitch, M. 1997 Mathematical models of parasite responses to host immune defences. Parasitology 115, S155-S167. (doi:10.1017/S003118209700200X) (Pubitemid 28166143)
9. Ariën, K. K., Troyer, R. A., Gali, Y., Colebunders, R. L., Arts, E. J. & Vanham, G. 2005 Replicative fitness of historical and recent HIV-1 isolates suggests HIV-1 attenuation over time. AIDS 19, 1555-1564. (doi:10.1097/01.aids. 0000185989.16477.91) (Pubitemid 41502667)
10. Ariën, K. K., Vanham, G. & Arts, E. J. 2007 Is HIV-1 evolving to a less virulent form in humans? Nat. Rev. Microbiol. 5, 141-151. (doi:10.1038/nrmicro1594)
11. Beck, M. A., Handy, J. & Levander, O. A. 2004 Host nutritional status: the neglected virulence factor. Trends Microbiol. 12, 417-423. (doi:10.1016/j.tim.2004.07.007) (Pubitemid 39178593)
12. Bell, A. S., De Roode, J. C., Sim, D. & Read, A. F. 2006 Within-host competition in genetically diverse malaria infections: Parasite virulence and competitive success. Evolution 60, 1358-1371. (doi:10.1111/j.0014-3820.2006. tb01215.x) (Pubitemid 44795580)
13. Bonhoeffer, S. & Nowak, M. A. 1994 Mutation and the evolution of virulence. Proc. R. Soc. Lond. B 258, 133-140. (doi:10.1098/rspb.1994.0153)
14. Boots, M. & Mealor, M. 2007 Local interactions select for lower pathogen infectivity. Science 315, 1284-1286. (doi:10.1126/science.1137126) (Pubitemid 46364267)
15. Brault, A. C., Langevin, S. A., Bowen, R. A., Panella, N. A., Biggerstaff, B. J., Miller, B. R. & Komar, N. 2004 Differential virulence of West Nile strains for American crows. Emerg. Inf. Dis. 10, 2161-2168.
16. Brown, S. P., Cornell, S. J., Sheppard, M., Grant, A. J., Maskell, D. J., Grenfell, B. T. & Mastroeni, P. 2006 Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol. 4, e349. (doi:10.1371/journal.pbio.0040349)
17. Bull, J. J. & Ebert, D. 2008 Invasion thresholds and the evolution of nonequilibrium virulence. Evol. Appl. 1, 172-182. (doi:10.1111/j.1752-4571. 2007.00003.x)
18. Bull, J. J., Molineux, I. J. & Rice, W. R. 1991 Selection of benevolence in a host-parasite system. Evolution 45, 875-882. (doi:10.2307/2409695)
19. Courgnaud, V., Müller-Trutwin, M. & Sonigo, P. 2004 Evolution and virulence of primate lentiviruses. Medicine/ Sciences 20, 448-452.
20. Coutinho, F. A. B., Massad, E., Menezes, R. X. & Burattini, M. N. 1999 A theoretical model of the evolution of virulence in sexually transmitted HIV/AIDS. Rev. Saude Publ. 33, 329-333. (doi:10.1590/S0034-89101999000400002)
21. Davies, C. M., Fairbrother, E. & Webster, J. P. 2002 Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31-38. (doi:10.1017/S0031182001008873) (Pubitemid 34816183)
22. Day, T. 2002 On the evolution of virulence and the relationship between various measures of mortality. Proc. R. Soc. Lond. B 269, 1317-1323. (doi:10.1098/rspb.2002.2021)
23. Day, T. & Proulx, S. R. 2004 A general theory for the evolutionary dynamics of virulence. Am. Nat. 163, E40-E63. (doi:10.1086/382548)
24. de Roode, J. C., Yates, A. J. & Altizer, S. 2008 Virulence- transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489-7494. (doi:10.1073/pnas.0710909105)
25. Dieckmann, U., Metz, J. A. J., Sabelis, M. W. & Sigmund, K. (eds) 2002 Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge, UK: Cambridge University Press.
