1887

Journal of General Virology header logo

Volume 93, Issue 5

Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus Free

Abstract

A global phylogeny for chelonid fibropapilloma-associated herpesvirus (CFPHV), the most likely aetiological agent of fibropapillomatosis (FP) in sea turtles, was inferred, using dated sequences, through Bayesian Markov chain Monte Carlo analysis and used to estimate the virus evolutionary rate independent of the evolution of the host, and to resolve the phylogenetic positions of new haplotypes from Puerto Rico and the Gulf of Guinea. Four phylogeographical groups were identified: eastern Pacific, western Atlantic/eastern Caribbean, mid-west Pacific and Atlantic. The latter comprises the Gulf of Guinea and Puerto Rico, suggesting recent virus gene flow between these two regions. One virus haplotype from Florida remained elusive, representing either an independent lineage sharing a common ancestor with all other identified virus variants or an Atlantic representative of the lineage giving rise to the eastern Pacific group. The virus evolutionary rate ranged from 1.62×10 to 2.22×10 substitutions per site per year, which is much faster than what is expected for a herpesvirus. The mean time for the most recent common ancestor of the modern virus variants was estimated at 192.90–429.71 years ago, which, although more recent than previous estimates, still supports an interpretation that the global FP pandemic is not the result of a recent acquisition of a virulence mutation(s). The phylogeographical pattern obtained seems partially to reflect sea turtle movements, whereas altered environments appear to be implicated in current FP outbreaks and in the modern evolutionary history of CFPHV.

  • Received:
  • Accepted:
  • Published Online:
© 2012 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.038950-0
2012-05-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/5/1035.html?itemId=/content/journal/jgv/10.1099/vir.0.038950-0&mimeType=html&fmt=ahah

