1887

Journal of General Virology header logo

Volume 84, Issue 4

Phylogeography of infectious haematopoietic necrosis virus in North America Free

Abstract

Infectious hematopoietic necrosis virus (IHNV) is a rhabdoviral pathogen that infects wild and cultured salmonid fish throughout the Pacific Northwest of North America. IHNV causes severe epidemics in young fish and can cause disease or occur asymptomatically in adults. In a broad survey of 323 IHNV field isolates, sequence analysis of a 303 nucleotide variable region within the glycoprotein gene revealed a maximum nucleotide diversity of 8·6 %, indicating low genetic diversity overall for this virus. Phylogenetic analysis revealed three major virus genogroups, designated U, M and L, which varied in topography and geographical range. Intragenogroup genetic diversity measures indicated that the M genogroup had three- to fourfold more diversity than the other genogroups and suggested relatively rapid evolution of the M genogroup and stasis within the U genogroup. We speculate that factors influencing IHNV evolution may have included ocean migration ranges of their salmonid host populations and anthropogenic effects associated with fish culture.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18771-0
2003-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/4/vir840803.html?itemId=/content/journal/jgv/10.1099/vir.0.18771-0&mimeType=html&fmt=ahah

References

  1. Amend D. F., Wood J. W. 1972; Survey for infectious hematopoietic necrosis (IHN) virus in Washington salmon. Prog Fish-Cult 34:143–147
     [Google Scholar]
  2. Amend D. F., Smith L. 1975; Pathophysiology of infectious hematopoietic necrosis virus disease in rainbow trout, hematological and blood chemical changes in moribund fish. Infect Immun 11:171–179
     [Google Scholar]
  3. Anderson E. D., Engelking H. M., Emmenegger E. J., Kurath G. 2000; Molecular epidemiology reveals emergence of a virulent IHN virus strain in wild salmon and transmission to hatchery fish. J Aquat Anim Health 12:85–99
     [Google Scholar]
  4. Arkush K. D., Bovo G., de Kinkelin P., Winton J. R., Wingfield W. H., Hedrick R. P. 1989; Biochemical and antigenic properties of the first isolates of infectious hematopoietic necrosis virus from salmonid fish in Europe. J Aquat Anim Health 1:148–153
     [Google Scholar]
  5. Benmansour A., Basurco B., Monnier A. F., Vende P., Winton J. R., de Kinkelin P. 1997; Sequence variation of the glycoprotein gene identifies three distinct lineages within field isolates of viral haemorrhagic septicaemia virus, a fish rhabdovirus. J Gen Virol 78:2837–2846
     [Google Scholar]
  6. Bilsel P. A., Nichol S. T. 1990; Polymerase errors accumulating during natural evolution of the glycoprotein gene of vesicular stomatitis virus Indiana serotype isolates. J Virol 64:4873–4883
     [Google Scholar]
  7. Bootland L. M., Leong J. C. 1999; Infectious hematopoietic necrosis virus. In Fish Diseases and Disorders vol. 3 pp  57–112 Edited by Woo P. T. K., Bruno D. W. Wallingford, UK: CAB International;
     [Google Scholar]
  8. Burgner R. L. 1991; Life history of sockeye salmon ( Oncorhynchus nerka ). In Pacific Salmon Life Histories pp  1–118 Edited by Groot C., Margolis L. Vancouver, BC: UBC Press;
     [Google Scholar]
  9. Busby P. J., Wainwright T. C., Bryant G. J., Lierheimer L. J., Waples R. S., Waknitz F. W., Lagomarsino I. V. 1996; Status Review of West Coast Steelhead From Washington, Idaho, Oregon, and California . US Department Commer., NOAA Tech. Memo. NMFS-NWFSC-27
  10. Busch R. A. 1983; Viral disease considerations in the commercial trout industry in Idaho. In Proceedings of a Workshop on Viral Diseases of Salmonid Fishes in the Columbia River Basin . pp 84–100 Edited by Leong J. C., Barila T. Y. Portland, OR: Bonneville Power Administration Special Publication;
  11. Domingo E., Biebricher C. K., Eigen M., Holland J. J. 2001; Experimental studies on viral quasispecies. In Quasispecies and RNA Virus Evolution: Principles and Consequences pp  90–91 Georgetown, TX: Landes Bioscience;
