The phylogeography of human viruses

Viruses, especially those with RNA genomes, represent ideal organisms to study the dynamics of microevolutionary change. In particular, their rapid rate of nucleotide substitution means that the epidemiological processes that shape their diversity act on the same time‐scale as mutations are fixed in viral populations. Consequently, the branching structure of virus phylogenies provides a unique insight into spatial and temporal dynamics. Herein, I describe the key processes in virus phylogeography. These are generally associated with the relative rates of dispersal among populations and virus‐host codivergence (vicariance), and the division between acute (short‐term) and persistent (long‐term) infections. These processes will be illustrated by important human viruses — HIV, dengue, rabies, polyomavirus JC and human papillomavirus – which display varying spatial and temporal structures and virus‐host relationships. Key research questions for the future will also be established.

[1]  A. Lapedes,et al.  Timing the ancestor of the HIV-1 pandemic strains. , 2000, Science.

[2]  C. Moore,et al.  Evidence of HIV-1 Adaptation to HLA-Restricted Immune Responses at a Population Level , 2002, Science.

[3]  A. Halpern,et al.  Analysis of genomic sequences of 95 papillomavirus types: uniting typing, phylogeny, and taxonomy , 1995, Journal of virology.

[4]  Edward C Holmes,et al.  Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. , 2002, Virology.

[5]  J. Margolick,et al.  Consistent Viral Evolutionary Changes Associated with the Progression of Human Immunodeficiency Virus Type 1 Infection , 1999, Journal of Virology.

[6]  E. Holmes,et al.  Inferring population history from molecular phylogenies. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  P. Sharp,et al.  Evolution of human polyomavirus JC. , 2000, The Journal of general virology.

[8]  M. Stephens,et al.  Traces of Human Migrations in Helicobacter pylori Populations , 2003, Science.

[9]  P. Sharp,et al.  Origins and evolution of AIDS viruses: estimating the time-scale. , 2000, Biochemical Society transactions.

[10]  Andrew Rambaut,et al.  GENIE: estimating demographic history from molecular phylogenies , 2002, Bioinform..

[11]  E. Holmes,et al.  Ecology and evolution of rabies virus in Europe. , 1999, The Journal of general virology.

[12]  Martin A. Nowak,et al.  Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS , 1997, Nature Medicine.

[13]  A. Plyusnin,et al.  Virus evolution and genetic diversity of hantaviruses and their rodent hosts. , 2001, Current topics in microbiology and immunology.

[14]  D. Nickle,et al.  Consensus and Ancestral State HIV Vaccines , 2003, Science.

[15]  W. Fitch,et al.  Predicting the evolution of human influenza A. , 1999, Science.

[16]  Niccolo Leo Caldararo,et al.  The evolution of HIV , 2001 .

[17]  R. Page.  Parasites, phylogeny and cospeciation , 1993 .

[18]  L. Villarreal,et al.  Acute and persistent viral life strategies and their relationship to emerging diseases. , 2000, Virology.

[19]  N. Muñoz,et al.  Human papillomavirus and cancer: the epidemiological evidence. , 2000, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[20]  Edward C. Holmes,et al.  Molecular Clocks and the Puzzle of RNA Virus Origins , 2003, Journal of Virology.

[21]  N. Tordo,et al.  Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada. , 2001, Virus research.

[22]  S. Wooding.  Do human and JC virus genes show evidence of host-parasite codemography? , 2001, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[23]  N. Kiviat,et al.  The genetic drift of human papillomavirus type 16 is a means of reconstructing prehistoric viral spread and the movement of ancient human populations , 1993, Journal of virology.

[24]  N. Tordo,et al.  Evidence of Two Lyssavirus Phylogroups with Distinct Pathogenicity and Immunogenicity , 2001, Journal of Virology.

[25]  L L Cavalli-Sforza,et al.  The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations , 2001, Annals of human genetics.

[26]  E. Holmes,et al.  Population dynamics of HIV-1 inferred from gene sequences. , 1999, Genetics.

[27]  R. Rico-Hesse,et al.  Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. , 1997, Virology.

[28]  David L. Robertson,et al.  Human immunodeficiency virus: Phylogeny and the origin of HIV-1 , 2001, Nature.

[29]  J. Mullins,et al.  Molecular Epidemiology of HIV Transmission in a Dental Practice , 1992, Science.

[30]  Edward C Holmes,et al.  Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. , 2003, The Journal of general virology.

[31]  S. Frost,et al.  Genetic drift and within-host metapopulation dynamics of HIV-1 infection , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Edward C. Holmes,et al.  Rates of Molecular Evolution in RNA Viruses: A Quantitative Phylogenetic Analysis , 2002, Journal of Molecular Evolution.

[33]  N. Ferguson,et al.  The effect of antibody-dependent enhancement on the transmission dynamics and persistence of multiple-strain pathogens. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Elena,et al.  The evolution of RNA viruses: A population genetics view. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  E. Holmes,et al.  Evolutionary aspects of recombination in RNA viruses. , 1999, The Journal of general virology.

[36]  C. Wheeler,et al.  Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective , 1997, Journal of virology.

[37]  W. Schaftenaar.  Clinically silent rabies infection in (zoo) bats. , 1998, The Veterinary record.

[38]  A. Jetzt,et al.  High Rate of Recombination throughout the Human Immunodeficiency Virus Type 1 Genome , 2000, Journal of Virology.