References

  1. Aguirre A. A., Lutz P. L. 2004; Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator?. EcoHealth 1:275–283 [View Article]
     [Google Scholar]
  2. Arthur K., Limpus C., Balazs G., Capper A., Udy J., Shaw G., Keuper-Bennett U., Bennett P. 2008a; The exposure of green turtles (Chelonia mydas) to tumour promoting compounds produced by the cyanobacterium Lyngbya majuscula and their potential role in the aetiology of fibropapillomatosis. Harmful Algae 7:114–125 [View Article]
     [Google Scholar]
  3. Arthur K. E., Boyle M. C., Limpus C. J. 2008b; Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Mar Ecol Prog Ser 362:303–311 [View Article]
     [Google Scholar]
  4. Babkin I., Shchelkunov S. 2008; Molecular evolution of poxviruses. Russ J Genet 44:895–908 [View Article]
     [Google Scholar]
  5. Bowen B. W., Karl S. A. 2007; Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907 [View Article][PubMed]
     [Google Scholar]
  6. Bowen B. W., Grant W. S., Hillis-Starr Z., Shaver D. J., Bjorndal K. A., Bolten A. B., Bass A. L. 2007; Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60 [View Article][PubMed]
     [Google Scholar]
  7. Bowser P. R., Wooster G. A., Getchell R. G. 1999; Transmission of Walleye Dermal sarcoma and lymphocystis via waterborne exposure. J Aquat Anim Health 11:158–161 [View Article]
     [Google Scholar]
  8. Casale P., Abbate G., Freggi D., Conte N., Oliverio M., Argano R. 2008; Foraging ecology of loggerhead sea turtles Caretta caretta in the central Mediterranean Sea: evidence for a relaxed life history model. Mar Ecol Prog Ser 372:265–276 [View Article]
     [Google Scholar]
  9. Chaloupka M., Work T. M., Balazs G. H., Murakawa S. K. K., Morris R. 2008; Cause-specific temporal and spatial trends in green sea turtle strandings in the Hawaiian Archipelago (1982–2003). Mar Biol 154:887–898 [View Article]
     [Google Scholar]
  10. Chen R., Holmes E. C. 2006; Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 23:2336–2341 [View Article][PubMed]
     [Google Scholar]
  11. Curry S. S., Brown D. R., Gaskin J. M., Jacobson E. R., Ehrhart L. M., Blahak S., Herbst L. H., Klein P. A. 2000; Persistent infectivity of a disease-associated herpesvirus in green turtles after exposure to seawater. J Wildl Dis 36:792–797[PubMed] [CrossRef]
     [Google Scholar]
  12. Davison A. J. 2002; Evolution of the herpesviruses. Vet Microbiol 86:69–88 [View Article][PubMed]
     [Google Scholar]
  13. Debruyne R., Poinar H. N. 2009; Time dependency of molecular rates in ancient DNA data sets, a sampling artifact?. Syst Biol 58:348–360 [View Article][PubMed]
     [Google Scholar]
  14. Diez C. E., van Dam R. P., Velez-Zuazo X., Torres F., Scharer M., Molina M. 2010; Habitat and population assessment of Caribbean green turtle aggregations inhabiting the Culebra Archipelago’s coastal waters. In Proceedings of the 28th Annual Symposium on Sea Turtle Biology and Conservation22–26 January 2008, Loreto, Mexico. NOAA Technical Memorandum NOAA NMFS-SEFSC. Compiled by Dean K., Lopez-Castro M.C.
    [Google Scholar]
  15. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [View Article][PubMed]
     [Google Scholar]
  16. Drummond A. J., Nicholls G. K., Rodrigo A. G., Solomon W. 2002; Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320[PubMed]
     [Google Scholar]
  17. Drummond A. J., Ho S. Y., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88 [View Article][PubMed]
     [Google Scholar]
  18. Drummond A. J., Ho S. Y. W., Rawlence N., Rambaut A. 2007; A rough guide to beast 1.4. http://beast.bio.ed.ac.uk/Main_Page
  19. Duffy S., Shackelton L. A., Holmes E. C. 2008; Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276 [View Article][PubMed]
     [Google Scholar]
  20. Emerson B. C. 2007; Alarm bells for the molecular clock? No support for Ho et al.’s model of time-dependent molecular rate estimates. Syst Biol 56:337–345 [View Article][PubMed]
     [Google Scholar]
  21. Ene A., Su M., Lemaire S., Rose C., Schaff S., Moretti R., Lenz J., Herbst L. H. 2005; Distribution of chelonid fibropapillomatosis-associated herpesvirus variants in Florida: molecular genetic evidence for infection of turtles following recruitment to neritic developmental habitats. J Wildl Dis 41:489–497[PubMed] [CrossRef]
     [Google Scholar]
  22. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [View Article]
     [Google Scholar]
  23. Firth C., Charleston M. A., Duffy S., Shapiro B., Holmes E. C. 2009; Insights into the evolutionary history of an emerging livestock pathogen: porcine circovirus 2. J Virol 83:12813–12821 [View Article][PubMed]
     [Google Scholar]
  24. Firth C., Kitchen A., Shapiro B., Suchard M. A., Holmes E. C., Rambaut A. 2010; Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. Mol Biol Evol 27:2038–2051 [View Article][PubMed]
     [Google Scholar]
  25. Foley A. M., Schroeder B. A., Redlow A. E., Fick-Child K. J., Teas W. G. 2005; Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and associations with environmental factors. J Wildl Dis 41:29–41[PubMed] [CrossRef]
     [Google Scholar]
  26. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582 [View Article][PubMed]
     [Google Scholar]
