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Volume 89, Issue 9

Phylogeographical structure and evolutionary history of two Buggy Creek virus lineages in the western Great Plains of North America Free

Abstract

Buggy Creek virus (BCRV) is an unusual arbovirus within the western equine encephalitis complex of alphaviruses. Associated with cimicid swallow bugs () as its vector and the cliff swallow () and house sparrow () as its amplifying hosts, this virus is found primarily in the western Great Plains of North America at spatially discrete swallow nesting colonies. For 342 isolates collected in Oklahoma, Nebraska, Colorado and North Dakota, from 1974 to 2007, we sequenced a 2076 bp region of the 26S subgenomic RNA structural glycoprotein coding region, and analysed phylogenetic relationships, rates of evolution, demographical histories and temporal genetic structure of the two BCRV lineages found in the Great Plains. The two lineages showed distinct phylogeographical structure: one lineage was found in the southern Great Plains and the other in the northern Great Plains, and both occurred in Nebraska and Colorado. Within each lineage, there was additional latitudinal division into three distinct sublineages. One lineage is showing a long-term population decline. In comparing sequences taken from the same sites 8–30 years apart, in one case one lineage had been replaced by the other, and in the other cases there was little evidence of the same haplotypes persisting over time. The evolutionary rate of BCRV is in the order of 1.6–3.6×10 substitutions per site per year, similar to that estimated for other temperate-latitude alphaviruses. The phylogeography and evolution of BCRV could be better understood once we determine the nature of the ecological differences between the lineages.

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2008-09-01
2024-04-19
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References

