1887

Abstract

Salmonid alphavirus (SAV) causes infections in farmed Atlantic salmon and rainbow trout in Europe. Genetic diversity exists among SAV strains from farmed fish and six subtypes have been proposed based on genetic distance. Here, we used six full-genome sequences and 71 partial sequences of the structural ORF to estimate the evolutionary rate of SAV. The rate, 2.13×10 nt substitutions per site per year, was further used to date evolutionary events in a Bayesian phylogenetic framework. The comparison of these dates with known historical events suggested that all six subtypes diverged prior to the twentieth century, earlier than the first attempts to introduce and farm rainbow trout in Europe. The subtypes must therefore have existed in a wild reservoir, as yet unidentified. The strains of each subtype, with the exception of subtype 2, have a common ancestor that existed after the 1970s – the start of modern farming of Atlantic salmon. These ancestors are likely to represent the independent introductions to farmed fish populations from the wild reservoir. The subtypes have developed subsequently into self-sustainable epizootics. The most parsimonious phylogeographic reconstruction suggested that the location of the wild reservoir is in or around the North Sea. After the initial introductions to aquaculture, further transmission of SAV was likely related to the industry infrastructure. This was exemplified by the finding of genetically identical subtype 2 and 3 strains separated by large geographical distances, as well as genetically distinct co-circulating lineages within the same geographical area.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.057455-0
2014-01-01
2019-11-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/1/52.html?itemId=/content/journal/jgv/10.1099/vir.0.057455-0&mimeType=html&fmt=ahah

