Multiple scales of selection influence the evolutionary emergence of novel pathogens

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1614, 2013, Pages

  Park, Miran ^a   Loverdo, Claude ^a   Schreiber, Sebastian J ^b   Lloyd Smith, James O ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Adaptation; Branching processes; Emerging diseases; Pathogen evolution

Indexed keywords

ANTIBIOTICS; DISEASE INCIDENCE; EMERGENCE; FITNESS; GENOTYPE; LABORATORY METHOD; PATHOGEN; PROBABILITY; STOCHASTICITY;

ARTICLE; BIOLOGICAL MODEL; COMMUNICABLE DISEASE; COMPUTER SIMULATION; EVOLUTION; GENETIC SELECTION; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN; REPRODUCTIVE FITNESS;

BIOLOGICAL EVOLUTION; COMMUNICABLE DISEASES, EMERGING; COMPUTER SIMULATION; GENETIC FITNESS; GENOTYPE; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, GENETIC; SELECTION, GENETIC;

MLCS; MLOWN;

EID: 84873460086     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0333     Document Type: Article

References (64)

1. Morens DM, Folkers GK, Fauci AS. 2004 The challenge of emerging and re-emerging infectious diseases. Nature 430, 242-249. (doi:10.1038/ nature02759)
2. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak D. 2008 Global trends in emerging infectious diseases. Nature 451, 990-993. (doi:10.1038/nature06536)
3. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, Hudson PJ, Grenfell BT. 2009 Epidemic dynamics at the human-animal interface. Science 326, 1362-1367. (doi:10.1126/ science.1177345)
4. Iwasa Y, Michor F, Nowak MA. 2004 Evolutionary dynamics of invasion and escape. J. Theor. Biol. 226, 205-214. (doi:10.1016/j.jtbi.2003.08.014)
5. Pepin KM, Lass S, Pulliam JRC, Read AF, Lloyd-Smith JO. 2010 Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat. Rev. Microbiol. 8, 802-813. (doi:10.1038/ nrmicro2440)
6. Parrish CR, Holmes EC, Morens DM, Park E-C, Burke DS, Calisher CH, Laughlin CA, Saif LJ, Daszak P. 2008 Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72, 457-470. (doi:10.1128/MMBR.00004-08)
7. Imai M et al. 2012 Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420-428. (doi:10.1038/ nature10831)
8. Herfst S et al. 2012 Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534-1541. (doi:10.1126/science.1213362)
9. Fauci AS, Collins FS. 2012 Benefits and risks of influenza research: lessons learned. Science 336, 1522-1523. (doi:10.1126/science.1224305)
10. Poelwijk FJ, Kivient DJ, Weinreich DM, Tans SJ. 2007 Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445, 383-386. (doi:10.1038/nature05451)
11. Weinreich DM, Delaney NF, DePristo MA, Hartl DL 2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111-114. (doi:10.1126/science.1123539)
12. Lozovsky ER, Chookajorn T, Brown KM, Imwong M, Shaw PJ, Kamchonwongpaisan S, Neafsey DE, Weinreich DM, Hartl DL 2009 Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proc. Natl Acad. Sci. USA 106, 12 024-12 030. (doi:10.1073/pnas.0905922106)
13. Stucker KM, Pagan I, Cifuente JO, Kaelber JT, Lillie TD, Hafenstein S, Holmes EC, Parrish CR. 2012 The role of evolutionary intermediates in the host adaptation of canine parvovirus. J. Virol. 86, 1514-1521. (doi:10.1128/JVI.06222-11)
14. Hoelzer K, Murcia PR, Baillie GJ, Wood JL, Metzger SM, Osterrieder N, Dubovi EJ, Holmes EC, Parrish CR. 2010 Intrahost evolutionary dynamics of canine influenza virus in naive and partially immune dogs. J. Virol. 84, 5329-5335. (doi:10.1128/JVI.02469-09)
15. Murcia PR et al. 2010 Intra-and interhost evolutionary dynamics of equine influenza virus. J. Virol. 84, 6943-6954. (doi:10.1128/JVI.00112-10)
16. Murcia PR et al. 2012 Evolution of an Eurasian avian-like influenza virus in naive and vaccinated pigs. PLoS Pathog. 8, e1002730. (doi:10.1371/ journal.ppat.1002730)
17. Russell CA et al. 2012 The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336, 1541-1547. (doi:10.1126/science.1222526)