26. Dwyer, G., Levin, S. & Buttel, L. 1990 A simulation model of the population dynamics and evolution of myxomatosis. Ecol. Monogr. 60, 423-447. (doi:10.2307/1943014)
27. Ebert, D. 1994 Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084-1086. (doi:10.1126/science.265.5175. 1084)
28. Ebert, D. 1998 Experimental evolution of parasites. Science 282, 1432-1435. (doi:10.1126/science.282.5393.1432)
29. Ebert, D. 1999 The evolution and expression of parasite virulence. In Evolution in health & disease (ed. S. C. Stearns), ch. 14, pp. 161-172. Oxford, UK: Oxford University Press.
30. Ebert, D. & Bull, J. J. 2003 Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11, 15-20. (doi:10.1016/S0966-842X(02)00003-3)
31. Ebert, D. & Mangin, K. L. 1997 The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51, 1828-1837. (doi:10.2307/2411005) (Pubitemid 28104543)
32. Ewald, P. W. 1991 Transmission modes and the evolution of virulence, with special reference to cholera, influenza, and AIDS. Hum. Nat. 2, 1-30. (doi:10.1007/BF02692179)
33. Fenner, F., Day, M. F. & Woodroofe, G. M. 1956 Epidemiological consequences of the mechanical transmission of myxomatosis by mosquitoes. J. Hyg. (London) 54, 284-302. (doi:10.1017/S0022172400044521)
34. Frank, S. A. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37-78. (doi:10.1086/419267)
35. Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. 2007 Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17 441-17 446. (doi:10.1073/pnas.0708559104)
36. Gilchrist, M. A. & Coombs, D. 2006 Evolution of virulence: interdependence, constraints, and selection using nested models. Theor. Popul. Biol. 69, 145-153. (doi:10.1016/j.tpb.2005.07.002)
37. Herbeck, J. T., Gottlieb, G. S., Li, X., Hu, Z., Detels, R., Phair, J., Rinaldo, C., Jacobson, L. P., Margolick, J. B. & Mullins, J. I. 2008 Lack of evidence for changing virulence of HIV-1 in North America. PLoS ONE 3, e1525. (doi:10.1371/journal.pone.0001525)
38. Herre, E. A. 1995 Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111, S179-S191. (doi:10.1017/S0031182000075880)
39. Houle, D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
40. Jensen, K. H., Little, T., Skorping, A. & Ebert, D. 2006 Empirical support for optimal virulence in a castrating parasite. PLoS Biol. 4, e197. (doi:10.1371/journal.pbio.0040197)
41. Johnston, S. 1987 Epidemics: the forgotten factor in seventeenth century warfare in the St. Lawrence region. In Native peoples, native lands (ed. B. A. Cox), ch. 2, pp. 14-31. Montreal, Canada: McGill-Queen's University Press.
42. Kerr, B., Neuhauser, C., Bohannan, B. J. M. & Dean, A. M. 2006 Local migration promotes competitive restraint in a host-pathogen 'tragedy of the commons'. Nature 442, 75-78. (doi:10.1038/nature04864)
43. Knell, R. J. 2004 Syphilis in Renaissance Europe: rapid evolution of an introduced sexually transmitted disease? Proc. R. Soc. Lond. B 271, S174-S176. (doi:10.1098/rsbl.2003.0131)
44. Lenski, R. E. & May, R. M. 1994 The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theor. Biol. 169, 253-265. (doi:10.1006/jtbi.1994.1146)
45. Levin, B. R. & Bull, J. J. 1994 Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2, 76-81. (doi:10.1016/0966-842X(94)90538-X)
46. Levin, B. R. & Svanborg-Eden, C. 1990 Selection and the evolution of virulence in bacteria: an ecumenical excursion and modest suggestion. Parasitology 100, S103-115. (doi:10.1017/S0031182000073054)
47. Levin, B. R., Bull, J. J. & Stewart, F. M. 2001 Epidemiology, evolution, and future of the HIV/AIDS pandemic. Emerg. Inf. Dis. 7, 505-511. (doi:10.3201/eid0703.010305)
48. Levin, S. & Pimentel, D. 1981 Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117, 308-315. (doi:10.1086/283708)
49. Lipsitch, M. 1997 Transmission rates and HIV virulence: comments. Evolution 51, 319-320. (doi:10.2307/2410988)