     [Google Scholar]
  12. Emmenegger E. J., Kurath G. 2002; Genetic characterization of infectious hematopoietic necrosis virus of coastal salmonid stocks in Washington State. J Aquat Anim Health 14:25–34
     [Google Scholar]
  13. Emmenegger R. J., Meyers T. R., Burton T. O., Kurath G. 2000; Genetic diversity and epidemiology of infectious hematopoietic necrosis virus in Alaska. Dis Aquat Org 40:163–176
     [Google Scholar]
  14. Felsenstein J. 1993 PHYLIP: Phylogeny inference package, version 3.5c University of Washington; Seattle, WA, USA:
     [Google Scholar]
  15. Fijan N., Sulimanovič D., Bearzotti M., Muzinič D., Zwillenberg L. O., Chilmonczyk S., Vautherot J. F., de Kinkelin P. 1983; Some properties of the epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio . Ann Virol (Paris 134:207–220
     [Google Scholar]
  16. Grischkowsky R. S., Amend D. F. 1976; Infectious hematopoietic necrosis virus, prevalence in certain Alaskan sockeye salmon, Oncorhynchus nerka . J Fish Res Board Can 33:186–188
     [Google Scholar]
  17. Groberg W. J. 1983; The status of viral fish diseases in the Columbia River Basin. In Proceedings of a Workshop on Viral Diseases of Salmonid Fishes in the Columbia River Basin . pp 1–22 Edited by Leong J. C., Barila T. Y. Portland, OR: Bonneville Power Administration Special Publication;
  18. Groberg W. J., Fryer J. L. 1983; Increased Occurrence of Infectious Hematopoietic Necrosis Virus in Fish at Columbia River Basin Hatcheries, 1980–1982 . Technical paper no: 6620 Corvallis, Oregon: Oregon Agricultural Experiment Station, ORESU-T-83-002;
     [Google Scholar]
  19. Guenther R. W., Watson S. W., Rucker R. R. 1959; Etiology of sockeye salmon “virus” disease. U S Fish Wildl Serv Spec Sci Rep Fish 296:1–10
     [Google Scholar]
  20. Gustafson R. G., Wainwright T. C., Winans G. A., Waknitz F. W., Parker L. T., Waples R. S. 1997; Status Review of Sockeye Salmon From Washington and Oregon . US Department Commer., NOAA Tech. Memo. NMFS-NWFSC-33
     [Google Scholar]
  21. Healey M. C. 1991; Life history of chinook salmon ( Oncorhynchus tshawytscha ). In Pacific Salmon Life Histories pp  311–394 Edited by Groot C., Margolis L. Vancouver, BC: UBC Press;
     [Google Scholar]
  22. Heard W. R. 1991; Life history of pink salmon ( Oncorhynchus gorbuscha ). In Pacific Salmon Life Histories pp  119–230 Edited by Groot C., Margolis L. Vancouver, BC: UBC Press;
     [Google Scholar]
  23. Holmes E. C., Woelk C. H., Kassis R., Bourhy H. 2002; Genetic constraints and the adaptive evolution of rabies virus in nature. Virology 292:247–257
     [Google Scholar]
  24. Hsu Y. L., Engelking H. M., Leong J. C. 1986; Occurrence of different types of infectious hematopoietic necrosis virus in fish. Appl Environ Microbiol 52:1353–1361
     [Google Scholar]
  25. Huang C., Chien M.-S., Landolt M., Batts W., Winton J. 1996; Mapping the neutralizing epitopes on the glycoprotein of infectious hematopoietic necrosis virus, a fish rhabdovirus. J Gen Virol 77:3033–3040
     [Google Scholar]
  26. Kent M. L., Traxler G. S., Kieser D., Richard J., Dawe S. C., Shaw R. W., Prosperi-Porta G., Ketcheson J., Evelyn T. P. T. 1998; Survey of salmonid pathogens in ocean-caught fishes in British Columbia, Canada. J Aquat Anim Health 10:211–219
     [Google Scholar]
  27. Kurath G., Ahern K. G., Pearson G. D., Leong J. C. 1985; Molecular cloning of six mRNA species of infectious hematopoietic necrosis virus, a fish rhabdovirus, and gene order determined by R-loop mapping. J Virol 53:469–476
     [Google Scholar]
  28. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C. 2002; Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165
     [Google Scholar]
  29. Lannan C. N., Winton J. R., Fryer J. L. 1984; Fish cell lines, establishment and characterization of nine cell lines from salmonids. In Vitro 20:671–676
     [Google Scholar]
