Molecular clock-like evolution of human immunodeficiency virus type 1.

The molecular clock hypothesis states that the rate of nucleotide substitution per generation is constant across lineages. If generation times were equal across lineages, samples obtained at the same calendar time would have experienced the same number of generations since their common ancestor. However, if sequences are not derived from contemporaneous samples, differences in the number of generations may be misinterpreted as variation in substitution rates and hence may lead to false rejection of the molecular clock hypothesis. A recent study has called into doubt the validity of clock-like evolution for HIV-1, using molecular sequences derived from noncontemporaneous samples. However, after separating their within-individual data according to sampling time, we found that what appeared to be nonclock-like behavior could be attributed, in most cases, to noncontemporaneous sampling, with contributions also likely to derive from recombination. Natural selection alone did not appear to obscure the clock-like evolution of HIV-1.

[1]  T. Leitner,et al.  The molecular clock of HIV-1 unveiled through analysis of a known transmission history. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  D. Richman,et al.  Evidence for positive selection driving the evolution of HIV-1 env under potent antiviral therapy. , 2001, Virology.

[3]  F J Ayala,et al.  Neutralism and selectionism: the molecular clock. , 2000, Gene.

[4]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .

[5]  D. Posada,et al.  Unveiling the molecular clock in the presence of recombination. , 2001, Molecular biology and evolution.

[6]  D. Nickle,et al.  Importance and detection of virus reservoirs and compartments of HIV infection. , 2003, Current opinion in microbiology.

[7]  E. Holmes,et al.  A likelihood method for the detection of selection and recombination using nucleotide sequences. , 1997, Molecular biology and evolution.

[8]  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.

[9]  Nick Goldman,et al.  Statistical tests of models of DNA substitution , 1993, Journal of Molecular Evolution.

[10]  R. A. Fisher,et al.  The Genetical Theory of Natural Selection , 1931 .

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

[12]  B. Walker,et al.  Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays , 1994, Journal of virology.

[13]  Jon A Yamato,et al.  Maximum likelihood estimation of recombination rates from population data. , 2000, Genetics.

[14]  J H Gillespie,et al.  The molecular clock may be an episodic clock. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Felsenstein,et al.  Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. , 1999, Genetics.

[16]  Masami Hasegawa,et al.  Estimation of effective population size of HIV-1 within a host: a pseudomaximum-likelihood approach. , 2002, Genetics.

[17]  Xiping Wei,et al.  Antiviral pressure exerted by HIV-l-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus , 1997, Nature Medicine.

[18]  A. Jetzt,et al.  Human Immunodeficiency Virus Type 1 Recombination: Rate, Fidelity, and Putative Hot Spots , 2002, Journal of Virology.

[19]  G. Shaw,et al.  Dynamics of HIV-1 recombination in its natural target cells , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  E. Margoliash PRIMARY STRUCTURE AND EVOLUTION OF CYTOCHROME C. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Ho,et al.  Genotypic and phenotypic characterization of HIV-1 patients with primary infection. , 1993, Science.

[22]  Jon A Yamato,et al.  Maximum likelihood estimation of population growth rates based on the coalescent. , 1998, Genetics.

[23]  J. Huelsenbeck,et al.  A Likelihood-Ratio Test of Monophyly , 1996 .

[24]  T Gojobori,et al.  Molecular clock of viral evolution, and the neutral theory. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Felsenstein Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

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

[27]  Andrew Rambaut,et al.  Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phylogenies , 2000, Bioinform..

[28]  J. Margolick,et al.  Influence of Random Genetic Drift on Human Immunodeficiency Virus Type 1 env Evolution During Chronic Infection , 2004, Genetics.

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

[30]  Alan S. Perelson,et al.  A Novel Antiviral Intervention Results in More Accurate Assessment of Human Immunodeficiency Virus Type 1 Replication Dynamics and T-Cell Decay In Vivo , 2003, Journal of Virology.

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

[32]  Sebastian Bonhoeffer,et al.  Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis , 1999, The Lancet.

[33]  V. Bryson,et al.  Evolving Genes and Proteins. , 1965, Science.

[34]  D. Richman,et al.  Characterization of HIV Isolates Arising After Prolonged Zidovudine Therapy , 1992, Journal of acquired immune deficiency syndromes.

[35]  Jon A Yamato,et al.  Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. , 1995, Genetics.

[36]  E. Holmes,et al.  Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection , 1993, Journal of virology.

[37]  B. Rannala,et al.  Phylogenetic methods come of age: testing hypotheses in an evolutionary context. , 1997, Science.

[38]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[39]  F J Ayala,et al.  Erratic overdispersion of three molecular clocks: GPDH, SOD, and XDH , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Peter Beerli,et al.  Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Andrew Rambaut,et al.  Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees , 1997, Comput. Appl. Biosci..

[42]  A. Rodrigo,et al.  Reconstructing genealogies of serial samples under the assumption of a molecular clock using serial-sample UPGMA. , 2000, Molecular biology and evolution.

[43]  L. M. Mansky,et al.  Forward mutation rate of human immunodeficiency virus type 1 in a T lymphoid cell line. , 1996, AIDS research and human retroviruses.

[44]  M. Daucher,et al.  Selective pressure exerted by immunodominant HIV‐1‐specific cytotoxic T lymphocyte responses during primary infection drives genetic variation restricted to the cognate epitope , 1999, European journal of immunology.

[45]  A. J. Brown,et al.  Analysis of HIV-1 env gene sequences reveals evidence for a low effective number in the viral population. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  T. Takano Rate variation of DNA sequence evolution in the Drosophila lineages. , 1998, Genetics.

[48]  R. Desrosiers,et al.  Envelope sequence variation, neutralizing antibodies, and primate lentivirus persistence. , 1994, Current topics in microbiology and immunology.

[49]  D. Posada,et al.  Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1). , 2001, Molecular biology and evolution.

[50]  R. Doms,et al.  Chemokines and coreceptors in HIV/SIV-host interactions. , 1998, AIDS.

[51]  J H Gillespie,et al.  Natural selection and the molecular clock. , 1986, Molecular biology and evolution.

[52]  S. Wright Evolution in mendelian populations , 1931 .

[53]  H. Clifford Lane,et al.  Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression , 1995, Nature Medicine.

[54]  A. Moya,et al.  Frequency-dependent selection in human immunodeficiency virus type 1. , 2002, The Journal of general virology.

[55]  James Theiler,et al.  Advantage of rare HLA supertype in HIV disease progression , 2003, Nature Medicine.

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

[57]  J Overbaugh,et al.  Selection Forces and Constraints on Retroviral Sequence Variation , 2001, Science.

[58]  Andrew Rambaut,et al.  End-Epi: an application for inferring phylogenetic and population dynamical processes from molecular sequences , 1997, Comput. Appl. Biosci..

[59]  J. Hein,et al.  Recombination and the molecular clock. , 2000, Molecular biology and evolution.