[39]  Allen G. Rodrigo,et al.  Immune-Mediated Positive Selection Drives Human Immunodeficiency Virus Type 1 Molecular Variation and Predicts Disease Duration , 2002, Journal of Virology.

[40]  B. Drescher,et al.  Molecular variants of human papillomavirus type 16 from four continents suggest ancient pandemic spread of the virus and its coevolution with humankind , 1992, Journal of virology.

[41]  D. Gubler,et al.  Dengue and dengue hemorrhagic fever. , 2014 .

[42]  P. Simmonds,et al.  Mosaic Structure of the Human Immunodeficiency Virus Type 1 Genome Infecting Lymphoid Cells and the Brain: Evidence for Frequent In Vivo Recombination Events in the Evolution of Regional Populations , 1999, Journal of Virology.

[43]  Roy M. Anderson,et al.  Population dynamics of fox rabies in Europe , 1981, Nature.

[44]  P. Sharp,et al.  AIDS as a zoonosis: scientific and public health implications. , 2000, Science.

[45]  S. Halstead,et al.  Pathogenesis of dengue: challenges to molecular biology. , 1988, Science.

[46]  E. Holmes,et al.  Extinction and rapid emergence of strains of dengue 3 virus during an interepidemic period. , 2002, Virology.

[47]  S. Nadin-Davis,et al.  Phylogeographic patterns exhibited by Ontario rabies virus variants , 1999, Epidemiology and Infection.

[48]  J. Coffin,et al.  Search for the Mechanism of Genetic Variation in the pro Gene of Human Immunodeficiency Virus , 1999, Journal of Virology.

[49]  A. Vaheri,et al.  Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. , 2002, Virus research.

[50]  E. Holmes,et al.  Population dynamics of flaviviruses revealed by molecular phylogenies. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  O. Pybus,et al.  The Epidemic Behavior of the Hepatitis C Virus , 2001, Science.

[52]  C. Chappey,et al.  Simian immunodeficiency viruses from central and western Africa: evidence for a new species-specific lentivirus in tantalus monkeys , 1993, Journal of virology.

[53]  P H Harvey,et al.  The mid-depth method and HIV-1: a practical approach for testing hypotheses of viral epidemic history. , 1999, Molecular biology and evolution.

[54]  C. Ryschkewitsch,et al.  Genotype profile of human polyomavirus JC excreted in urine of immunocompetent individuals , 1996, Journal of clinical microbiology.

[55]  R. Weiss.  The Leeuwenhoek Lecture 2001. Animal origins of human infectious disease. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  H. Pfister,et al.  Evolution of human papillomavirus type 18: an ancient phylogenetic root in Africa and intratype diversity reflect coevolution with human ethnic groups , 1993, Journal of virology.

[57]  C. Ryschkewitsch,et al.  JC virus as a marker of human migration to the Americas. , 2000, Microbes and infection.

[58]  Edward C Holmes,et al.  The origin, emergence and evolutionary genetics of dengue virus. , 2003, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[59]  M. Hasegawa,et al.  Evolution of Human Polyomavirus JC: Implications for the Population History of Humans , 2002, Journal of Molecular Evolution.

[60]  T. Kitamura,et al.  Asian domains of four major genotypes of JC virus, Af2, B1-b, CY and SC , 2002, Archives of Virology.

[61]  S. Williamson,et al.  Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression. , 2003, Molecular biology and evolution.

[62]  S. Hales,et al.  Potential effect of population and climate changes on global distribution of dengue fever: an empirical model , 2002, The Lancet.

[63]  O. Pybus,et al.  An integrated framework for the inference of viral population history from reconstructed genealogies. , 2000, Genetics.

[64]  M. Charleston,et al.  Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. , 2002, Systematic biology.

[65]  D. Focks,et al.  Potential changes in the distribution of dengue transmission under climate warming. , 1997, The American journal of tropical medicine and hygiene.

[66]  Anne-Mieke Vandamme,et al.  U.S. Human Immunodeficiency Virus Type 1 Epidemic: Date of Origin, Population History, and Characterization of Early Strains , 2003, Journal of Virology.

[67]  D. Ferber.  Human Diseases Threaten Great Apes , 2000, Science.

[68]  E. Holmes,et al.  Selection-driven evolution of emergent dengue virus. , 2003, Molecular biology and evolution.

[69]  Heather A Baird,et al.  Comparing the Ex Vivo Fitness of CCR5-Tropic Human Immunodeficiency Virus Type 1 Isolates of Subtypes B and C , 2003, Journal of Virology.

[70]  H. Bernard,et al.  Genomic diversity and evolution of papillomaviruses in rhesus monkeys , 1997, Journal of virology.

[71]  E. Major,et al.  Progressive multifocal leukoencephalopathy: molecular biology, pathogenesis and clinical impact. , 1997, Intervirology.

[72]  David R. Scott,et al.  Persistence of type-specific human papillomavirus infection among cytologically normal women. , 1994, The Journal of infectious diseases.

[73]  K. Sorensen,et al.  Clinically silent rabies infection in (zoo) bats , 1998, The Veterinary Record.

[74]  Anne-Mieke Vandamme,et al.  Tracing the origin and history of the HIV-2 epidemic , 2003, Proceedings of the National Academy of Sciences of the United States of America.