50. Lipsitch, M. & Moxon, E. R. 1997 Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol. 5, 31-37. (doi:10.1016/S0966-842X(97)81772-6)
51. Lipsitch, M. & Nowak, M. A. 1995 The evolution of virulence in sexually-transmitted HIV/AIDS. J. Theor. Biol. 174, 427-440. (doi:10.1006/jtbi.1995.0109)
52. Mackinnon, M. J. & Read, A. F. 1999a Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689-703. (doi:10.2307/2640710)
53. Mackinnon, M. J. & Read, A. F. 1999b Selection for high and low virulence in the malaria parasite Plasmodium chabaudi. Proc. R. Soc. Lond. B 266, 741-748. (doi:10.1098/rspb.1999.0699)
54. Mackinnon, M. J. & Read, A. F. 2004 Immunity promotes virulence evolution in a malaria model. PLoS Biol. 2, e230. (doi:10.1371/journal.pbio. 0020230)
55. Mackinnon, M. J., Bell, A. & Read, A. F. 2005 The effects of mosquito transmission and population bottlenecking on virulence, multiplication rate and rosetting in rodent malaria. Int. J. Parasitol. 35, 145-153. (doi:10.1016/j.ijpara.2004.11.011)
56. Massad, E. 1996 Transmission rates and the evolution of HIV virulence. Evolution 50, 916-918. (doi:10.2307/2410863)
57. Messenger, S. L., Molineux, I. J. & Bull, J. J. 1999 Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. Lond. B 266, 397-404. (doi:10.1098/rspb.1999.0651)
58. Moya, A., Elena, S. F., Bracho, A., Miralles, R. & Barrio, E. 2000 The evolution of RNA viruses: a population genetics view. Proc. Natl Acad. Sci. USA 97, 6967-6973. (doi:10.1073/pnas.97.13.6967)
59. Müller, V. et al. 2006 Stable virulence levels in the HIV epidemic of Switzerland over two decades. AIDS 20, 889-894. (doi:10.1097/01.aids. 0000218553.51908.6b)
60. Müller, V. et al. 2009 Increasing clinical virulence in two decades of the Italian HIV epidemic. PLoS Pathogens 5, e1000454. (doi:10.1371/journal. ppat.1000454)
61. Paul, R. E. L., Lafond, T., Muller-Graf, C. D. M., Nithiuthai, S., Brey, P. T. & Koella, J. C. 2004 Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections. BMC Evol. Biol. 4, 30. (doi:10.1186/1471-2148-4-30)
62. R Development Core Team. 2007 R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. See http://www.R-project.org.
63. Sabelis, M. W. & Metz, J. A. J. 2002 Taking stock: relating theory to experiment. In Adaptive dynamics of infectious diseases: in pursuit of virulence management (eds U. Dieckmann, J. A. J. Metz, M. W. Sabelis & K. Sigmund), pp. 379-398. Cambridge, UK: Cambridge University Press.
64. Sarkar, D. 2009 lattice: lattice graphics. See http://CRAN.R-project.org/ package=lattice. R package version 0.17-25.
65. Sarkar, D. & Andrews, F. 2009 latticeExtra: extra graphical utilities based on lattice. See http://CRAN.R-project.org/package=latticeExtra. R package version 0.6-1.
66. Soetaert, K., Petzoldt, T. & Setzer, R. W. 2009 deSolve: general solvers for initial value problems of ordinary differential equations (ODE), partial differential equations (PDE) and differential algebraic equations (DAE). See http://CRAN.R-project.org/package=deSolve. R package version 1.3.
67. Topley, W. W. C. 1942 The Croonian lecture: the biology of epidemics. Proc. R. Soc. Lond. B 130, 337-359. (doi:10.1098/rspb.1942.0005)
68. Turelli, M. 1988 Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution 42, 1342-1347. (doi:10.2307/2409017)
69. Velasco-Hernandez, J. X., Gershgorn, H. B. & Blower, S. M. 2002 Could widespread use of combination antiretroviral therapy eradicate HIV epidemics? Lancet 2, 487-493. (doi:10.1016/S1473-3099(02)00346-8)
70. Wonham, M. J., de Camino-Beck, T. & Lewis, M. A. 2004 An epidemiological model for West Nile virus: invasion analysis and control applications. Proc. R. Soc. Lond. B 271, 501-507. (doi:10.1098/rspb.2003.2608)
71. Woolhouse, M. E. J., Haydon, D. T. & Antia, R. 2005 Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol. Evol. 20, 238-244. (doi:10.1016/j.tree.2005.02.009)