  27. Greenblatt R. J., Quackenbush S. L., Casey R. N., Rovnak J., Balazs G. H., Work T. M., Casey J. W., Sutton C. A. 2005; Genomic variation of the fibropapilloma-associated marine turtle herpesvirus across seven geographic areas and three host species. J Virol 79:1125–1132 [View Article][PubMed]
     [Google Scholar]
  28. Guindon S., Lethiec F., Duroux P., Gascuel O. 2005; phyml Online – a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:Web Server issueW557–W559 [View Article][PubMed]
     [Google Scholar]
  29. Hall B. G. 2007 Phylogenetic Trees Made Easy: A How-to-Manual Sunderland, MA: Sinauer Associates;
     [Google Scholar]
  30. 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 [View Article][PubMed]
     [Google Scholar]
  31. Herbst L. H. 1994; Fibropapillomatosis of marine turtles. Annu Rev Fish Dis 4:389–425 [View Article]
     [Google Scholar]
  32. Herbst L. H., Klein P. A. 1995; Green turtle fibropapillomatosis: challenges to assessing the role of environmental cofactors. Environ Health Perspect 103:Suppl. 427–30[PubMed] [CrossRef]
     [Google Scholar]
  33. Herbst L. H., Jacobson E. R., Moretti R., Brown T., Sundberg J. P., Klein P. A. 1995; Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Dis Aquat Organ 22:1–12 [View Article]
     [Google Scholar]
  34. Herbst L. H., Moretti R., Brown T., Klein P. A. 1996; Sensitivity of the transmissible green turtle fibropapillomatosis agent to chloroform and ultracentrifugation conditions. Dis Aquat Organ 25:225–228 [View Article]
     [Google Scholar]
  35. Herbst L. H., Ene A., Su M., Desalle R., Lenz J. 2004; Tumor outbreaks in marine turtles are not due to recent herpesvirus mutations. Curr Biol 14:R697–R699 [View Article][PubMed]
     [Google Scholar]
  36. Herbst L. H., Lemaire S., Ene A. R., Heslin D. J., Ehrhart L. M., Bagley D. A., Klein P. A., Lenz J. 2008; Use of baculovirus-expressed glycoprotein H in an enzyme-linked immunosorbent assay developed to assess exposure to chelonid fibropapillomatosis-associated herpesvirus and its relationship to the prevalence of fibropapillomatosis in sea turtles. Clin Vaccine Immunol 15:843–851 [View Article][PubMed]
     [Google Scholar]
  37. Hirama S., Ehrhart L. M. 2007; Description, prevalence and severity of green turtle papillomatosis in three developmental habitats on the east coast of Florida. Fla Sci 70:435–448
     [Google Scholar]
  38. Ho S. Y. W., Larson G. 2006; Molecular clocks: when times are a-changin’. Trends Genet 22:79–83 [View Article][PubMed]
     [Google Scholar]
  39. Ho S. Y. W., Phillips M. J., Cooper A., Drummond A. J. 2005a; Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568 [View Article][PubMed]
     [Google Scholar]
  40. Ho S. Y. W., Phillips M. J., Drummond A. J., Cooper A. 2005b; Accuracy of rate estimation using relaxed-clock models with a critical focus on the early metazoan radiation. Mol Biol Evol 22:1355–1363 [View Article][PubMed]
     [Google Scholar]
  41. Ho S. Y. W., Kolokotronis S.-O., Allaby R. G. 2007a; Elevated substitution rates estimated from ancient DNA sequences. Biol Lett 3:702–705 [View Article][PubMed]
     [Google Scholar]
  42. Ho S. Y. W., Shapiro B., Phillips M. J., Cooper A., Drummond A. J. 2007b; Evidence for time dependency of molecular rate estimates. Syst Biol 56:515–522 [View Article][PubMed]
     [Google Scholar]
  43. Hughes A. L., Irausquin S., Friedman R. 2010; The evolutionary biology of poxviruses. Infect Genet Evol 10:50–59 [View Article][PubMed]
     [Google Scholar]
  44. IUCN 2010; IUCN Red List of Threatened Species, version 2010.4. www.iucnredlist.org
  45. Lackovich J. K., Brown D. R., Homer B. L., Garber R. L., Mader D. R., Moretti R. H., Patterson A. D., Herbst L. H., Oros J. other authors 1999; Association of herpesvirus with fibropapillomatosis of the green turtle Chelonia mydas and the loggerhead turtle Caretta caretta in Florida. Dis Aquat Organ 37:89–97 [View Article][PubMed]
     [Google Scholar]
  46. Lahanas P. N., Bjorndal K. A., Bolten A. B., Encalada S. E., Miyamoto M. M., Valverde R. A., Bowen B. W. 1998; Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Mar Biol 130:345–352 [View Article]
     [Google Scholar]
  47. Maddison W., Maddison D. R. 2001; Mesquite: a modular system for evolutionary analysis. Evolution 62:1103–1118
     [Google Scholar]
  48. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [View Article][PubMed]
     [Google Scholar]
  49. Martin D. P., Posada D., Crandall K. A., Williamson C. 2005; A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102 [View Article][PubMed]
     [Google Scholar]
  50. Martin D. P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. 2010; rdp3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463 [View Article][PubMed]
     [Google Scholar]
  51. Maynard Smith J. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129 [View Article][PubMed]
     [Google Scholar]
  52. McGeoch D. J., Gatherer D. 2005; Integrating reptilian herpesviruses into the family Herpesviridae . J Virol 79:725–731 [View Article][PubMed]
     [Google Scholar]
  53. McGeoch D. J., Dolan A., Ralph A. C. 2000; Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J Virol 74:10401–10406 [View Article][PubMed]
     [Google Scholar]
