The Evolution and Genetics of Virus Host Shifts

PLoS Pathogens

Volumn 10, Issue 11, 2014, Pages

  Longdon, Ben ^a   Brockhurst, Michael A ^b   Russell, Colin A ^a   Welch, John J ^a   Jiggins, Francis M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CHIKUNGUNYA ALPHAVIRUS; CROSS INFECTION; GENE MUTATION; GENETIC DISTANCE; HOST PARASITE INTERACTION; HOST RANGE; HOST SHIFT; IMMUNE RESPONSE; INFLUENZA VIRUS; NONHUMAN; PHYLOGENY; RECEPTOR BINDING; VIRAL GENETICS; VIRUS ENTRY; VIRUS GENOME; VIRUS LOAD; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; EVOLUTION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; VIRAL PHENOMENA AND FUNCTIONS; VIRUS;

ANIMALS; BIOLOGICAL EVOLUTION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

EID: 84912096314     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004395     Document Type: Article

References (89)

1. Sharp PM, Hahn BH, (2010) The evolution of HIV-1 and the origin of AIDS. Philos Trans R Soc Lond B Biol Sci 365: 2487–2494.
2. Webby RJ, Webster RG, (2001) Emergence of influenza A viruses. Philos Trans R Soc Lond B Biol Sci 356: 1817–1828.
3. Liu WM, Li YY, Learn GH, Rudicell RS, Robertson JD, et al. (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467: 420–U467.
4. Li WD, Shi ZL, Yu M, Ren WZ, Smith C, et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310: 676–679.
5. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, et al. (2000) Nipah virus: a recently emergent deadly paramyxovirus. Science 288: 1432–1435.
6. Furuse Y, Suzuki A, Oshitani H, (2010) Origin of measles virus: divergence from rinderpest virus between the 11th and 12th centuries. Virol J 7: 52.
7. de Vienne DM, Refregier G, Lopez-Villavicencio M, Tellier A, Hood ME, et al. (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol 198: 347–385.
8. Sharp PM, Simmonds P, (2011) Evaluating the evidence for virus/host co-evolution. Curr Opin Virol 1: 436–441.
9. Cleaveland S, Laurenson MK, Taylor LH, (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc Lond B Biol Sci 356: 991–999.
10. Davies TJ, Pedersen AB, (2008) Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc Biol Sci 275: 1695–1701.
11. Taylor LH, Latham SM, Woolhouse ME, (2001) Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 356: 983–989.
12. Woolhouse ME, Haydon DT, Antia R, (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20: 238–244.
13. Faria NR, Suchard MA, Rambaut A, Streicker DG, Lemey P, (2013) Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Philos Trans R Soc Lond B Biol Sci 368: 20120196.
14. Pedersen AB, Davies TJ, (2009) Cross-species pathogen transmission and disease emergence in primates. Ecohealth 6: 496–508.
15. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647–652.
16. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM, (2011) Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathogens 7: e1002260.
17. de Vienne DM, Hood ME, Giraud T, (2009) Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol 22: 2532–2541.
18. Gilbert GS, Webb CO, (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci U S A 104: 4979–4983.
19. Tinsley MC, Majerus MEN, (2007) Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts. BMC Evol Biol 7: 238.
20. Russell JA, Goldman-Huertas B, Moreau CS, Baldo L, Stahlhut JK, et al. (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63: 624–640.
21. Perlman SJ, Jaenike J, (2003) Infection success in novel hosts: An experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution 57: 544–557.
22. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, et al. (2010) Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats. Science 329: 676–679.
23. Cooper N, Griffin R, Franz M, Omotayo M, Nunn CL, et al. (2012) Phylogenetic host specificity and understanding parasite sharing in primates. Ecol Lett 15: 1370–1377.
24. Waxman D, Weinert LA, Welch JJ, (2014) Inferring host range dynamics from comparative data: the protozoan parasites of new world monkeys. Am Nat 184: 65–74.
25. Huang S, Bininda-Emonds ORP, Stephens PR, Gittleman JL, Altizer S, (2013) Phylogenetically related and ecologically similar carnivores harbor similar parasite assemblages. J Anim Ecol E-pub ahead of print. doi:10.1111/1365-2656.12160
26. Hadfield JD, Krasnov BR, Poulin R, Nakagawa S, (2014) A Tale of Two Phylogenies: Comparative Analyses of Ecological Interactions. Am Nat 183: 174–187.
27. Ramsden C, Holmes EC, Charleston MA, (2009) Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol Biol Evol 26: 143–153.