  1. Anonymous 2006; Kansas Drought Report; 2006 Report No. 4 Topeka, KS: Kansas Water Office;
     [Google Scholar]
  2. Brault A. C., Powers A. M., Villarreal C. L., Lopez R. N., Cachon M. F., Gutierrez L. F. L., Kang W., Tesh R. B., Shope R. E., Weaver S. C. 1999; Genetic and antigenic diversity among eastern equine encephalitis viruses from North, Central, and South America. Am J Trop Med Hyg 61:579–586
     [Google Scholar]
  3. Brault A. C., Powers A. M., Weaver S. C. 2002; Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J Virol 76:6387–6392 [CrossRef]
     [Google Scholar]
  4. Brown C. R., Brown M. B. 1995; Cliff swallow ( Hirundo pyrrhonota . In Birds of North America no 149Edited by Poole A., Gill F. Philadelphia, PA: Academy of Natural Sciences and; Washington DC: The American Ornithologists'; Union:
     [Google Scholar]
  5. Brown C. R., Brown M. B. 1996 Coloniality in the Cliff Swallow: the Effect of Group Size on Social Behavior Chicago: University of Chicago Press;
     [Google Scholar]
  6. Brown C. R., Brown M. B. 2004; Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85:1619–1626 [CrossRef]
     [Google Scholar]
  7. Brown C. R., Brown M. B. 2005; Between-group transmission dynamics of the swallow bug, Oeciacus vicarius . J Vector Ecol 30:137–143
     [Google Scholar]
  8. Brown C. R., Komar N., Quick S. B., Sethi R. A., Panella N. A., Brown M. B., Pfeffer M. 2001; Arbovirus infection increases with group size. Proc R Soc Lond B 268:1833–1840 [CrossRef]
     [Google Scholar]
  9. Brown C. R., Brown M. B., Moore A. T., Komar N. 2007; Bird movement predicts Buggy Creek virus infection in insect vectors. Vector Borne Zoonotic Dis 7:304–314 [CrossRef]
     [Google Scholar]
  10. Brown C. R., Brown M. B., Padhi A., Foster J. E., Pfeffer M., Moore A. T., Komar N. 2008; Host and vector movement affects genetic diversity and spatial structure of Buggy Creek virus (Togaviridae).. Mol Ecol 17:2164–2173 [CrossRef]
     [Google Scholar]
  11. Calisher C. H., Monath T. P., Muth D. J., Lazuick J. S., Trent D. W., Francy D. B., Kemp G. E., Chandler F. W. 1980; Characterization of Fort Morgan virus, an alphavirus of the western equine encephalitis virus complex in an unusual ecosystem. Am J Trop Med Hyg 29:1428–1440
     [Google Scholar]
  12. Cilnis M. J., Kang W., Weaver S. C. 1996; Genetic conservation of Highlands J viruses. Virology 218:343–351 [CrossRef]
     [Google Scholar]
  13. Cooper L. A., Scott T. W. 2001; Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157:1403–1412
     [Google Scholar]
  14. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [CrossRef]
     [Google Scholar]
  15. 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
     [Google Scholar]
  16. Drummond A. J., Rambaut A., Shapiro B., Pybus O. G. 2005; Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192 [CrossRef]
     [Google Scholar]
  17. Drummond A. J., Ho S. Y. W., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88 [CrossRef]
     [Google Scholar]
  18. Hayes R. O., Francy D. B., Lazuick J. S., Smith G. C., Gibbs E. P. J. 1977; Role of the cliff swallow bug ( Oeciacus vicarius ) in the natural cycle of a western equine encephalitis-related alphavirus. J Med Entomol 14:257–262 [CrossRef]
     [Google Scholar]
  19. Holmes E. C. 2004; The phylogeography of human viruses. Mol Ecol 13:745–756 [CrossRef]
     [Google Scholar]
  20. Hopla C. E., Francy D. B., Calisher C. H., Lazuick J. S. 1993; Relationship of cliff swallows, ectoparasites, and an alphavirus in west-central Oklahoma. J Med Entomol 30:267–272 [CrossRef]
     [Google Scholar]
  21. Huelsenbeck J. P., Ronquist F. 2001; mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755 [CrossRef]
     [Google Scholar]
  22. 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 [CrossRef]
     [Google Scholar]
  23. Kitchen A., Miyamoto M. M., Mulligan C. J. 2008; Utility of DNA viruses for studying human host history: case study of JC virus. Mol Phylogenet Evol 46:673–682 [CrossRef]
     [Google Scholar]
  24. Kondig J. P., Turell M. J., Lee J. S., O'Guinn M. L., Wasieloski L. P. Jr 2007; Genetic analysis of South American eastern equine encephalomyelitis viruses isolated from mosquitoes collected in the Amazon basin region of Peru. Am J Trop Med Hyg 76:408–416
     [Google Scholar]
  25. Kramer L. D., Fallah H. M. 1999; Genetic variation among isolates of western equine encephalomyelitis virus from California. Am J Trop Med Hyg 60:708–713
     [Google Scholar]
  26. Lindsay M. D. A., Coelen R. J., Mackenzie J. S. 1993; Genetic heterogeneity among isolates of Ross River virus from different geographical regions. J Virol 67:3576–3585
     [Google Scholar]
  27. Lowther P. E., Cink C. L. 1992; House sparrow. In Birds of North America no 12Edited by Poole A., Stettenheim P., Gill F. Philadelphia, PA: Academy of Natural Sciences and; Washington, DC: The American Ornithologists'; Union:
     [Google Scholar]
  28. Moore A. T., Edwards E. A., Brown M. B., Komar N., Brown C. R. 2007; Ecological correlates of Buggy Creek virus infection in Oeciacus vicarius , southwestern Nebraska, 2004. J Med Entomol 44:42–49 [CrossRef]
     [Google Scholar]
  29. Moratorio G., Costa-Mattioli M., Piovani R., Romero H., Musto H., Cristina J. 2007; Bayesian coalescent inference of hepatitis A virus populations: evolutionary rates and patterns. J Gen Virol 88:3039–3042 [CrossRef]
     [Google Scholar]
  30. Moya A., Holmes E. C., Gonzalez-Candelas F. 2004; The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol 2:279–288 [CrossRef]
     [Google Scholar]
