JC virus (JCV) is a double-stranded DNA polyomavirus co-evolving with humans since the time of their origin in Africa. JCV seems to provide new insights into the history of human populations, as it suggests an expansion of humans from Africa via two distinct migrations, each carrying a different lineage of the virus. A possible alternative to this interpretation could be that the divergence between the two lineages is due to selective pressures favouring adaptation of JCV to different climates, thus making any inference about human history debatable. In the present study, the evolution of JCV was investigated by applying correspondence analysis to a set of 273 fully sequenced strains. The first and more important axis of ordination led to the detection of 61 nt positions as the main determinants of the divergence between the two virus lineages. One lineage includes strains of types 1 and 4, the other strains of types 2, 3, 7 and 8. The distinctiveness of the Caucasian lineage (types 1 and 4), largely diffused in the northern areas of the world, was almost entirely ascribed to synonymous substitutions. The findings provided by the subsequent axes of ordination supported the view of an evolutionary history of JCV characterized by genetic drift and migration, rather than by natural selection. Correspondence analysis was also applied to a set of 156 human mitochondrial genome sequences. A detailed comparison between the substitution patterns in JCV and mitochondria brought to light some relevant advantages of the use of the virus in tracing human migrations.
AgostiniH. T.,
YanagiharaR.,
DavisV.,
RyschkewitschC. F.,
StonerG. L.1997a; Asian genotypes of JC virus in Native Americans and in a Pacific Island population: markers of viral evolution and human migration. Proc Natl Acad Sci U S A 94:14542–14546[CrossRef]
AgostiniH. T.,
RyschkewitschC. F.,
BrubakerG. R.,
ShaoJ.,
StonerG. L.1997b; Five complete genomes of JC virus type 3 from Africans and African Americans. Arch Virol 142:637–655[CrossRef]
AgostiniH. T.,
RyschkewitschC. F.,
SingerE. J.,
StonerG. L.1997c; JC virus regulatory region rearrangements and genotypes in progressive multifocal leukoencephalopathy: two independent aspects of virus variation. J Gen Virol 78:659–664
AgostiniH. T.,
JobesD. V.,
StonerG. L.2001b; Molecular evolution and epidemiology of JC virus. In Human Polyomavirus: Molecular and Clinical Perspectives pp 491–526 Edited by
KhaliliK.,
StonerG. L.
New York, NY: Wiley-Liss Inc;
BannaiM.,
OhashiJ.,
HariharaS.,
TakahashiY.,
JujiT.,
OmotoK.,
TokunagaK.2000; Analysis of HLA genes and haplotypes in Ainu (from Hokkaido, northern Japan) supports the premise that they descent from Upper Paleolithic populations of East Asia. Tissue Antigens 55:128–139[CrossRef]
Cavalli-SforzaL. L.,
MenozziP.,
PiazzaA.1994; Genetic history of world populations. In The History and Geography of Human Genes pp 60–157 NJ: Princeton University Press;
ChimaS. C.,
RyschkewitschC. F.,
StonerG. L.1998; Molecular epidemiology of human polyomavirus JC in the Biaka Pygmies and Bantu of Central Africa. Mem Inst Oswaldo Cruz 93:615–623[CrossRef]
CuiX.,
WangJ. C.,
DeckhutA.,
JosephB. C.,
EberweinP.,
CubittC. L.,
RyschkewitschC. F.,
AgostiniH. T.,
StonerG. L.2004; Chinese strains (Type 7) of JC virus are Afro-Asiatic in origin but are phylogenetically distinct from the Mongolian and Indian strains (Type 2D) and the Korean and Japanese strains (Type 2A). J Mol Evol 58:568–583[CrossRef]
Fernandez-CoboM.,
AgostiniH. T.,
BritezG.,
RyschkewitschC. F.,
StonerG. L.2002; Strains of JC virus in Amerind-speakers of North America (Salish) and South America (Guaraní), Na-Dene-speakers of New Mexico (Navajo), and modern Japanese suggest links through an ancestral Asian population. Am J Phys Anthropol 118:154–168[CrossRef]
GuoJ.,
KitamuraT.,
EbiharaH.9 other authors1996; Geographical distribution of the human polyomavirus JC virus types A and B and isolation of a new type from Ghana. J Gen Virol 77:919–927[CrossRef]
HoL.,
ChanS. Y.,
BurkR. D.19 other authors1993; The genetic drift of human papillomavirus type 16 is a means of reconstructing prehistoric viral spread and the movement of ancient human populations. J Virol 67:6413–6423
IngmanM.,
GyllenstenU.2003; Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigenes. Genome Res 13:1600–1606[CrossRef]
JobesD. V.,
FriedlaenderJ. S.,
MgoneC. S.7 other authors2001; New JC virus (JCV) genotypes from Papua New Guinea and Micronesia (Type 8 and Type 2E) and evolutionary analysis of 32 complete JCV genomes. Arch Virol 146:2097–2113[CrossRef]
KatoA.,
KitamuraT.,
SugimotoC.,
OgawaY.,
NakazatoK.,
NagashimaK.,
HallW. W.,
KawabeK.,