  30. LaPatra S. E. 1994; Infectious hematopoietic necrosis virus. In Suggested Procedures for the Detection and Identification of Certain Finfish and Shellfish Pathogens . , 4th edn. pp 1–5 Edited by Thoesen J. C. Bethesda, MD: American Fisheries Society, Fish Health Section;
  31. LaPatra S. E., Lauda K. A., Jones G. R. 1994; Antigenic variants of infectious hematopoietic necrosis virus and implications for vaccine development. Dis Aquat Org 20:119–126
     [Google Scholar]
  32. Morzunov S. P., Winton J. R., Nichol S. T. 1995; The complete genome structure and phylogenetic relationship of infectious hematopoietic necrosis virus. Virus Res 38:175–192
     [Google Scholar]
  33. Mulcahy D. M., Tebbit G. L., Groberg W. J., McMichael J. S., Winton J. R., Hedrick R. P., Philippon-Fried M., Pilcher K. S., Fryer J. L. 1980; The Occurrence and Distribution of Salmonid Viruses in Oregon. Technical paper no. 5504, Oregon Agricultural Experiment Station, Corvallis, Oregon, ORESU-T-80-004
  34. Mulcahy D., Pascho R., Jenes C. K. 1984; Comparison of in vitro growth characteristics of ten isolates of infectious hematopoietic necrosis virus. J Gen Virol 65:2199–2207
     [Google Scholar]
  35. Myers J. M., Kope R. G., Bryant G. J. 8 other authors 1998; Status Review of Chinook Salmon from Washington. Idaho, Oregon and California . US Department Commer., NOAA Tech. Memo. NMFS-NWFSC-35
     [Google Scholar]
  36. Nadin-Davis S. A. 2000; Rabies and rabies-related viruses. In Molecular Epidemiology of Infectious Diseases pp  245–257 Edited by Thompson R. C. A. New York: Oxford University Press;
     [Google Scholar]
  37. Nei M. 1987 Molecular Evolutionary Genetics New York: Columbia University Press;
     [Google Scholar]
  38. Nei M., Gojobori T. 1986; Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol Biol Evol 3:418–426
     [Google Scholar]
  39. Nichol S. T., Rowe J. E., Fitch W. M. 1989; Glycoprotein evolution of vesicular stomatitis virus New Jersey. Virology 168:281–291
     [Google Scholar]
  40. Nichol S. T., Rowe J. E., Winton J. R. 1995; Molecular epizootiology and evolution of the glycoprotein and non-virion protein genes of infectious hematopoietic necrosis virus, a fish rhabdovirus. Virus Res 38:159–173
     [Google Scholar]
  41. Nicholas J. W., Hankin D. G. 1988 Chinook Salmon Populations in Oregon Coastal River Basins: Description of Life Histories and Assessment of Recent Trends in Run Strengths Ore: Dep. Fish Wildl., Fish. Div. Info. Rep., No. 88-1
    [Google Scholar]
  42. Oshima K. H., Arakawa C. K., Higman K. H., Landolt M. L., Nichol S. T., Winton J. R. 1995; The genetic diversity and epizootiology of infectious hematopoietic necrosis virus. Virus Res 35:123–141
     [Google Scholar]
  43. Pilcher K. S., Fryer J. L. 1980; The viral diseases of fish, a review through 1978. I. Diseases of proven viral etiology. CRC Crit Rev Microbiol 7:287–364
     [Google Scholar]
  44. Quinn T. P. 1984; Homing and straying in Pacific salmon. In Mechanisms of Migration in Fishes pp  357–362 Edited by McCleave J. D., Arnold G. P., Dodson J. J., Neill W. H. New York: Plenum Press;
     [Google Scholar]
  45. Quinn T. P. 1993; A review of homing and straying of wild and hatchery-produced salmon. Fish Res 18:29–44
     [Google Scholar]
  46. Ristow S. S., Arnzen J. M. 1989; Development of monoclonal antibodies that recognize a type-2 specific and a common epitope on the nucleoprotein of infectious hematopoeitic necrosis virus. J Aquat Anim Health 1:119–125
     [Google Scholar]
  47. Ristow S. S., Arnzen de Avila J. 1991; Monoclonal antibodies to the glycoprotein and nucleoprotein of infectious hematopoietic necrosis virus (IHNV) reveal differences among isolates of the virus by fluorescence, neutralization, and electrophoresis. Dis Aquat Org 11:105–115
     [Google Scholar]
  48. Roppel P. 1982; Alaska Salmon Hatcheries 1891–1959 . Alaska Historical Commission Studies. no. 20 Library of Congress #82-600591;
     [Google Scholar]
  49. Rozas J., Rozas R. 1999; DnaSP version 3, an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175
     [Google Scholar]