18. The Chinese-SARS Molecular Epidemiology Consortium. 2004 Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303, 1666-1669. (doi:10.1126/ science.1092002)
19. Reperant LA, Kuiken T, Grenfell BT, Osterhaus ADME, Dobson AP. 2012 Linking influenza virus tissue tropism to population-level reproductive fitness. PLoS ONE 7, e43115. (doi:10.1371/journal.pone.0043115)
20. Williams GC. 1992 Natural selection: domains, levels and challenges, vol. 4. Oxford series in ecology and evolution. New York, NY: Oxford University Press.
21. Keller L. 1999 Levels of selection in evolution. Princeton, NJ: Princeton University Press.
22. Okasha S. 2006 Evolution and the levels of selection. Oxford, UK: Clarendon Press.
23. Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP 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)
24. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, Meehan MO, Lutalo T, Gray RH. 2000 Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342, 921-929. (doi:10.1056/NEJM200003303421303)
25. Antia R, Levin BR, May RM. 1994 Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am. Nat. 144, 457-472. (doi:10.1086/285686)
26. Ganusov VV, Antia R. 2003 Trade-offs and the evolution of virulence of microparasites: do details matter? Theor. Popul. Biol. 64, 211-220. (doi:10.1016/S0040-5809(03)00063-7)
27. Porco TC, Lloyd-Smith JO, Gross KL, Galvani AP. 2005. The effect of treatment on pathogen virulence. J. Theor. Biol. 233, 91-102. (doi:10.1016/j.jtbi.2004.09.009)
28. Reperant LA, Kuiken T, Grenfell BT, Osterhaus ADME, Dobson AP. 2012 Linking influenza virus tissue tropism to population-level reproductive fitness. PLoS ONE 7, e43115. (doi:10.1371/ journal.pone.0043115)
29. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT. 2006 Host species barrier to influenza virus infections. Science 312, 394-397. (doi:10.1126/science.1122818)
30. Antia R, Regoes RR, Koella JC, Bergstrom CT. 2003 The role of evolution in the emergence of infectious diseases. Nature 426, 658-661. (doi:10.1038/ nature02104)
31. Yates A, Antia R, Regoes RR. 2006 How do pathogen evolution and host heterogeneity interact in disease emergence? Proc. R. Soc. B 273, 3075-3083. (doi:10.1098/rspb.2006.3681)
32. Arinaminpathy N, McLean AR. 2009 Evolution and emergence of novel human infections. Proc. R. Soc. B 276, 3937-3943. (doi:10.1098/rspb.2009.1059)
33. Alexander HK, Day T. 2010 Risk factors for the evolutionary emergence of pathogens. J. R. Soc. Interface 7, 1455-1474. (doi:10.1098/rsif.2010.0123)
34. André J-B, Day T. 2005 The effect of disease life history on the evolutionary emergence of novel pathogens. Proc. R. Soc. B 272, 1949-1956. (doi:10.1098/rspn.2005.3170)
35. Amaku M, Burattini M, Coutinho F, Massad E. 2010 Modeling the dynamics of viral evolution considering competition within individual hosts and at population level: the effects of treatment. Bull. Math. Biol. 72, 1294-1314. (doi:10.1007/s11538-009-9495-6)
36. Iwasa Y, Michor F, Nowak MA. 2005 Virus evolution within patients increases pathogenicity. J. Theor. Biol. 232, 17-26. (doi:10.1016/j.jtbi.2004.07.016)
37. Mullins JI, Rolland M, Allen TM. 2008 Viral evolution and escape during primary human immunodeficiency virus-1 infection: implications for vaccine design. Curr. Opin. HIV AIDS 3, 60-66. (doi:10.1097/COH.0b013e3282f233d9)
38. da Silva J, Coetzer M, Nedellec R, Pastore C, Mosier DE. 2010 Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region. Genetics 185, 293-303. (doi:10.1534/genetics.109.112458)
39. Gillespie JH. 1984 Molecular evolution over the mutational landscape. Evolution 38, 1116-1129.
40. Harris TE. 1963 The theory of branching processes. Berlin, Germany: Springer.
41. Jensen JLWV. 1906 Sur les fonctions convexes et les inégalités entre les valeurs. Acta Mathematica 30, 175-193.