  31. Nagata L. P., Hu W.-G., Parker M., Chau D., Rayner G. A., Schmaltz F. L., Wong J. P. 2006; Infectivity variation and genetic diversity among strains of western equine encephalitis virus. J Gen Virol 87:2353–2361 [CrossRef]
     [Google Scholar]
  32. Navaratnarajah C. K., Kuhn R. J. 2007; Functional characterization of the Sindbis virus E2 glycoprotein by transposon linker-insertion mutagenesis. Virology 363:134–147 [CrossRef]
     [Google Scholar]
  33. Norder H., Lundström J. O., Kozuch O., Magnius L. O. 1996; Genetic relatedness of Sindbis virus strains from Europe, the Middle East, and Africa. Virology 222:440–445 [CrossRef]
     [Google Scholar]
  34. Oberste M. S., Weaver S. C., Watts D. M., Smith J. F. 1998; Identification and genetic analysis of Panama-genotype Venezuelan equine encephalitis virus subtype ID in Peru. Am J Trop Med Hyg 58:41–46
     [Google Scholar]
  35. Pfeffer M., Foster J. E., Edwards E. A., Brown M. B., Komar N., Brown C. R. 2006; Phylogenetic analysis of Buggy Creek virus: evidence for multiple clades in the western Great Plains, United States of America. Appl Environ Microbiol 72:6886–6893 [CrossRef]
     [Google Scholar]
  36. Poidinger M., Roy S., Hall R. A., Turley P. J., Scherret J. H., Lindsay M. D., Broom A. K., Mackenzie J. S. 1997; Genetic stability among temporally and geographically diverse isolates of Barmah Forest virus. Am J Trop Med Hyg 57:230–234
     [Google Scholar]
  37. Posada D. 2004; Collapse: Describing Haplotypes from Sequence Alignments . Version 1.2. Vigo, Spain: University of Vigo; Available from http://darwin.uvigo.es/software/collapse.html
  38. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [CrossRef]
     [Google Scholar]
  39. Powers A. M., Brault A. C., Tesh R. B., Weaver S. C. 2000; Re-emergence of chikungunya and o'nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 81:471–479
     [Google Scholar]
  40. Powers A. M., Brault A. C., Shirako Y., Strauss E. G., Kang W., Strauss J. H., Weaver S. C. 2001; Evolutionary relationships and systematics of the alphaviruses. J Virol 75:10118–10131 [CrossRef]
     [Google Scholar]
  41. Rambaut A., Drummond A. J. 2007; Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer
  42. Rannala B. H. 1995; Demography and genetic structure in island populations . PhD thesis New Haven, Connecticut: Yale University;
  43. Reisen W. K., Monath T. P. 1989; Western equine encephalomyelitis. In The Arboviruses, Epidemiology and Ecology vol. 5 pp 89–137Edited by Monath T. P. Boca Raton, FL: CRC Press;
     [Google Scholar]
  44. Romano C. M., de Melo F. L., Corsini M. A. B., Holmes E. C., Zanotto P. M. A. 2007; Demographic histories of ERV-K in humans, chimpanzees and rhesus monkeys. PLOS One 2:e1026 [CrossRef]
     [Google Scholar]
  45. Sammels L. M., Lindsay M. D., Poidinger M., Coelen R. J., Mackenzie J. S. 1999; Geographic distribution and evolution of Sindbis virus in Australia. J Gen Virol 80:739–748
     [Google Scholar]
  46. Sauchyn D. J., Stroich J., Beriault A. 2003; A paleoclimatic context for the drought of 1999–2001 in the northern Great Plains of North America. Geogr J 169:158–167 [CrossRef]
     [Google Scholar]
  47. Scott T. W., Bowen G. S., Monath T. P. 1984; A field study on the effects of Fort Morgan virus, an arbovirus transmitted by swallow bugs, on the reproductive success of cliff swallows and symbiotic house sparrows in Morgan County. Colorado: 1976 Am J Trop Med Hyg 33:981–991
     [Google Scholar]
  48. Smith G. C., Eads R. B. 1978; Field observations on the cliff swallow, Petrochelidon pyrrhonota (Vieillot), and the swallow bug, Oeciacus vicarius Horvath. J Wash Acad Sci 68:23–26
     [Google Scholar]
  49. Strauss J. H., Strauss E. G. 1994; The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491–562
     [Google Scholar]
  50. Strickler S. A. 2006 Winter ecology of a bird-associated arbovirus . MSc thesis Tulsa, OK: University of Tulsa;
     [Google Scholar]
  51. Swofford D. L. 2002 paup*: phylogenetic analysis using parsimony (*and other methods), version 4 Sunderland, MA: Sinauer Associates;
     [Google Scholar]
  52. 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 [CrossRef]
     [Google Scholar]
  53. Weaver S. C., Rico-Hesse R., Scott T. W. 1992; Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Top Microbiol Immunol 176:99–117
     [Google Scholar]
  54. Weaver S. C., Bellew L. A., Gousset L., Repik P. M., Scott T. W., Holland J. J. 1993; Diversity within natural populations of eastern equine encephalomyelitis virus. Virology 195:700–709 [CrossRef]
     [Google Scholar]
  55. Weaver S. C., Hagenbaugh A., Bellew L. A., Gousset L., Mallampalli V., Holland J. J., Scott T. W. 1994; Evolution of alphaviruses in the eastern equine encephalomyelitis complex. J Virol 68:158–169
     [Google Scholar]
  56. Weaver S. C., Kang W., Shirako Y., Rumenapf T., Strauss E. G., Strauss J. H. 1997; Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses. J Virol 71:613–623
     [Google Scholar]
  57. Weaver S. C., Brault A. C., Kang W., Holland J. J. 1999; Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73:4316–4326
     [Google Scholar]
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Phylogeographical structure and evolutionary history of two Buggy Creek virus lineages in the western Great Plains of North America
J. Gen. Virol. 89, 2122 (2008); https://doi.org/10.1099/vir.0.2008/001719-0
/content/journal/jgv/10.1099/vir.0.2008/001719-0
/content/journal/jgv/10.1099/vir.0.2008/001719-0
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