Unravelling the paradox of rabbit haemorrhagic disease virus emergence, using phylogenetic analysis; possible implications for rabbit conservation strategies

Biological Conservation

Volumn 131, Issue 2, 2006, Pages 296-306

  Forrester, N L ^a   Trout, R C ^a   Turner, S L ^a   Kelly, D ^a   Boag, B ^a   Moss, S ^a   Gould, E A ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHYLOGENETICS; SMALL MAMMAL; SPECIES CONSERVATION; VIRAL DISEASE;

MYXOMA VIRUS; ORYCTOLAGUS CUNICULUS; RABBIT HEMORRHAGIC DISEASE VIRUS;

EID: 33744923165     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2006.05.005     Document Type: Article

References (74)

1. Abu Elzein E.M., and al Afaleq A.I. Rabbit haemorrhagic disease in Saudi Arabia. Vet. Rec. 144 (1999) 480-481
2. Angulo E., and Cooke B. First synthesize new viruses then regulate their release? The case of the wild rabbit. Mol. Ecol. 11 (2002) 2701-2709
3. Asgari S., Hardy J.R., and Cooke B.D. Sequence analysis of rabbit haemorrhagic disease virus (RHDV) in Australia: alterations after its release. Arch. Virol. 144 (1999) 135-145
4. Barlow N.D., Barron M.C., and Parkes J.P. Rabbit haemorrhagic disease in New Zealand: field test of a disease-host model. Wildl. Res. 29 (2002) 649-653
5. Best S.M., and Kerr P.J. Coevolution of host and virus: the pathogenesis of virulent and attenuated strains of myxoma virus in resistent and susceptible European rabbits. Virology 267 (2000) 36-48
6. Boga J.A., Casais R., Marin M.S., Martin Alonso J.M., Carmenes R.S., Prieto M., and Parra F. Molecular cloning, sequencing and expression in Escherichia coli of the capsid protein gene from rabbit haemorrhagic disease virus (Spanish isolate AST/89). J. Gen. Virol. 75 (1994) 2409-2413
7. Calvete C., Estrada R., Lucientes J., Osacar J.J., and Villafuerte R. Effects of vaccination against viral haemorrhagic disease and myxomatosis on long-term mortality rates of European wild rabbits. Vet. Rec. 155 (2004) 388-392
8. Capucci L., Chasey D., Lavazza A., and Westcott D. Preliminary characterization of a non-haemagglutinating strain of rabbit haemorrhagic disease virus from the United Kingdom. Zentralblatt Veterinarmedizin Reihe B 43 (1996) 245-250
9. Capucci L., Fusi P., Lavazza A., Pacciarini M.L., and Rossi C. Detection and preliminary characterization of a new rabbit calicivirus related to rabbit hemorrhagic disease virus but nonpathogenic. J. Virol. 70 (1996) 8614-8623
10. Carver T., and Bleasby A. The design of Jemboss: a graphical user interface to EMBOSS. Bioinformatics 19 (2003) 1837-1843
11. Carver T.J., and Mullan L.J. A new graphical user interface to EMBOSS. Comp. Funct. Genomics 3 (2002) 75-78
12. Chambers T.J., Halevy M., Nestorowicz A., Rice C.M., and Lustig S. West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J. Gen. Virol. 79 (1998) 2375-2380
13. Chasey D. Rabbit haemorrhagic disease: the new scourge of Oryctolagus cuniculus. Lab. Anim. 31 (1997) 33-44
14. Chasey D., Trout R.C., and Edwards S. Susceptibility of wild rabbits (Oryctolagus cuniculus) in the United Kingdom to rabbit haemorrhagic disease (RHD). Vet. Res. 28 (1997) 271-276
15. Collery P.M., Mooney J., O'Connor M., and Nowotny N. Rabbit haemorrhagic disease in Ireland. Vet. Rec. 137 (1995) 547
16. Cooke B.D. Rabbit haemorrhagic disease: field epidemiology and the management of wild rabbit populations. Rev. - Off. Int. Epizoot. 21 (2002) 347-358
17. Cooke B.D., and Fenner F. Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildl. Res. 29 (2002) 689-706
18. Cook, S., Bennett, N., Holmes, E.C., de Chesse, R., Moureau, G., de Lamballerie, X., 2006. Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico.