References

  1. Allison A. B., Stallknecht D. E.. ( 2009; ). Genomic sequencing of Highlands J virus: a comparison to western and eastern equine encephalitis viruses. . Virus Res 145:, 334–340. [CrossRef] [PubMed]
    [Google Scholar]
  2. Andersen L., Hodneland K., Nylund A.. ( 2010; ). No influence of oxygen levels on pathogenesis and virus shedding in Salmonid alphavirus (SAV)-challenged Atlantic salmon (Salmo salar L.). . Virol J 7:, 198. [CrossRef] [PubMed]
    [Google Scholar]
  3. Arrigo N. C., Adams A. P., Weaver S. C.. ( 2010; ). Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision. . J Virol 84:, 1014–1025. [CrossRef] [PubMed]
    [Google Scholar]
  4. Auguste A. J., Adams A. P., Arrigo N. C., Martinez R., Travassos da Rosa A. P., Adesiyun A. A., Chadee D. D., Tesh R. B., Carrington C. V., Weaver S. C.. ( 2010; ). Isolation and characterization of sylvatic mosquito-borne viruses in Trinidad: enzootic transmission and a new potential vector of Mucambo virus. . Am J Trop Med Hyg 83:, 1262–1265. [CrossRef] [PubMed]
    [Google Scholar]
  5. Boucher P., Baudin Laurencin F.. ( 1994; ). Sleeping disease (SD) of salmonids. . Bull Eur Assoc Fish Pathol 14:, 179–180.
    [Google Scholar]
  6. Bratland A., Nylund A.. ( 2009; ). Studies on the possibility of vertical transmission of Norwegian salmonid Alphavirus in production of Atlantic salmon in Norway. . J Aquat Anim Health 21:, 173–178. [CrossRef] [PubMed]
    [Google Scholar]
  7. Drummond A. J., Suchard M. A., Xie D., Rambaut A.. ( 2012; ). Bayesian phylogenetics with BEAUti and the BEAST 1.7. . Mol Biol Evol 29:, 1969–1973. [CrossRef] [PubMed]
    [Google Scholar]
  8. Edgar R. C.. ( 2004; ). MUSCLE: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32:, 1792–1797. [CrossRef] [PubMed]
    [Google Scholar]
  9. Fringuelli E., Rowley H. M., Wilson J. C., Hunter R., Rodger H., Graham D. A.. ( 2008; ). Phylogenetic analyses and molecular epidemiology of European salmonid alphaviruses (SAV) based on partial E2 and nsP3 gene nucleotide sequences. . J Fish Dis 31:, 811–823. [CrossRef] [PubMed]
    [Google Scholar]
  10. Garoff H., Sjöberg M., Cheng R. H.. ( 2004; ). Budding of alphaviruses. . Virus Res 106:, 103–116. [CrossRef] [PubMed]
    [Google Scholar]
  11. Graham D. A., Fringuelli E., Rowley H. M., Cockerill D., Cox D. I., Turnbull T., Rodger H., Morris D., McLoughlin M. F.. ( 2012; ). Geographical distribution of salmonid alphavirus subtypes in marine farmed Atlantic salmon, Salmo salar L., in Scotland and Ireland. . J Fish Dis 35:, 755–765. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hasegawa M., Kishino H., Yano T.. ( 1985; ). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. . J Mol Evol 22:, 160–174. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hershberger W. K.. ( 1992; ). Genetic variability in rainbow trout populations. . Aquaculture 100:, 51–71. [CrossRef]
    [Google Scholar]
  14. Hjortaas M. J., Skjelstad H. R., Taksdal T., Olsen A. B., Johansen R., Bang-Jensen B., Ørpetveit I., Sindre H.. ( 2013; ). The first detections of subtype 2-related salmonid alphavirus (SAV2) in Atlantic salmon, Salmo salar L., in Norway. . J Fish Dis 36:, 71–74. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hodneland K., Bratland A., Christie K. E., Endresen C., Nylund A.. ( 2005; ). New subtype of salmonid alphavirus (SAV), Togaviridae, from Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss in Norway. . Dis Aquat Organ 66:, 113–120. [CrossRef] [PubMed]
    [Google Scholar]
  16. Jansen M. D., Gjerset B., Modahl I., Bohlin J.. ( 2010; ). Molecular epidemiology of salmonid alphavirus (SAV) subtype 3 in Norway. . Virol J 7:, 188. [CrossRef] [PubMed]
    [Google Scholar]
  17. Karlsen M., Hodneland K., Endresen C., Nylund A.. ( 2006; ). Genetic stability within the Norwegian subtype of salmonid alphavirus (family Togaviridae). . Arch Virol 151:, 861–874. [CrossRef] [PubMed]
    [Google Scholar]
  18. Karlsen M., Yousaf M. N., Villoing S., Nylund A., Rimstad E.. ( 2010; ). The amino terminus of the salmonid alphavirus capsid protein determines subcellular localization and inhibits cellular proliferation. . Arch Virol 155:, 1281–1293. [CrossRef] [PubMed]
    [Google Scholar]
  19. Kristoffersen A. B., Viljugrein H., Kongtorp R. T., Brun E., Jansen P. A.. ( 2009; ). Risk factors for pancreas disease (PD) outbreaks in farmed Atlantic salmon and rainbow trout in Norway during 2003-2007. . Prev Vet Med 90:, 127–136. [CrossRef] [PubMed]
    [Google Scholar]
  20. Lester K., Black J., Bruno D.. ( 2011; ). Prevalence of salmonid alphavirus in Scottish fish farms from 2006 to 2007. . Bull Eur Assoc Fish Pathol 31:, 199–204.