  54. Ng T. F. F., Manire C., Borrowman K., Langer T., Ehrhart L., Breitbart M. 2009; Discovery of a novel single-stranded DNA virus from a sea turtle fibropapilloma by using viral metagenomics. J Virol 83:2500–2509 [View Article][PubMed]
     [Google Scholar]
  55. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [View Article][PubMed]
     [Google Scholar]
  56. Plotkin P. T., Byles R. A., Rostal D. C., Owens D. W. 1995; Independent versus socially facilitated oceanic migrations of the olive ridley, Lepidochelys olivacea . Mar Biol 122:137–143 [View Article]
     [Google Scholar]
  57. Pond S. L. K., Muse S. V. 2005; HyPhy: hypothesis testing using phylogenies. In Statistical Methods in Molecular Evolution (Statistics for Biology and Health) pp. 125–181 Edited by Nielsen R. New York: Springer; [View Article]
     [Google Scholar]
  58. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [View Article][PubMed]
     [Google Scholar]
  59. Quackenbush S. L., Work T. M., Balazs G. H., Casey R. N., Rovnak J., Chaves A., duToit L., Baines J. D., Parrish C. R. other authors 1998; Three closely related herpesviruses are associated with fibropapillomatosis in marine turtles. Virology 246:392–399 [View Article][PubMed]
     [Google Scholar]
  60. Quackenbush S. L., Casey R. N., Murcek R. J., Paul T. A., Work T. M., Limpus C. J., Chaves A., duToit L., Perez J. V. other authors 2001; Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real-time PCR. Virology 287:105–111 [View Article][PubMed]
     [Google Scholar]
  61. Rambaut A., Drummond A. 2003; Tracer. http://tree.bio.ed.ac.uk/software/tracer/
  62. Rambaut A., Drummond A. J. 2009; TreeAnnotator v1.5.3: MCMC output analysis. http://beast.bio.ed.ac.uk/TreeAnnotator
  63. Rambaut A., Drummond A. 2010; FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK. http://tree.bio.ed.ac.uk/software/figtree/
  64. Rambaut A., Pybus O. G., Nelson M. I., Viboud C., Taubenberger J. K., Holmes E. C. 2008; The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–619 [View Article][PubMed]
     [Google Scholar]
  65. Sakaoka H., Kurita K., Iida Y., Takada S., Umene K., Kim Y. T., Ren C. S., Nahmias A. J. 1994; Quantitative analysis of genomic polymorphism of herpes simplex virus type 1 strains from six countries: studies of molecular evolution and molecular epidemiology of the virus. J Gen Virol 75:513–527 [View Article][PubMed]
     [Google Scholar]
  66. Shackelton L. A., Parrish C. R., Truyen U., Holmes E. C. 2005; High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci U S A 102:379–384 [View Article][PubMed]
     [Google Scholar]
  67. Shapiro B., Rambaut A., Drummond A. J. 2006; Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9 [View Article][PubMed]
     [Google Scholar]
  68. Smith G. J. D., Bahl J., Vijaykrishna D., Zhang J., Poon L. L. M., Chen H., Webster R. G., Peiris J. S. M., Guan Y. 2009; Dating the emergence of pandemic influenza viruses. Proc Natl Acad Sci U S A 106:11709–11712 [View Article][PubMed]
     [Google Scholar]
  69. Suyama M., Torrents D., Bork P. 2006; pal2nal: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:Web Server issueW609–W612 [View Article][PubMed]
     [Google Scholar]
  70. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
     [Google Scholar]
  71. Tavaré S. 1986; Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 17:57–86
     [Google Scholar]
  72. Thompson J. D., Gibson T. J., Higgins D. G. 2002; Multiple sequence alignment using ClustalW and ClustalX. In Current Protocols in Bioinformatics2.3.1–2.3.22 John Wiley & Sons;
     [Google Scholar]
  73. Umene K., Sakaoka H. 1999; Evolution of herpes simplex virus type 1 under herpesviral evolutionary processes. Arch Virol 144:637–656 [View Article][PubMed]
     [Google Scholar]
  74. Van Houtan K. S., Hargrove S. K., Balazs G. H. 2010; Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS ONE 5:e12900 [View Article][PubMed]
     [Google Scholar]
  75. Velez-Zuazo X., Diez C. E., van Dam R. P., Torres-Velez F. 2010; Genetic structure and origin of a juvenile aggregation affected by fibropapillomatosis: potential impact on adult recruitment. In Proceedings of the 28th Annual Symposium on Sea Turtle Biology and Conservation22–26 January 2008, Loreto, Mexico. NOAA Technical Memorandum NOAA NMFS-SEFSC. Compiled by Dean K., Lopez-Castro M.C.
    [Google Scholar]
  76. Work T. M., Balazs G. H. 1999; Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. J Wildl Dis 35:804–807[PubMed] [CrossRef]
     [Google Scholar]
  77. Work T. M., Balazs G. H., Wolcott M., Morris R. 2003; Bacteraemia in free-ranging Hawaiian green turtles Chelonia mydas with fibropapillomatosis. Dis Aquat Organ 53:41–46 [View Article][PubMed]
     [Google Scholar]
  78. Work T. M., Balazs G. H., Rameyer R. A., Morris R. A. 2004; Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian Islands, 1993–2003. Dis Aquat Organ 62:163–176 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.038950-0
Loading
Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus
J. Gen. Virol. 93, 1035 (2012); https://doi.org/10.1099/vir.0.038950-0
/content/journal/jgv/10.1099/vir.0.038950-0
/content/journal/jgv/10.1099/vir.0.038950-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

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