19. Crochu S., Cook S., Attoui H., Charrel R.N., De Chesse R., Belhouchet M., Lemasson J.-J., de Micco P., and de Lamballerie X. Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J. Gen. Virol. 85 (2004) 1971-1980
20. Edwards G.P., Dobbie W., and Berman D.M. Population trends in European rabbits and other wildlife of central Australia in the wake of rabbit haemorrhagic disease. Wildl. Res. 29 (2002) 557-565
21. Edwards G.P., Dobbie W., and Berman D.M. Warren ripping: its impacts on European rabbits and other wildlife of central Australia amid the establishment of rabbit haemorrhagic disease. Wildl. Res. 29 (2002) 567-575
22. Fenner F., and Fantini B. Biological control of vertebrate pests: the history of myxomatosis, an experiment in evolution (1999), CABI, Wallingford
23. Fenner F., and Marshall I.D. Occurrence of attenuated strains of Myxoma virus in Europe. Nature 176 (1955) 782-783
24. Forrester N.L., Boag B., Moss S.R., Turner S.L., Trout R.C., White P.J., Hudson P.J., and Gould E.A. Long-term survival of New Zealand rabbit haemorrhagic disease virus RNA in wild rabbits revealed by RT-PCR and phylogenetic analysis. J. Gen. Virol. 84 (2003) 3079-3086
25. Forrester N.L., Abubakr M.I., Abu Elzein E.M., Al-Afaleq A.I., Housawi F.M., Moss S.R., Turner S.L., and Gould E.A. Phylogenetic analysis of rabbit haemorrhagic disease virus strains from the Arabian Peninsula: did RHDV emerge simultaneously in Europe and Asia?. Virology 344 (2006) 277-282
26. Fuller H.E., Chasey D., Lucas M.H., and Gibbens J.C. Rabbit haemorrhagic disease in the United Kingdom. Vet. Rec. 133 (1993) 611-613
27. Gould A.R., Kattenbelt J.A., Lenghaus C., Morrissy C., Chamberlain T., Collins B.J., and Westbury H.A. The complete nucleotide sequence of rabbit haemorrhagic disease virus (Czech V351): use of the polymerase chain reaction to detect replication in Australian vertebrates and analysis of viral population sequence variation. Virus Res. 47 (1997) 7-17
28. Heneidi Zeckua A., Zepeda Sein C., Mateos Poumian A., and Velazquez G. Model for evaluating the risk of introducing rabbit viral hemorrhagic disease based on experience in Mexico. Rev. - Off. Int. Epizoot. 16 (1997) 91-103
29. Henzell R.P., Cunningham R.B., and Neave H.M. Factors affecting the survival of Australian wild rabbits exposed to rabbit haemorrhagic disease. Wildl. Res. 29 (2002) 523-542
30. Hill J.M., Dudley J.B., Shimomura Y., and Kaufman H.E. Quantitation and kinetics of induced HSV-1 ocular shedding. Curr. Eye Res. 5 (1986) 241-246
31. Hudson J.R., and Mansi W. Attenuated strains of Myxoma virus in Britain. Vet. Rec. 67 (1955) 746
32. Le Gall G., Boilletot E., and Morisse J.P. Viral haemorrhagic disease of rabbit: purification and characterization of a strain isolated in France. Ann. Rech. Vet. 23 (1992) 381-387
33. Le Gall G., Arnauld C., Boilletot E., Morisse J.P., and Rasschaert D. Molecular epidemiology of rabbit haemorrhagic disease virus outbreaks in France during 1988 to 1995. J. Gen. Virol. 79 (1998) 11-16
34. Le Gall Recule G., Zwingelstein F., Laurent S., de Boisseson C., Portejoie Y., and Rasschaert D. Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000, and the characterisation of RHDV antigenic variants. Arch. Virol. 148 (2003) 65-81
35. Liu S.J., Xue H.P., Pu B.Q., and Quian N.H. A new viral disease in rabbits. Anim. Husb. Vet. Med. 16 (1984) 253-255 (in Chinese)
36. Lugton I.W. A cross-sectional study of risk factors affecting the outcome of rabbit haemorrhagic disease virus releases in New South Wales. Aust. Vet. J. 77 (1999) 322-328