  50. Rucker R. R., Whipple W. J., Parvin J. R., Evans C. A. 1953; A contagious disease of salmon possibly of virus origin. U S Fish Wildl Serv Fish Bull 54:35–46
     [Google Scholar]
  51. Salo E. O. 1991; Life history of chum salmon ( Oncorhynchus keta ). In Pacific Salmon Life Histories pp  231–310 Edited by Groot C., Margolis L. Vancouver, BC: UBC Press;
     [Google Scholar]
  52. Sandercock F. K. 1991; Life history of coho salmon ( Oncorhynchus kisutch ). In Pacific Salmon Life Histories pp  395–446 Edited by Groot C., Margolis L. Vancouver, BC: UBC Press;
     [Google Scholar]
  53. Sano T., Nishimura T., Okamoto N., Yamazaki T., Hanada H., Watanabe Y. 1977; Studies on viral diseases of Japanese fish. VI. Infectious hematopoietic necrosis (IHN) of salmonids in the mainland of Japan. J Tokyo Univ Fish 63:81–85
     [Google Scholar]
  54. Schneider S., Kueffer J. M., Roessli D., Excoffier L. 1997 Arlequin, a software for population genetic data analysis version 1.1 Departments of Anthropology and Ecology, University of Geneva; Geneva, Switzerland:
     [Google Scholar]
  55. Snow M., Cunningham C. O., Melvin W. T., Kurath G. 1999; Analysis of the nucleoprotein gene identifies distinct lineages of viral haemorrhagic septicaemia virus within the European marine environment. Virus Res 63:35–44
     [Google Scholar]
  56. Stone D. M., Way K., Dixon P. F. 1997; Nucleotide sequence of the glycoprotein of viral haemorrhagic septicaemia (VHS) viruses from different geographical areas, a link between VHS in farmed fish species and viruses isolated from North Sea cod ( Gadus morhua L.). J Gen Virol 78:1319–1326
     [Google Scholar]
  57. Swofford D. L. 1998 PAUP* Phylogenetic Analysis Using Parsimony (*and other methods), Version 4 Sinauer Associates; Sunderland, MA, USA:
     [Google Scholar]
  58. Thorpe J. E. 1988; Salmon migration. Sci Prog 72:345–370
     [Google Scholar]
  59. Tordo N., Badrane H., Bourhy H., Sacramento D. 1993; Molecular epidemiology of lyssaviruses, focus on the glycoprotein and pseudogenes. Onderstepoort J Vet Res 60:315–323
     [Google Scholar]
  60. Traxler G. S., Roome J. R., Lauda K. A., LaPatra S. 1997; Appearance of infectious hematopoietic necrosis virus (IHNV) and neutralizing antibodies in sockeye salmon Oncorhynchus nerka during their migration and maturation period. Dis Aquat Org 28:31–38
     [Google Scholar]
  61. Troyer R. M., LaPatra S., Kurath G. 2000; Genetic analyses reveal unusually high diversity of infectious hematopoietic necrosis virus in rainbow trout aquaculture. J Gen Virol 81:2823–2832
     [Google Scholar]
  62. USDA Economic Research Service; 2001; Aquaculture outlook; (March 2001)
  63. Watson S. W., Guenther R. W., Rucker R. R. 1954; A virus disease of sockeye salmon, interim report. U S Fish Wildl Serv Spec Sci Rep Fish 138:1–36
     [Google Scholar]
  64. Wingfield W. H., Fryer J. L., Pilcher K. S. 1969; Properties of the sockeye salmon virus (Oregon strain). Proc Soc Exp Biol Med 130:1055–1059
     [Google Scholar]
  65. Wingfield W. H., Nims L., Fryer J. L., Pilcher K. S. 1970; Species specificity of the sockeye salmon virus (Oregon strain) and its cytopathic effects in salmonid cell lines. In A Symposium on Diseases of Fishes and Shellfishes pp  319–326 Edited by Snieszko S. F. Washington, DC: American Fisheries Society;
     [Google Scholar]
  66. Winton J. R., Arakawa C. K., Lannan C. N., Fryer J. L. 1988; Neutralizing monoclonal antibodies recognize antigenic variants among isolates of infectious hematopoietic necrosis virus. Dis Aquat Org 4:199–204
     [Google Scholar]
  67. Wolf K. 1988 Fish Viruses and Fish Viral Diseases pp  83–114 Ithaca: Cornell University Press;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18771-0
Loading
Phylogeography of infectious haematopoietic necrosis virus in North America
J. Gen. Virol. 84, 803 (2003); https://doi.org/10.1099/vir.0.18771-0
/content/journal/jgv/10.1099/vir.0.18771-0
/content/journal/jgv/10.1099/vir.0.18771-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error