YogoY.1997; Lack of evidence for the transmission of JC polyomavirus between human populations. Arch Virol 142:875–882[CrossRef]
KatoA.,
SugimotoC.,
ZhengH. Y.,
KitamuraT.,
YogoY.2000; Lack of disease-specific amino acid changes in the viral proteins of JC virus isolates from the brain with progressive multifocal leukoencephalopathy. Arch Virol 145:2173–2182[CrossRef]
KunitakeT.,
KitamuraT.,
GuoJ.,
TaguchiF.,
KawabeK.,
YogoY.1995; Parent-to-child transmission is relatively common in the spread of the human polyomavirus JC. J Clin Microbiol 33:1448–1451
LebartL.,
MorineauA.,
WarwickK. A.1984Multivariate Descriptive Statistical Analysis. Correspondence Analysis and Related Techniques for Large Matrices New York: Wiley & Sons;
MirandaJ. J.,
TakasakaT.,
ZhengH.-Y.,
KitamuraT.,
YogoY.2004; JC virus genotype profile in the Mamanwa, a Philippine Negrito tribe, and implications for its population history. Anthropol Sci 112:173–178[CrossRef]
MishmarD.,
Ruiz-PesiniE.,
GolikP.10 other authors2003; Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci U S A 100:171–176[CrossRef]
MiuraT.,
FukunagaT.,
IgarashiT.17 other authors1994; Phylogenetic subtypes of human T-lymphotropic virus type I and their relations to the anthropological background. Proc Natl Acad Sci U S A 91:1124–1127[CrossRef]
OngC. K.,
ChanS. Y.,
CampoM. S.8 other authors1993; Evolution of human papillomavirus type 18: an ancient phylogenetic root in Africa and intratype diversity reflect coevolution with human ethnic groups. J Virol 67:6424–6431
PadgettB. L.,
WalkerD. L.1973; Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive leukoencephalopathy. J Infect Dis 127:467–470[CrossRef]
SalemiM.,
VandammeA. M.,
DesmyterJ.,
CasoliC.,
BertazzoniU.1999; The origin and evolution of human T-cell lymphotropic virus type II (HTLV-II) and the relationship with its replication strategy. Gene 234:11–21[CrossRef]
SaruwatariL.,
SugimotoC.,
KitamuraT.12 other authors2002; Asian domains of four major genotypes of JC virus, Af2, B1-b, CY and SC. Arch Virol 147:1–10[CrossRef]
SugimotoC.,
KitamuraT.,
GuoJ.16 other authors1997; Typing of urinary JC virus DNA offers a novel means for tracing human migrations. Proc Natl Acad Sci U S A 94:9191–9196[CrossRef]
SugimotoC.,
HasegawaM.,
ZhengH. Y.14 other authors2002a; JC virus strains indigenous to northeastern Siberians and Canadian Inuits are unique but evolutionally related to those distributed throughout Europe and Mediterranean areas. J Mol Evol 55:322–335[CrossRef]
SugimotoC.,
HasegawaM.,
KatoA.,
ZhengH. Y.,
EbiharaH.,
TaguchiF.,
KitamuraT.,
YogoY.2002b; Evolution of human polyomavirus JC: implications for the population history of humans. J Mol Evol 54:285–297[CrossRef]
SwensonJ. J.,
TrowbridgeP. W.,
FrisqueR. J.1996; Replication activity of JC virus large T antigen phosphorylation and zinc finger domain mutants. J Neurovirol 2:78–86[CrossRef]
TakasakaT.,
MirandaJ. J.,
SugimotoC.,
ParaguisonR.,
ZhengH.-Y.,
KitamiraT.,
YogoY.2004; Genotypes of JC virus in Southeast Asia and the western Pacific: implications for human migrations from Asia to the Pacific. Anthropol Sci 112:53–59[CrossRef]
ThompsonJ. D.,
HigginsD. G.,
GibsonT. J.1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680[CrossRef]
VawterL.,
BrownW. M.1986; Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196[CrossRef]
VenterM.,
SmitS. B.,
LemanP.,
SwanepoelR.2004; Phylogenetic evidence of widespread distribution of genotype 3 JC virus in Africa and identification of a type 7 isolate in an African AIDS patient. J Gen Virol 85:2215–2219[CrossRef]
YanagiharaR.,
NerurkarV. R.,
ScheirichI.9 other authors2002; JC virus in the western Pacific suggest Asian mainland relationships and virus association with early population movements. Hum Biol 74:473–488[CrossRef]
YogoY.,
ZhengH.-Y.,
HasegawaM.,
SugimotoC.,
TanakaS.,
HonjoT.,
KobayashiN.,
OhtaN.,
KitamuraT.2003; Phylogenetic analysis of JC virus DNAs detected in Ainus: an attempt to elucidate the origin and diversity of the Ainu. Anthropol Sci 111:19–34
YogoY.,
SugimotoC.,
ZhengH. Y.,
IkegayaH.,
TakasakaT.,
KitamuraT.2004; JC virus genotyping offers a new paradigm in the study of human populations. Rev Med Virol 14:179–191[CrossRef]
ZhengH. Y.,
SugimotoC.,
HasegawaM.8 other authors2003; Phylogenetic relationships among JC virus strains in Japanese/Koreans and native Americans speaking Amerind or Na-Dene. J Mol Evol 56:18–27[CrossRef]
ZhengH. Y.,
ZhaoP.,
SuganamiH.7 other authors2004a; Regional distribution of two related Northeast Asian genotypes of JC virus, CY-a and -b: implications for the dispersal of Northeast Asians. Microbes Infect 6:596–603[CrossRef]
ZhivotovskyL. A.,
RosenbergN. A.,
FeldmanM. W.2003; Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. Am J Hum Genet 72:1171–1186[CrossRef]