37. Marchandeau S., Chantal J., Portejoie Y., Barraud S., and Chaval Y. Impact of viral haemorrhagic disease on a wild population of European rabbits in France. J. Wildl. Dis. 34 (1998) 429-435
38. Marchandeau S., Bertagnoli S., Peralta B., Boucraut-Baralon C., Letty J., and Reitz F. Possible interaction between myxomatosis and calicivirosis related to rabbit haemorrhagic disease affecting the European rabbit. Vet. Rec. 155 (2004) 589-592
39. McColl K.A., Morrissy C.J., Collins B.J., and Westbury H.A. Persistence of rabbit haemorrhagic disease virus in decomposing rabbit carcases. Aust. Vet. J. 80 (2002) 298-299
40. Moss S.R., Turner S.L., Trout R.C., White P.J., Hudson P.J., Desai A., Armesto M., Forrester N.L., and Gould E.A. Molecular epidemiology of rabbit haemorrhagic disease virus. J. Gen. Virol. 83 (2002) 2461-2467
41. Motha M.X.J., and Clark R.G. Confirmation of rabbit haemorrhagic disease in wild New Zealand rabbits using the ELISA. N.Z. Vet. J. 46 (1998) 83-84
42. Mutze G., Bird P., Kovaliski J., Peacock D., Jennings S., and Cooke B. Emerging epidemiological patterns in rabbit haemorrhagic disease, its interaction with myxomatosis and their effects on rabbit populations in South Australia. Wildl. Res. 20 (2002) 577-590
43. Nagesha H.S., McColl K.A., Collins B.J., Morrissy C.J., Wang L.F., and Westbury H.A. The presence of cross-reactive antibodies to rabbit haemorrhagic disease virus in Australian wild rabbits prior to the escape of virus from quarantine. Arch. Virol. 145 (2000) 749-757
44. Nowotny N., Bascunana C.R., Ballagi Pordany A., Gavier Widen D., Uhlen M., and Belak S. Phylogenetic analysis of rabbit haemorrhagic disease and European brown hare syndrome viruses by comparison of sequences from the capsid protein gene. Arch. Virol. 142 (1997) 657-673
45. Ohlinger V.F., and Thiel H.J. Identification of the viral haemorrhagic disease virus of rabbits as a calicivirus. Rev. Off. Int. Epizoot. 10 (1991) 311-323
46. Ohlinger V.F., Haas B., Meyers G., Weiland F., and Thiel H.J. Identification and characterization of the virus causing rabbit hemorrhagic disease. J. Virol. 64 (1990) 3331-3336
47. O'Keefe J.S., Tempero J.E., Motha M.X., Hansen M.F., and Atkinsona P.H. Serology of rabbit haemorrhagic disease virus in wild rabbits before and after release of the virus in New Zealand. Vet. Microbiol. 66 (1999) 29-40
48. Parkes J.P., Norbury G.L., Heyward R.P., and Sullivan G. Epidemiology of rabbit haemorrhagic disease (RHD) in the South Island, New Zealand, 1997-2001. Wildl. Res. 29 (2002) 543-555
49. Parra F., and Prieto J.M. Purification and characterization of a calicivirus as the causative agent of a lethal hemorrhagic disease in rabbits. J. Virol. 64 (1990) 4013-4015
50. Posada D.C., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
51. Robinson A.J., Kirkland P.D., Forrester R.I., Capucci L., Cooke B.D., and Philbey A.W. Serological evidence for the presence of a calicivirus in Australian wild rabbits, Oryctolagus cuniculus, before the introduction of rabbit haemorrhagic disease virus (RHDV): its potential influence on the specificity of a competitive ELISA for RHDV. Wildl. Res. 29 (2002) 655-662
52. Rodak L., Smid B., Valicek L., Vesely T., Stpanek J., Hampl J., and Jurak E. Enzyme-linked immunosorbent assay of antibodies to rabbit haemorrhagic disease virus and determination of its major structural proteins. J. Gen. Virol. 71 (1990) 1075-1080
53. Ross J.R., and Sanders M.F. Innate resistance of myxomatosis in wild rabbits in England. J. Hyg. 79 (1977) 411-415
54. Ross J.R., and Sanders M.F. The development of genetic resistance to myxomatosis in wild rabbits in Britain. J. Hyg. 92 (1984) 255-261
