Skip to main content

Advertisement

SpringerLink
Log in

The Evolutionary Dynamics of Bluetongue Virus

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Bluetongue virus (BTV) is a midge-borne member of the genus Orbivirus that causes an eponymous debilitating livestock disease of great agricultural impact and which has expanded into Europe in recent decades. Reassortment among the ten segments comprising the double-stranded (ds) RNA genome of BTV has played an important role in generating the epidemic strains of this virus in Europe. In this study, we investigated the dynamics of BTV genome segment evolution utilizing time-structured data sets of complete sequences from four segments, totalling 290 sequences largely sampled from ruminant hosts. Our analysis revealed that BTV genome segments generally evolve under strong purifying selection and at substitution rates that are generally lower (mean rates of ~0.5–7 × 10−4 nucleotide substitutions per site, per year) than vector-borne positive-sense viruses with single-strand (ss) RNA genomes. These also represent the most robust estimates of the nucleotide substitution rate in a dsRNA virus generated to date. Additionally, we determined that patterns of geographic structure and times to most recent common ancestor differ substantially between each segment, including a relatively recent origin for the diversity of segment 10 within the past millennium. Together, these findings demonstrate the effect of reassortment to decouple the evolutionary dynamics of BTV genome segments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anthony SJ, Maan N, Maan S, Sutton G, Attoui H, Mertens PPC (2009) Genetic and phylogenetic analysis of the non-structural proteins NS1, NS2 and NS3 of epizootic haemorrhagic disease virus (EHDV). Virus Res 145:211–219

    Article  CAS  PubMed  Google Scholar 

  • Barratt-Boyes SM, MacLachlan NJ (1994) Dynamics of viral spread in bluetongue virus infectedcalves. Vet Microbiol 40:361–371

    Article  CAS  PubMed  Google Scholar 

  • Batten CA, Maan S, Shaw AE, Maan NS, Mertens PP (2008) A European field strain of bluetongue virus derived from two parental vaccine strains by genome segment reassortment. Virus Res 137:56–63

    Article  CAS  PubMed  Google Scholar 

  • Bonneau KR, Mullens BA, MacLachlan NJ (2001) Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J Virol 75:8298–8305

    Article  CAS  PubMed  Google Scholar 

  • Chare ER, Holmes EC (2004) Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 85:3149–3157

    Article  CAS  PubMed  Google Scholar 

  • Coffey LL, Vasilakis N, Brault AC, Powers AM, Tripet F, Weaver SC (2008) Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci USA 105:6970–6975

    Article  CAS  PubMed  Google Scholar 

  • de Mattos CC, de Mattos CA, MacLachlan NJ, Giavedoni LD, Yilma T, Osburn BI (1996) Phylogenetic comparison of the S3 gene of United States prototype strains of bluetongue virus with that of field isolates from California. J Virol 70:5735–5739

    PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:e214

    Article  Google Scholar 

  • Drummond AJ, Pybus OG, Rambaut A (2003) Inference of viral evolutionary rates from molecular sequences. Adv Parasitol 54:331–358

    Article  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PloS Biol 4:699–710

    Article  CAS  Google Scholar 

  • Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  Google Scholar 

  • Gould AR, Pritchard LI (1990) Relationships amongst bluetongue viruses revealed by comparisons of capsid and outer coat protein nucleotide sequences. Virus Res 17:31–52

    Article  CAS  PubMed  Google Scholar 

  • Hanada K, Suzuki Y, Gojobori T (2004) A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 21:1074–1080

    Article  CAS  PubMed  Google Scholar 

  • Heath L, van der Walt E, Varsani A, Martin DP (2006) Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80:11827–11832

    Article  CAS  PubMed  Google Scholar 

  • Holmes EC (2009) The evolution and emergence of RNA viruses. Oxford University Press, Oxford

    Google Scholar 

  • Jenkins GM, Rambaut A, Pybus OG, Holmes EC (2002) Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 2:156–165

    Article  Google Scholar 

  • Kowalik TF, Li JKK (1991) Bluetongue virus evolution: sequence analysis of the genomic S1 segments and major core protein VP7. Virol 181:749–755

