Pacing a small cage: mutation and RNA viruses

RNA viruses have an extremely high mutation rate, and we argue that the most plausible explanation for this is a trade-off with replication speed. We suggest that research into further increasing this mutation rate artificially as an antiviral treatment requires a theoretical reevaluation, especially relating to the so-called error threshold. The main evolutionary consequence of a high mutation rate appears to have been to restrict RNA viruses to a small genome; they thus rapidly exploit a limited array of possibilities. Investigating this constraint to their evolution, and how it is occasionally overcome, promises to be fruitful. We explain the many terms used in investigating RNA viral evolution and highlight the specific experimental and comparative work that needs to be done.

[1]  R. Sanjuán,et al.  The cost of replication fidelity in human immunodeficiency virus type 1 , 2007, Proceedings of the Royal Society B: Biological Sciences.

[2]  M. Goodman,et al.  Error-prone replication for better or worse. , 2004, Trends in microbiology.

[3]  Manfred Eigen,et al.  Error catastrophe and antiviral strategy , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  A. Kondrashov Deleterious mutations and the evolution of sexual reproduction , 1988, Nature.

[5]  Julie K. Pfeiffer,et al.  A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Sarafianos,et al.  Role of methionine 184 of human immunodeficiency virus type-1 reverse transcriptase in the polymerase function and fidelity of DNA synthesis. , 1996, Biochemistry.

[7]  C. Wilke,et al.  Evolution of mutational robustness. , 2003, Mutation research.

[8]  J. J. Bull,et al.  Theory of Lethal Mutagenesis for Viruses , 2007, Journal of Virology.

[9]  O. Tenaillon,et al.  Evolution of Mutational Robustness in an RNA Virus , 2005, PLoS biology.

[10]  M. Eigen,et al.  Emergence of the Hypercycle , 1979 .

[11]  Claus O Wilke,et al.  Quasispecies theory in the context of population genetics , 2005, BMC Evolutionary Biology.

[12]  R. Sanjuán,et al.  The cost of replication fidelity in an RNA virus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Peter Schuster,et al.  A principle of natural self-organization , 1977, Naturwissenschaften.

[14]  J. H. Strauss,et al.  Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses , 1997, Journal of virology.

[15]  Todd M. Allen,et al.  Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef , 1999, Nature Medicine.

[16]  Samuel Litwin,et al.  Examining The Theory of Error Catastrophe , 2006, Journal of Virology.

[17]  E. Domingo,et al.  Foot-and-Mouth Disease Virus Mutant with Decreased Sensitivity to Ribavirin: Implications for Error Catastrophe , 2006, Journal of Virology.

[18]  Marco Vignuzzi,et al.  Ribavirin and lethal mutagenesis of poliovirus: molecular mechanisms, resistance and biological implications. , 2005, Virus research.

[19]  Michael Lachmann,et al.  Quasispecies Made Simple , 2005, PLoS Comput. Biol..

[20]  E. Holmes,et al.  A phylogenetic survey of recombination frequency in plant RNA viruses , 2006, Archives of Virology.

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

[22]  Christoph Adami,et al.  Viral evolution under the pressure of an adaptive immune system: Optimal mutation rates for viral escape , 2002, Complex..

[23]  J. Ziebuhr,et al.  Nidovirales: Evolving the largest RNA virus genome , 2006, Virus Research.

[24]  L. Mansky In Vivo Analysis of Human T-Cell Leukemia Virus Type 1 Reverse Transcription Accuracy , 2000, Journal of Virology.

[25]  F. Guirakhoo,et al.  High Fidelity of Yellow Fever Virus RNA Polymerase , 2004, Journal of Virology.

[26]  P. Klenerman,et al.  Viral escape mechanisms – escapology taught by viruses , 2001, International journal of experimental pathology.

[27]  E. Domingo,et al.  Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. , 1992, Gene.

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

[29]  Edward C Holmes,et al.  High rate of viral evolution associated with the emergence of carnivore parvovirus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Edward C Holmes,et al.  Error thresholds and the constraints to RNA virus evolution , 2003, Trends in Microbiology.

[31]  M. Eigen,et al.  What is a quasispecies? , 2006, Current topics in microbiology and immunology.

[32]  G. Wagner,et al.  What is the difference between models of error thresholds and Muller's ratchet? , 1993 .

[33]  J. Drake,et al.  Mutation rates among RNA viruses. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Domingo,et al.  The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance--a review. , 1985, Gene.

[35]  Andrew Rambaut,et al.  The evolution of genome compression and genomic novelty in RNA viruses. , 2007, Genome research.

[36]  A. Kondrashov,et al.  Classification of hypotheses on the advantage of amphimixis. , 1993, The Journal of heredity.

[37]  M. Eigen Selforganization of matter and the evolution of biological macromolecules , 1971, Naturwissenschaften.

[38]  Mario Recker,et al.  The generation of influenza outbreaks by a network of host immune responses against a limited set of antigenic types , 2007, Proceedings of the National Academy of Sciences.

[39]  Santiago F. Elena,et al.  Adaptive Value of High Mutation Rates of RNA Viruses: Separating Causes from Consequences , 2005, Journal of Virology.

[40]  Rafael Sanjuán,et al.  The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Eigen,et al.  The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. , 1977, Die Naturwissenschaften.

[42]  Rafael Sanjuán,et al.  Mechanisms of genetic robustness in RNA viruses , 2006, EMBO reports.

[43]  Rafael Sanjuán,et al.  Epistasis correlates to genomic complexity , 2006, Proceedings of the National Academy of Sciences.

[44]  M. Vignuzzi,et al.  Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population , 2006, Nature.

[45]  M. Eigen,et al.  The Hypercycle: A principle of natural self-organization , 2009 .

[46]  J. Drake,et al.  Rates of spontaneous mutation. , 1998, Genetics.

[47]  Reuben S. Harris,et al.  Retroviral restriction by APOBEC proteins , 2004, Nature Reviews Immunology.

[48]  L. Reha-Krantz Regulation of DNA polymerase exonucleolytic proofreading activity: studies of bacteriophage T4 "antimutator" DNA polymerases. , 1998, Genetics.

[49]  P. Schuster,et al.  Stationary mutant distributions and evolutionary optimization. , 1988, Bulletin of mathematical biology.

[50]  Thomas Wiehe,et al.  Model dependency of error thresholds: the role of fitness functions and contrasts between the finite and infinite sites models , 1997 .

[51]  Sebastian Bonhoeffer,et al.  Virus evolution: The importance of being erroneous , 2002, Nature.