42. Elena SF, Sanjuán R. 2007 Virus evolution: insights from an experimental approach. Annu. Rev. Ecol. Evol. Syst. 38, 27-52. (doi:10.1146/annurev.ecolsys.38.091206.095637)
43. Fernàndez G, Clotet B, Martínez MA. 2006 Fitness landscape of human immunodeficiency virus type 1 protease quasispecies. J. Virol. 81, 2485-2496. (doi:10.1128/JVI.01594-06)
44. Burch CL, Chao L. 1999 Evolution by small steps and rugged landscapes in the RNA virus f 6. Genetics 151, 921-927.
45. Park AW, Daly JM, Lewis NS, Smith DJ, Wood JL, Grenfell BT. 2009 Quantifying the impact of immune escape on transmission dynamics of influenza. Science 326, 726-728. (doi:10.1126/science.1175980)
46. Schreiber SJ, Lloyd-Smith JO. 2009 Invasion dynamics in spatially heterogeneous environments. Am. Nat. 174, 490-505. (doi:10.1086/605405)
47. Gilchrist MA, 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)
48. Coombs D, Gilchrist MA, Ball CL. 2007 Evaluating the importance of within-and between-host selection pressures on the evolution of chronic pathogens. Theor. Popul. Biol. 72, 576-591. (doi:10.1016/j.tpb.2007.08.005)
49. Mideo N, Alizon S, Day T. 2008 Linking within-and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23, 511-517. (doi:10.1016/j.tree.2008.05.009)
50. Burch CL, Chao L. 2000 Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406, 625-628. (doi:10.1038/35020564)
51. Loverdo C, Park M, Schreiber SJ, Lloyd-Smith JO. 2012 Influence of viral replication mechanisms on within-host evolutionary dynamics. Evolution 66, 3462-3471. (doi:10.1111/j.1558-5646.2012.01687.x)
52. Wright CF, Morelli MJ, Thbaud G, Knowles NJ, Herzyk P, Paton DJ, Haydon DT, King DP. 2010 Beyond the consensus: dissecting within-host viral population diversity of foot-and-mouth disease virus by using next-generation genome sequencing. J. Virol. 85, 2266-2275. (doi:10.1128/JVI.01396-10)
53. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. 2010 Viral mutation rates. J. Virol. 84, 9733-9748. (doi:10.1128/JVI.00694-10)
54. Eigen M. 1993 Viral quasispecies. Sci. Am. 269, 42-49. (doi:10.1038/scientificamerican0793-42)
55. Más A, López-Galíndez C, Cacho I, Gómez J, Martínez MA. 2010 Unfinished stories on viral quasispecies and Darwinian views of evolution. J. Mol. Biol. 397, 865-877. (doi:10.1016/j.jmb.2010.02.005)
56. Keele BF et al. 2008 Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl Acad. Sci. USA 105, 7552-7557. (doi:10.1073/ pnas.0802203105)
57. Wang GP, Sherrill-Mix SA, Chang K-M, Quince C, Bushman FD. 2010 Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J. Virol. 84, 6218-6228. (doi:10.1128/JVI.02271-09)
58. Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB, Ortega AN, Sawyer SL, Parrish CR. 2012 Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog. 8, e1002666. (doi:10.1371/ journal.ppat.1002666)
59. Allison AB et al. 2012 Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. J. Virol. 86, 865-872. (doi:10.1128/JVI.06187-11)
60. Zhao G-P. 2007 SARS molecular epidemiology: a Chinese fairy tale of controlling an emerging zoonotic disease in the genomics era. Phil. Trans. R. Soc. B 352, 1063-1081. (doi:10.1098/rstb.2007.2034)
61. Sheahan T, Rockx B, Donaldson E, Corti D, Baric R. 2008 Pathways of cross-species transmission of synthetically reconstructed zoonotic severe acute respiratory syndrome coronavirus. J. Virol. 82, 8721-8732. (doi:10.1128/JVI.00818-08)
62. Lythgoe KA, Fraser C 2012 New insights into the evolutionary rate of HIV-1 at the within-host and epidemiological levels. Proc. R. Soc. B 279, 3367-3375. (doi:10.1098/rspb.2012.0595)
63. Faure M, Schreiber SJ. 2012 Quasi-stationary distributions for randomly perturbed dynamical systems. (http://arxiv.org/abs/1101.3420)
64. Haldane JBS. 1927 The mathematical theory of natural and artificial selection. V. Selection and mutation. Proc. Camb. Philos. Soc. 23, 838-844. (doi:10.1017/S0305004100015644)