1887

Abstract

To elucidate the spatiotemporal phylodynamics, dispersion and evolutionary processes underlying the emergence of novel porcine parvovirus 2 (PPV2), PPV3 and PPV4 species, we analysed all available complete capsid genes, together with ours, obtained in Europe. Bayesian phylogeography indicates that Romania (PPV2 and PPV4) and Croatia (PPV3) are the most likely ancestral areas from which PPVs have subsequently spread to other European countries and regions. The timescale of our reconstruction supported a relatively recent history of the currently circulating novel PPV species (1920s to 1980s) in the domestic or sylvatic host. While PPV2 strains exhibited a large genetic exchange characterized by significant recombination and gene flow between distinct regions and hosts, PPV3 and PPV4 showed a diversification reflected by the accumulation of geographically structured polymorphisms. The RNA-like evolutionary rates detected inter- and intrahost recombination and the positive selection sites provided evidence that the PPV2–4 capsid gene plays a prominent role in host adaptation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.055129-0
2013-10-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/10/2330.html?itemId=/content/journal/jgv/10.1099/vir.0.055129-0&mimeType=html&fmt=ahah

References

  1. Bielejec F., Rambaut A., Suchard M. A., Lemey P.. ( 2011;). SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. . Bioinformatics 27:, 2910–2912. [CrossRef][PubMed]
    [Google Scholar]
  2. Cadar D., Cságola A., Lorincz M., Tombácz K., Spînu M., Tuboly T.. ( 2011;). Distribution and genetic diversity of porcine hokovirus in wild boars. . Arch Virol 156:, 2233–2239. [CrossRef][PubMed]
    [Google Scholar]
  3. Cadar D., Dán A., Tombácz K., Lőrincz M., Kiss T., Becskei Z., Spînu M., Tuboly T., Cságola A.. ( 2012;). Phylogeny and evolutionary genetics of porcine parvovirus in wild boars. . Infect Genet Evol 12:, 1163–1171. [CrossRef][PubMed]
    [Google Scholar]
  4. Cadar D., Cságola A., Kiss T., Tuboly T.. ( 2013;). Capsid protein evolution and comparative phylogeny of novel porcine parvoviruses. . Mol Phylogenet Evol 66:, 243–253. [CrossRef][PubMed]
    [Google Scholar]
  5. Cheung A. K., Wu G., Wang D., Bayles D. O., Lager K. M., Vincent A. L.. ( 2010;). Identification and molecular cloning of a novel porcine parvovirus. . Arch Virol 155:, 801–806. [CrossRef][PubMed]
    [Google Scholar]
  6. Cságola A., Lőrincz M., Cadar D., Tombácz K., Biksi I., Tuboly T.. ( 2012;). Detection, prevalence and analysis of emerging porcine parvovirus infections. . Arch Virol 157:, 1003–1010. [CrossRef][PubMed]
    [Google Scholar]
  7. Drummond A. J., Rambaut A.. ( 2007;). BEAST: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef][PubMed]
    [Google Scholar]
  8. 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][PubMed]
    [Google Scholar]
  9. Duffy S., Holmes E. C.. ( 2008;). Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. . J Virol 82:, 957–965. [CrossRef][PubMed]
    [Google Scholar]
  10. 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. [CrossRef][PubMed]
    [Google Scholar]
  11. Hijikata M., Abe K., Win K. M., Shimizu Y. K., Keicho N., Yoshikura H.. ( 2001;). Identification of new parvovirus DNA sequence in swine sera from Myanmar. . Jpn J Infect Dis 54:, 244–245.[PubMed]
    [Google Scholar]
  12. Hoelzer K., Shackelton L. A., Parrish C. R., Holmes E. C.. ( 2008;). Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. . J Gen Virol 89:, 2280–2289. [CrossRef][PubMed]
    [Google Scholar]
  13. Huang L., Zhai S. L., Cheung A. K., Zhang H. B., Long J. X., Yuan S. S.. ( 2010;). Detection of a novel porcine parvovirus, PPV4, in Chinese swine herds. . Virol J 7:, 333. [CrossRef][PubMed]
    [Google Scholar]
  14. Huson D. H., Bryant D.. ( 2006;). Application of phylogenetic networks in evolutionary studies. . Mol Biol Evol 23:, 254–267. [CrossRef][PubMed]
    [Google Scholar]
  15. Jobb G., von Haeseler A., Strimmer K.. ( 2004;). treefinder: a powerful graphical analysis environment for molecular phylogenetics. . BMC Evol Biol 4:, 18. [CrossRef][PubMed]
    [Google Scholar]
  16. Kosakovsky Pond S. L., Frost S. D.. ( 2005;). Not so different after all: a comparison of methods for detecting amino acid sites under selection. . Mol Biol Evol 22:, 1208–1222. [CrossRef][PubMed]
    [Google Scholar]
  17. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D.. ( 2006;). Automated phylogenetic detection of recombination using a genetic algorithm. . Mol Biol Evol 23:, 1891–1901. [CrossRef][PubMed]