    Article  CAS  Google Scholar 

  • Maan S, Maan NS, Samuel AR, Rao S, Attoui H, Mertens PP (2007) Analysis and phylogenetic comparisons of full-length VP2 genes of the 24 bluetongue virus serotypes. J Gen Virol 88:621–630

    Article  CAS  PubMed  Google Scholar 

  • Maan S, Maan NS, Ross-Smith N, Batten CA, Shaw AE, Anthony SJ, Samuel AR, Darpel KE, Veronesi E, Oura CA, Singh KP, Nomikou K, Potgieter AC, Attoui H, van Rooij E, van Rijn P, De Clercq K, Vandenbussche F, Zientara S, Breard E, Sailleau C, Beer M, Hoffman B, Mellor PS, Mertens PPC (2008) Sequence analysis of bluetongue virus serotype 8 from the Netherlands 2006 and comparison to other European strains. Virol 377:308–318

    Article  CAS  Google Scholar 

  • MacLachlan NJ (1994) The pathogenesis and immunology of bluetongue virus infection of ruminants. Comp Immunol Microbiol Infect Dis 17:197–206

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102

    Article  CAS  PubMed  Google Scholar 

  • Mellor PS, Wittmann EJ (2002) Bluetongue virus in the mediterranean basin 1998–2001. Vet J 164:20–37

    Article  CAS  PubMed  Google Scholar 

  • Mellor PS, Carpenter S, Harrup L, Baylis M, Mertens PP (2008) Bluetongue in Europe and the Mediterranean Basin: history of occurrence prior to 2006. Prev Vet Med 87:4–20

    Article  PubMed  Google Scholar 

  • Mertens PP, Pedley S, Cowley J, Burroughs JN, Corteyn AH, Jeggo MH, Jennings DM, Gorman BM (1989) Analysis of the roles of bluetongue virus outer capsid proteins VP2 and VP5 in determination of virus serotype. Virol 170:561–565

    Article  CAS  Google Scholar 

  • Mertens PP, Maan S, Samuel A, Attoui H (2005) Family Reoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy: Classification and nomenclature. Eighth report of the international committee on the taxonomy of viruses. Elsevier Academic Press, Oxford, pp 466–483

    Google Scholar 

  • Nomikou K, Dovas CI, Maan S, Anthony SJ, Samuel AR, Papanastassopoulou M, Maan NS, Mangana O, Mertens PP (2009) Evolution and phylogenetic analysis of full-length VP3 genes of Eastern Mediterranean bluetongue virus isolates. PloS ONE 4:e6437

    Article  PubMed  Google Scholar 

  • Oberst RD, Stott JL, Blanchard-Channell M, Osburn BI (1987) Genetic reassortment of bluetongue virus serotype 11 strains in the bovine. Vet Microbiol 15:11–18

    Article  CAS  PubMed  Google Scholar 

  • Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 8:239–246

    Article  CAS  PubMed  Google Scholar 

  • Parra GI, Bok K, Martinez M, Gomez JA (2004) Evidence of rotavirus intragenic recombination between two sublineages of the same genotype. J Gen Virol 85:1713–1716

    Article  CAS  PubMed  Google Scholar 

  • Pierce CM, Balasuriya UB, MacLachlan NJ (1998) Phylogenetic analysis of the S10 gene of field and laboratory strains of bluetongue virus from the United States. Virus Res 55:15–27

    Article  CAS  PubMed  Google Scholar 

  • Pond SLK, Frost SDW (2005a) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  PubMed  Google Scholar 

  • Pond SLK, Frost SDW (2005b) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    Article  CAS  PubMed  Google Scholar 

  • Pond SLK, Frost SDW (2005c) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222

    Article  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (2001) Selecting the best-fit model of nucleotide substitution. Syst Biol 50:580–601

    Article  CAS  PubMed  Google Scholar 

  • Pritchard LI, Gould AR, Wilson WC, Thompson L, Mertens PP, Wade-Evans AM (1995) Complete nucleotide sequence of RNA segment 3 of bluetongue virus serotype 2 (Ona-A). Phylogenetic analyses reveal the probable origin and relationship with other orbiviruses. Virus Res 35:247–261

    Article  CAS  PubMed  Google Scholar 

  • Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PP, Baylis M (2005) Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol 3:171–181