55. Ross J.R., and Sanders M.F. Changes in the virulence of Myxoma virus strains in Britain. Epidemiol Infect. 103 (1987) 333-357
56. Sandell P.R. Implications of rabbit haemorrhagic disease for the short-term recovery of semi-arid woodland communities in north-west Victoria. Wildl. Res. 29 (2002) 591-598
57. Shien J.H., Shieh H.K., and Lee L.H. Experimental infections of rabbits with rabbit haemorrhagic disease virus monitored by polymerase chain reaction. Res. Vet. Sci. 68 (2000) 255-259
58. Shirato K., Miyoshi H., Goto A., Ako Y., Ueko T., Kariwa H., and Takashima I. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J. Gen. Virol. 85 (2004) 3637-3645
59. Simon M.C., Girones O., Muguruza R., Alonso J.L., Muzquiz J.L., and Ortega C. Diagnostic survey of viral haemorrhagic disease in wild rabbits (Oryctolagus cuniculus) in four regions of Spain. Rev. - Off. Int. Epizoot. 14 (1995) 789-799 801-810
60. Simon M.C., Ortega C., Maynar P., Muzquiz J.L., De Blas I., Girones O., Alonso J.L., and Sanchez J. Studies in wild rabbit (Oryctolagus cuniculus) populations in Navarra (Spain). I. Epidemiology of rabbit viral haemorrhagic disease. Gibier Faune Sauvage 15 (1998) 47-64
61. Sumption K.J., and Flowerdew J.R. The ecological effects of the decline in rabbits due to myxomatosis. Mammal Rev. 15 (1985) 151-186
62. * Phylogenetic Analysis Using Parsimony (* and other methods).Version 4. (2000), Sinauer Associates, Sunderland, MA
63. Tapper S.C. Game Heritage: An Ecological Review from Shooting and Gamekeeping Records (1992), Game Conservancy, Fordingbridge
64. Thompson H.V. The rabbit in Britain. In: Thompson H.V., and King C.M. (Eds). The European Rabbit: The History and Biology of a Successful Colonizer (1994), Oxford University Press, Oxford 64-107
65. Thompson H.V., and Worden A.N. The rabbit (1956), Collins New Naturalist, London
66. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL X window interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 15 (1997) 4876-4882
67. Torres J.M., Sanchez C., Ramirez M.A., Morales M., Barcena J., Ferrer J., Espuna E., Pages Mante A., and Sanchez Vizcaino J.M. First field trial of a transmissible recombinant vaccine against myxomatosis and rabbit hemorrhagic disease. Vaccine 19 (2001) 4536-4543
68. Trout R.C. Rabbits in the farmland ecosystems. Conservation and Conflict: Mammals and Farming in Britain Proceedings of a Joint Conference of the Mammal Society and Linnean Society (2003), Westbury Publishing, Otley 198-210
69. Trout R.C., Tapper S.C., and Harradine J. Recent trends in the rabbit population in Britain. Mammal Rev. 16 (1986) 117-123
70. Trout R.C., Chasey D., and Sharp G. Seroepidemiology of rabbit haemorrhagic disease (RHD) in wild rabbits (Oryctolagus cuniculus) in the United Kingdom. J. Zool. London 243 (1997) 846-853
71. Trout R.C., Ross J., Tittensor A.M., and Fox A.P. The effect on a British wild rabbit population (Oryctolagus cuniculus) of manipulating myxomatosis. J. Appl. Ecol. 29 (1992) 679-686
72. Villafuerte R., Calvete C., Gortazar C., and Moreno S. First epizootic of rabbit haemorrhagic disease in free living populations of Oryctolagus cuniculus at Donana National Park, Spain. J. Wildl. Dis. 30 (1994) 176-179
73. White P.J., Norman R.A., Trout R.C., Gould E.A., and Hudson P.J. The emergence of rabbit haemorrhagic disease virus: will a non-pathogenic strain protect the UK?. Phil. Trans. R. Soc. Lond., B. Biol. Sci. 356 (2001) 1087-1095
74. Zheng T., Napier A.M., Parkes J.P., O'Keefe J.S., and Atkinson P.H. Detection of RNA of rabbit haemorrhagic disease virus from New Zealand wild rabbits. Wildl. Res. 29 (2002) 683-688