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PMID: 15626758 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

High rate of viral evolution associated with the emergence of carnivore parvovirus.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 102 ·No. 2 ·2005-01-11 ·Pages 379-84

Shackelton LA, Parrish CR, Truyen U, Holmes EC

Abstract

Canine parvovirus (CPV) is an emerging DNA virus that was first observed to cause disease in canines in 1978 and has since become a ubiquitous pathogen worldwide. CPV emerged from feline panleukopenia parvovirus (FPLV) or a closely related virus, differing at several key amino acid residues. Here we characterize the evolutionary processes underlying the emergence of CPV. Although FPLV has remained an endemic infection in its host populations, we show that, since the 1970s, the newly emerged CPV has undergone an epidemic-like pattern of logistic/exponential growth, effectively doubling its population size every few years. This rapid population growth was associated with a lineage of CPV that acquired a broader host range and greater infectivity. Recombination played no role in the emergence of CPV. Rather, any preexisting variation in the donor species and the subsequent rapid adaptation of the virus to canines were likely dependent on a high rate of mutation and the positive selection of mutations in the major capsid gene. Strikingly, although these single-stranded viruses have a DNA genome and use cellular replication machinery, their rate of nucleotide substitution is closer to that of RNA viruses than to that of double-stranded DNA viruses.

MeSH Terms
Animals Base Sequence Biological Evolution Dogs Molecular Sequence Data Parvovirus, Canine/classification,genetics Phylogeny Selection, Genetic
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Shackelton Laura A
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom.
Parrish Colin R
Truyen Uwe
Holmes Edward C
References (39)
39 references, click to expand
  1. Host range relationships and the evolution of canine parvovirus.
    Vet Microbiol. 1999 Sep 1;69(1-2):29-40 PMID: 10515266
  2. Genetic variability of natural populations of cotton leaf curl geminivirus, a single-stranded DNA virus
    J Mol Evol. 1999 Nov;49(5):672-81 PMID: 10552048
  3. Genetic characterization of feline parvovirus sequences from various carnivores.
    J Gen Virol. 2000 Feb;81(Pt 2):345-50 PMID: 10644832
  4. Evolution of human polyomavirus JC.
    J Gen Virol. 2000 May;81(Pt 5):1191-200 PMID: 10769060
  5. Codon-substitution models for heterogeneous selection pressure at amino acid sites.
    Genetics. 2000 May;155(1):431-49 PMID: 10790415
  6. Predominance of canine parvovirus (CPV) in unvaccinated cat populations and emergence of new antigenic types of CPVs in cats.
    Virology. 2000 Dec 5;278(1):13-9 PMID: 11112475
  7. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis.
    J Mol Evol. 2002 Feb;54(2):156-65 PMID: 11821909
  8. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor.
    J Virol. 2003 Feb;77(3):1718-26 PMID: 12525605
  9. Evidence for specificity of psittacine beak and feather disease viruses among avian hosts.
    Virology. 2003 Feb 1;306(1):109-15 PMID: 12620803
  10. Residues in the apical domain of the feline and canine transferrin receptors control host-specific binding and cell infection of canine and feline parvoviruses.
    J Virol. 2003 Aug;77(16):8915-23 PMID: 12885908
  11. B19 virus genome diversity: epidemiological and clinical correlations.
    J Clin Virol. 2003 Sep;28(1):1-13 PMID: 12927746
  12. Parvovirus host range, cell tropism and evolution.
    Curr Opin Microbiol. 2003 Aug;6(4):392-8 PMID: 12941411
  13. Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses.
    J Virol. 2003 Sep;77(18):10099-105 PMID: 12941920
  14. The small non-structural protein NS2 of the autonomous parvovirus minute virus of mice is required for virus growth in murine cells.
    J Gen Virol. 1992 Jul;73 ( Pt 7):1839-43 PMID: 1385828
  15. Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants.
    J Virol. 2003 Nov;77(22):12211-21 PMID: 14581558
  16. The role of evolution in the emergence of infectious diseases.
    Nature. 2003 Dec 11;426(6967):658-61 PMID: 14668863
  17. Mosaic evolution of the severe acute respiratory syndrome coronavirus.
    J Virol. 2004 Jan;78(1):76-82 PMID: 14671089
  18. Inference of viral evolutionary rates from molecular sequences.
    Adv Parasitol. 2003;54:331-58 PMID: 14711090
  19. Human circoviruses.
    Vet Microbiol. 2004 Feb 4;98(2):95-101 PMID: 14741121
  20. Viral evolution and the emergence of SARS coronavirus.
    Philos Trans R Soc Lond B Biol Sci. 2004 Jul 29;359(1447):1059-65 PMID: 15306390
  21. A constant rate of spontaneous mutation in DNA-based microbes.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160-4 PMID: 1831267
  22. Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus.
    J Virol. 1991 Dec;65(12):6544-52 PMID: 1942246
  23. The small nonstructural protein (NS2) of the parvovirus minute virus of mice is required for efficient DNA replication and infectious virus production in a cell-type-specific manner.
    J Virol. 1990 Dec;64(12):6166-75 PMID: 2147041
  24. Emergence, natural history, and variation of canine, mink, and feline parvoviruses.
    Adv Virus Res. 1990;38:403-50 PMID: 2171302
  25. Statistical tests for detecting gene conversion.
    Mol Biol Evol. 1989 Sep;6(5):526-38 PMID: 2677599
  26. Presence of antibody cross-reacting with canine parvovirus in the sera of dogs from Greece.
    Vet Rec. 1986 Mar 22;118(12):332-3 PMID: 3705371
  27. Characterization of the feline host range and a specific epitope of feline panleukopenia virus.
    Virology. 1994 May 1;200(2):494-503 PMID: 7513918
  28. Evolution of the feline-subgroup parvoviruses and the control of canine host range in vivo.
    J Virol. 1995 Aug;69(8):4702-10 PMID: 7609035
  29. Pathogenesis of feline panleukopenia virus and canine parvovirus.
    Baillieres Clin Haematol. 1995 Mar;8(1):57-71 PMID: 7663051
  30. Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses.
    J Mol Biol. 1995 Mar 31;247(3):443-58 PMID: 7714900
  31. Coevolution of papillomaviruses with human populations.
    Trends Microbiol. 1994 Apr;2(4):140-3 PMID: 8012758
  32. 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. 1994 Mar;75 ( Pt 3):513-27 PMID: 8126449
  33. Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid.
    Virology. 1994 Jan;198(1):175-84 PMID: 8259653
  34. Evolution of canine parvovirus involved loss and gain of feline host range.
    Virology. 1996 Jan 15;215(2):186-9 PMID: 8560765
  35. The NS2 polypeptide of parvovirus MVM is required for capsid assembly in murine cells.
    Virology. 1997 May 12;231(2):267-80 PMID: 9168889
  36. Long term trends in the evolution of H(3) HA1 human influenza type A.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7712-8 PMID: 9223253
  37. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  38. Nonstructural protein-2 and the replication of canine parvovirus.
    Virology. 1998 Jan 20;240(2):273-81 PMID: 9454701
  39. Differences in the evolutionary pattern of feline panleukopenia virus and canine parvovirus.
    Virology. 1998 Sep 30;249(2):440-52 PMID: 9791034
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.0406765102
Published
2005-01-11
Epub
2004-00-30
Pages
379-84
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC544290
Subset
IM
Grants
NIAID NIH HHS · R01 AI028385 · United States
NIAID NIH HHS · R01AI028385 · United States
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External Links
PubMed source DOI: 10.1073/pnas.0406765102 PMC Full Text View journal details
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