    Article  CAS  PubMed  Google Scholar 

  • Purse BV, Brown HE, Harrup L, Mertens PP, Rogers DJ (2008) Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes. Rev Sci Tech 27:427–442

    CAS  PubMed  Google Scholar 

  • Rambaut A (1996) Se-Al: sequence alignment editor. http://evolve.zoo.ox.ac.uk/

  • Ramig RF, Garrison C, Chen D, Bell-Robinson D (1989) Analysis of reassortment and superinfection during mixed infection of vero cells with bluetongue virus serotypes 10 and 17. J Gen Virol 70:2595–2603

    Article  PubMed  Google Scholar 

  • Saegerman C, Bolkaerts B, Baricalla C, Raes M, Wiggers L, de Leeuw I, Vandenbuscche F, Zimmer J-Y, Haubruge E, Cassart D, Clercq KD, Kirschvink N The impact of naturally-occurring, trans-placental bluetongue virus serotype-8 infection on reproductive performance in sheep. Veterin J. doi:10.1016/j.tvjl.2009.11.012 (in press)

  • Saegerman C, Berkvens D, Mellor PS (2008) Bluetongue epidemiology in the European Union. Emerg Infect Dis 14:539–544

    Article  PubMed  Google Scholar 

  • Schwartz-Cornil I, Mertens PP, Contreras V, Hemati B, Pascale F, Bréard E, Mellor PS, MacLachlan NJ, Zientara S (2008) Bluetongue virus: virology, pathogenesis and immunity. Vet Res 39:e46

    Article  Google Scholar 

  • Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9

    Article  CAS  PubMed  Google Scholar 

  • Slatkin M, Maddison WP (1989) A cladistic measure of gene flow measured from phylogenies of alleles. Genet 123:603–613

    CAS  Google Scholar 

  • Spreull J (1905) Malarial catarrhal fever (bluetongue) of sheep in South Africa. J Comp Pathol Ther 18:321–337

    Google Scholar 

  • Stott JL, Blanchard-Channell M, Stott ML, Barratt-Boyes SM, Maclachlan NJ (1992) Bluetongue virus tropism for bovine lymphocyte sub-populations. In: Walton TE, Osburn BI (eds) Bluetongue African Horse Sickness and related orbiviruses. CRC Press, Boca Raton, pp 781–787

    Google Scholar 

  • Swofford DL (2001) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Takamatsu H, Mellor PS, Mertens PP, Kirkham PA, Burroughs JN, Parkhouse RM (2003) A possible overwintering mechanism for bluetongue virus in the absence of the insect vector. J Gen Virol 84:227–235

    Article  CAS  PubMed  Google Scholar 

  • Wang TH, Donaldson YK, Brettle RP, Bell JE, Simmonds P (2001) Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J Virol 75:11686–11699

    Article  CAS  PubMed  Google Scholar 

  • Wilson A, Mellor P (2008) Bluetongue in Europe: vectors, epidemiology and climate change. Parasitol Res 103:S69–S77

    Article  PubMed  Google Scholar 

  • Wilson A, Darpel K, Mellor PSS (2008) Where does bluetongue virus sleep in the winter? PLoS Biol 6:e210

    Article  PubMed  Google Scholar 

  • Woelk CH, Holmes EC (2002) Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol 19:2333–2336

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. IASMA Research and Innovation Centre, Fondazione Edmund Mach, Environment and Natural Resources Area, S. Michele all’Adige, Trento, Italy

    Giovanna Carpi

  2. Department of Biology, Center for Infectious Disease Dynamics, The Pennsylvania State University, 609 Mueller Laboratory, University Park, PA, 16802, USA

    Edward C. Holmes & Andrew Kitchen

  3. Fogarty International Center, National Institutes of Health, Bethesda, MD, 20892, USA

    Edward C. Holmes

Authors
  1. Giovanna Carpi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edward C. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew Kitchen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew Kitchen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2776 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carpi, G., Holmes, E.C. & Kitchen, A. The Evolutionary Dynamics of Bluetongue Virus. J Mol Evol 70, 583–592 (2010). https://doi.org/10.1007/s00239-010-9354-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-010-9354-y

Keywords

Search

Navigation