    [Google Scholar]
  18. Lau S. K., Woo P. C., Tse H., Fu C. T., Au W. K., Chen X. C., Tsoi H. W., Tsang T. H., Chan J. S.. & other authors ( 2008;). Identification of novel porcine and bovine parvoviruses closely related to human parvovirus 4. . J Gen Virol 89:, 1840–1848. [CrossRef][PubMed]
    [Google Scholar]
  19. Lemey P., Rambaut A., Drummond A. J., Suchard M. A.. ( 2009;). Bayesian phylogeography finds its roots. . PLOS Comput Biol 5:, e1000520. [CrossRef][PubMed]
    [Google Scholar]
  20. Li S., Wei Y., Liu J., Tang Q., Liu C.. ( 2013;). Prevalence of porcine hokovirus and its co-infection with porcine circovirus 2 in China. . Arch Virol. [CrossRef][PubMed]
    [Google Scholar]
  21. 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. [CrossRef][PubMed]
    [Google Scholar]
  22. Murrell B., Wertheim J. O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S. L.. ( 2012;). Detecting individual sites subject to episodic diversifying selection. . PLoS Genet 8:, e1002764. [CrossRef][PubMed]
    [Google Scholar]
  23. Murrell B., Moola S., Mabona A., Weighill T., Sheward D., Kosakovsky Pond S. L., Scheffler K.. ( 2013;). fubar: a fast, unconstrained bayesian approximation for inferring selection. . Mol Biol Evol 30:, 1196–1205. [CrossRef][PubMed]
    [Google Scholar]
  24. Ndze V. N., Cadar D., Cságola A., Kisfali P., Kovács E., Farkas S., Ngu A. F., Esona M. D., Dán A.. & other authors ( 2013;). Detection of novel porcine bocaviruses in fecal samples of asymptomatic pigs in Cameroon. . Infect Genet Evol 17:, 277–282. [CrossRef][PubMed]
    [Google Scholar]
  25. Opriessnig T., Xiao C. T., Gerber P. F., Halbur P. G.. ( 2013;). Emergence of a novel mutant PCV2b variant associated with clinical PCVAD in two vaccinated pig farms in the U.S. concurrently infected with PPV2. . Vet Microbiol 163:, 177–183. [CrossRef][PubMed]
    [Google Scholar]
  26. Parker J., Rambaut A., Pybus O. G.. ( 2008;). Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. . Infect Genet Evol 8:, 239–246. [CrossRef][PubMed]
    [Google Scholar]
  27. Parrish C. R., Kawaoka Y.. ( 2005;). The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. . Annu Rev Microbiol 59:, 553–586. [CrossRef][PubMed]
    [Google Scholar]
  28. 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. [CrossRef][PubMed]
    [Google Scholar]
  29. Streck A. F., Bonatto S. L., Homeier T., Souza C. K., Gonçalves K. R., Gava D., Canal C. W., Truyen U.. ( 2011;). High rate of viral evolution in the capsid protein of porcine parvovirus. . J Gen Virol 92:, 2628–2636. [CrossRef][PubMed]
    [Google Scholar]
  30. Szelei J., Liu K., Li Y., Fernandes S., Tijssen P.. ( 2010;). Parvovirus 4-like virus in blood products. . Emerg Infect Dis 16:, 561–564. [CrossRef][PubMed]
    [Google Scholar]
  31. Tse H., Tsoi H. W., Teng J. L., Chen X. C., Liu H., Zhou B., Zheng B. J., Woo P. C., Lau S. K., Yuen K. Y.. ( 2011;). Discovery and genomic characterization of a novel ovine partetravirus and a new genotype of bovine partetravirus. . PLoS ONE 6:, e25619. [CrossRef][PubMed]
    [Google Scholar]
  32. Wang F., Wei Y., Zhu C., Huang X., Xu Y., Yu L., Yu X.. ( 2010;). Novel parvovirus sublineage in the family of Parvoviridae. . Virus Genes 41:, 305–308. [CrossRef][PubMed]
    [Google Scholar]
  33. Xiao C. T., Giménez-Lirola L. G., Halbur P. G., Opriessnig T.. ( 2012;). Increasing porcine PARV4 prevalence with pig age in the U.S. pig population. . Vet Microbiol 160:, 290–296. [CrossRef][PubMed]
    [Google Scholar]
  34. Xiao C. T., Gerber P. F., Giménez-Lirola L. G., Halbur P. G., Opriessnig T.. ( 2013a;). Characterization of porcine parvovirus type 2 (PPV2) which is highly prevalent in the USA. . Vet Microbiol 161:, 325–330. [CrossRef][PubMed]
    [Google Scholar]
  35. Xiao C. T., Halbur P. G., Opriessnig T.. ( 2013b;). Molecular evolutionary genetic analysis of emerging parvoviruses identified in pigs. . Infect Genet Evol 16:, 369–376. [CrossRef][PubMed]
    [Google Scholar]
  36. Zhang H. B., Huang L., Liu Y. J., Lin T., Sun C. Q., Deng Y., Wei Z. Z., Cheung A. K., Long J. X., Yuan S. S.. ( 2011;). Porcine bocaviruses: genetic analysis and prevalence in Chinese swine population. . Epidemiol Infect 139:, 1581–1586. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.055129-0
Loading
/content/journal/jgv/10.1099/vir.0.055129-0
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