    [Google Scholar]
  21. McLoughlin M. F., Graham D. A.. ( 2007; ). Alphavirus infections in salmonids – a review. . J Fish Dis 30:, 511–531. [CrossRef] [PubMed]
    [Google Scholar]
  22. McLoughlin M. F., Nelson R. N., McCormack J. I., Rowley H. M., Bryson D. B.. ( 2002; ). Clinical and histopathological features of naturally occurring pancreas disease in farmed Atlantic salmon, Salmo salar L. . J Fish Dis 25:, 33–43. [CrossRef]
    [Google Scholar]
  23. Minin V. N., Bloomquist E. W., Suchard M. A.. ( 2008; ). Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. . Mol Biol Evol 25:, 1459–1471. [CrossRef] [PubMed]
    [Google Scholar]
  24. Munro A. L. S., Ellis A. E., McVicar A. H., Anne McLay H., Needham E. A.. ( 1984; ). An exocrine pancreas disease of farmed Atlantic salmon in Scotland. . Helgol Meersunters 37:, 571–586.
    [Google Scholar]
  25. Nelson R. T., McLoughlin M. F., Rowley H. M., Platten M. A., McCormick J. I.. ( 1995; ). Isolation of a toga-like virus from farmed Atlantic salmon Salmo salar with pancreas disease. . Dis Aquat Organ 22:, 25–32. [CrossRef]
    [Google Scholar]
  26. Padhi A., Moore A. T., Brown M. B., Foster J. E., Pfeffer M., Gaines K. P., O’Brien V. A., Strickler S. A., Johnson A. E., Brown C. R.. ( 2008; ). Phylogeographical structure and evolutionary history of two Buggy Creek virus lineages in the western Great Plains of North America. . J Gen Virol 89:, 2122–2131. [CrossRef] [PubMed]
    [Google Scholar]
  27. Poppe T., Rimstad E., Hyllseth B.. ( 1989; ). Pancreas Disease in Atlantic salmon (Salmo salar) post-smolts infected with infectious pancreatic necrosis (IPNV). . Bull Eur Assoc Fish Pathol 9:, 83–85.
    [Google Scholar]
  28. Shapiro B., Ho S. Y. W., Drummond A. J., Suchard M. A., Pybus O. G., Rambaut A.. ( 2011; ). A Bayesian phylogenetic method to estimate unknown sequence ages. . Mol Biol Evol 28:, 879–887. [CrossRef] [PubMed]
    [Google Scholar]
  29. Snow M., Black J., Matejusova I., McIntosh R., Baretto E., Wallace I. S., Bruno D. W.. ( 2010; ). Detection of salmonid alphavirus RNA in wild marine fish: implications for the origins of salmon pancreas disease in aquaculture. . Dis Aquat Organ 91:, 177–188. [CrossRef] [PubMed]
    [Google Scholar]
  30. Tamura K., Nei M.. ( 1993; ). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. . Mol Biol Evol 10:, 512–526.[PubMed]
    [Google Scholar]
  31. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. ( 2011; ). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  32. Tavaré S.. ( 1986; ). Some probabilistic and statistical problems in the analysis of DNA sequences. . Lect Math Life Sci 17:, 57–86.
    [Google Scholar]
  33. Viljugrein H., Staalstrøm A., Molvaer J., Urke H. A., Jansen P. A.. ( 2009; ). Integration of hydrodynamics into a statistical model on the spread of pancreas disease (PD) in salmon farming. . Dis Aquat Organ 88:, 35–44. [CrossRef] [PubMed]
    [Google Scholar]
  34. Villoing S., Béarzotti M., Chilmonczyk S., Castric J., Brémont M.. ( 2000; ). Rainbow trout sleeping disease virus is an atypical alphavirus. . J Virol 74:, 173–183. [CrossRef] [PubMed]
    [Google Scholar]
  35. Volk S. M., Chen R., Tsetsarkin K. A., Adams A. P., Garcia T. I., Sall A. A., Nasar F., Schuh A. J., Holmes E. C.. & other authors ( 2010; ). Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. . J Virol 84:, 6497–6504. [CrossRef] [PubMed]
    [Google Scholar]
  36. Welsh M., Weston J., Borghmans B. J., Mackie D., Rowley H., Nelson R., McLoughlin M., Todd D.. ( 2000; ). Biochemical characterization of salmon pancreas disease virus. . J Gen Virol 81:, 813–820.[PubMed]
    [Google Scholar]
  37. Weston J. H., Welsh M. D., McLoughlin M. F., Todd D.. ( 1999; ). Salmon pancreas disease virus, an alphavirus infecting farmed Atlantic salmon, Salmo salar L.. Virology 256:, 188–195. [CrossRef] [PubMed]
    [Google Scholar]
  38. Weston J., Villoing S., Brémont M., Castric J., Pfeffer M., Jewhurst V., McLoughlin M., Rødseth O., Christie K. E.. & other authors ( 2002; ). Comparison of two aquatic alphaviruses, salmon pancreas disease virus and sleeping disease virus, by using genome sequence analysis, monoclonal reactivity, and cross-infection. . J Virol 76:, 6155–6163. [CrossRef] [PubMed]
    [Google Scholar]
  39. Yang Z.. ( 1994; ). Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. . J Mol Evol 39:, 306–314. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.057455-0
Loading
/content/journal/jgv/10.1099/vir.0.057455-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most Cited This Month

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