28. Li JL, Cornman RS, Evans JD, Pettis JS, Zhao Y, et al. (2014) Systemic spread and propagation of a plant-pathogenic virus in European honeybees, Apis mellifera. MBio 5: e00898-00813.
29. Campisano A, Ometto L, Compant S, Pancher M, Antonielli L, et al. (2014) Interkingdom Transfer of the Acne-Causing Agent, Propionibacterium acnes, from Human to Grapevine. Mol Biol Evol 31: 1059–1065.
30. Salazar-Jaramillo L, Paspati A, van de Zande L, Vermeulen CJ, Schwander T, et al. (2014) Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis. Genome Biol Evol 6: 273–289.
31. Weinert LA, Welch JJ, Suchard MA, Lemey P, Rambaut A, et al. (2012) Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biol Lett 8: 829–832.
32. Woolhouse ME, Gowtage-Sequeria S, (2005) Host range and emerging and reemerging pathogens. Emerg Infect Dis 11: 1842–1847.
33. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, et al. (2006) Avian flu: influenza virus receptors in the human airway. Nature 440: 435–436.
34. Tetart F, Repoila F, Monod C, Krisch HM, (1996) Bacteriophage T4 host range is expanded by duplications of a small domain of the tail fiber adhesin. J Mol Biol 258: 726–731.
35. Ferris MT, Joyce P, Burch CL, (2007) High frequency of mutations that expand the host range of an RNA virus. Genetics 176: 1013–1022.
36. Hall AR, Scanlan PD, Buckling A, (2011) Bacteria-Phage Coevolution and the Emergence of Generalist Pathogens. Am Nat 177: 44–53.
37. Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, et al. (2010) Antagonistic coevolution accelerates molecular evolution. Nature 464: 275–278.
38. Crill WD, Wichman HA, Bull JJ, (2000) Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154: 27–37.
39. Woolhouse M, Scott F, Hudson Z, Howey R, Chase-Topping M, (2012) Human viruses: discovery and emergence. Philos Trans R Soc Lond B Biol Sci 367: 2864–2871.
40. Truyen U, Evermann JF, Vieler E, Parrish CR, (1996) Evolution of canine parvovirus involved loss and gain of feline host range. Virology 215: 186–189.
41. Loverdo C, Lloyd-Smith JO, (2013) Evolutionary Invasion and Escape in the Presence of Deleterious Mutations. Plos ONE 8: e61879.
42. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R, (2010) Viral mutation rates. J Virol 84: 9733–9748.
43. Carrasco P, de la Iglesia F, Elena SF, (2007) Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco Etch virus. J Virol 81: 12979–12984.
44. Orr HA, (2000) The rate of adaptation in asexuals. Genetics 155: 961–968.
45. Lalic J, Cuevas JM, Elena SF, (2011) Effect of Host Species on the Distribution of Mutational Fitness Effects for an RNA Virus. Plos Genetics 7: e1002378.
46. Anishchenko M, Bowen RA, Paessler S, Austgen L, Greene IP, et al. (2006) Venezuelan encephalitis emergence mediated by a phylogenetically predicted viral mutation. Proc Natl Acad Sci U S A 103: 4994–4999.
47. Duffy S, Burch CL, Turner PE, (2007) Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61: 2614–2622.
48. Linster M, van Boheemen S, de Graaf M, Schrauwen EJ, Lexmond P, et al. (2014) Identification, Characterization, and Natural Selection of Mutations Driving Airborne Transmission of A/H5N1 Virus. Cell 157: 329–339.
49. Tsetsarkin KA, Chen RB, Leal G, Forrester N, Higgs S, et al. (2011) Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc Natl Acad Sci U S A 108: 7872–7877.
50. Remold SK, Rambaut A, Turner PE, (2008) Evolutionary genomics of host adaptation in vesicular stomatitis virus. Mol Biol Evol 25: 1138–1147.
51. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ, (1999) Different trajectories of parallel evolution during viral adaptation. Science 285: 422–424.
52. Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, et al. (1997) Exceptional convergent evolution in a virus. Genetics 147: 1497–1507.
53. Bedhomme S, Lafforgue G, Elena SF, (2012) Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Mol Biol Evol 29: 1481–1492.
54. Agudelo-Romero P, de la Iglesia F, Elena SF, (2008) The pleiotropic cost of host-specialization in Tobacco etch potyvirus. Infect Genet Evol 8: 806–814.
55. Wallis CM, Stone AL, Sherman DJ, Damsteegt VD, Gildow FE, et al. (2007) Adaptation of plum pox virus to a herbaceous host (Pisum sativum) following serial passages. J Gen Virol 88: 2839–2845.
56. Rico P, Ivars P, Elena SF, Hernandez C, (2006) Insights into the selective pressures restricting Pelargonium flower break virus genome variability: Evidence for host adaptation. J Virol 80: 8124–8132.
57. Liang XZ, Lee BTK, Wong SM, (2002) Covariation in the capsid protein of Hibiscus chlorotic ringspot virus induced by serial passaging in a host that restricts movement leads to avirulence in its systemic host. J Virol 76: 12320–12324.
58. Streicker DG, Altizer SM, Velasco-Villa A, Rupprecht CE, (2012) Variable evolutionary routes to host establishment across repeated rabies virus host shifts among bats. Proc Natl Acad Sci U S A 109: 19715–19720.
59. Wain LV, Bailes E, Bibollet-Ruche F, Decker JM, Keele BF, et al. (2007) Adaptation of HIV-1 to its human host. Mol Biol Evol 24: 1853–1860.
60. Liu W, Tang F, Fontanet A, Zhan L, Wang TB, et al. (2005) Molecular epidemiology of SARS-associated coronavirus, Beijing. Emerg Infect Dis 11: 1420–1424.
61. Malim MH, Bieniasz PD, (2012) HIV Restriction Factors and Mechanisms of Evasion. Cold Spring Harb Perspect Med 2: a006940.
62. Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, et al. (2008) Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455: 661–664.
63. Lama J, Mangasarian A, Trono D, (1999) Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef- and Vpu-inhibitable manner. Curr Biol 9: 622–631.
64. Sauter D, Schindler M, Specht A, Landford WN, Munch J, et al. (2009) Tetherin-Driven Adaptation of Vpu and Nef Function and the Evolution of Pandemic and Nonpandemic HIV-1 Strains. Cell Host & Microbe 6: 409–421.
65. Duffy S, Turner PE, Burch CL, (2006) Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6. Genetics 172: 751–757.
66. Benmayor R, Hodgson DJ, Perron GG, Buckling A, (2009) Host Mixing and Disease Emergence. Curr Biol 19: 764–767.
67. Novella IS, Clarke DK, Quer J, Duarte EA, Lee CH, et al. (1995) Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J Virol 69: 6805–6809.
68. Greene IP, Wang E, Deardorff ER, Milleron R, Domingo E, et al. (2005) Effect of alternating passage on adaptation of sindbis virus to vertebrate and invertebrate cells. J Virol 79: 14253–14260.
69. Coffey LL, Vasilakis N, Brault AC, Powers AM, Tripet F, et al. (2008) Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci U S A 105: 6970–6975.
70. Anderson RM, May RM, (1982) Coevolution of hosts and parasites. Parasitology 85 (Pt 2) 411–426.
71. Jensen KH, Little TJ, Skorping A, Ebert D, (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4: e197.
72. Ebert D, Bull JJ (2008) The evolution and expression of virulence. In: Stearns SC, Koella JC, editors. Evolution in Health and Disease. 2nd ed. Oxford: Oxford University Press. pp. 153–167.
73. de Roode JC, Yates AJ, Altizer S, (2008) Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc Natl Acad Sci U S A 105: 7489–7494.
74. 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 U S A 104: 17441–17446.
75. Kerr PJ, (2012) Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antiviral Res 93: 387–415.
76. Fenner F, Ratcliffe FN (1965) Myxomatosis. Cambridge: Cambridge University press.
77. Kerr PJ, Ghedin E, DePasse JV, Fitch A, Cattadori IM, et al. (2012) Evolutionary history and attenuation of myxoma virus on two continents. PLoS Pathog 8: e1002950.
78. Lo MK, Lowe L, Hummel KB, Sazzad HM, Gurley ES, et al. (2012) Characterization of Nipah virus from outbreaks in Bangladesh, 2008–2010. Emerg Infect Dis 18: 248–255.
79. Leroy EM, Rouquet P, Formenty P, Souquiere S, Kilbourne A, et al. (2004) Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303: 387–390.
80. Holmes EC, (2013) What can we predict about viral evolution and emergence? Curr Opin Virol 3: 180–184.
81. Wolfe ND, Dunavan CP, Diamond J, (2007) Origins of major human infectious diseases. Nature 447: 279–283.
82. Imai M, Watanabe T, Hatta M, Das SC, Ozawa 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.
83. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, de Wit E, et al. (2012) Airborne Transmission of Influenza A/H5N1 Virus Between Ferrets. Science 336: 1534–1541.
84. Russell CA, Fonville JM, Brown AE, Burke DF, Smith DL, et al. (2012) The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336: 1541–1547.
85. Engelstadter J, Hurst GD, (2006) The dynamics of parasite incidence across host species. Evol Ecol 20: 603–616.
86. Cuthill JH, Charleston MA, (2013) A Simple Model Explains the Dynamics of Preferential Host Switching among Mammal Rna Viruses. Evolution 67: 980–990.
87. Smith JM, (1976) What determines the rate of evolution? Am Nat 110: 331–338.
88. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton: Princeton University Press.
89. Joy JB, Crespi BJ, (2012) Island phytophagy: explaining the remarkable diversity of plant-feeding insects. Proc Biol Sci 279: 3250–3255.