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Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet
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Muller's ratchet is an important concept in population genetics. It predicts that when mutation rates are high and a significant proportion of mutations are deleterious, a kind of irreversible ratchet mechanism will gradually decrease the mean fitness of small populations of asexual organisms. In contrast, sexual recombination may stop or reverse this mutational ratchet by recombinational repair of genetic damage. Experimental support for Muller's ratchet has previously been obtained in protozoa and in a tripartite RNA bacteriophage. We now show clear evidence that Muller's ratchet can operate on a nonsegmented nonrecombining pathogenic RNA virus of animals and humans. We did genetic bottleneck passages (plaque-to-plaque transfers) of vesicular somatitis virus (VSV) and then quantitated relative fitness of the bottleneck clones by allowing direct replication competition in mixed infections in cell culture. We document variable fitness drops (some severe) following only 20 plaque-to-plaque transfers of VSV. In some clones no fitness changes (or only insignificant changes) were observed. Surprisingly, the most regular and severe fitness losses occurred during virus passages on a new host cell type. These results again demonstrate the extreme genetic and biological variability of RNA virus populations. Muller's ratchet could have significant implications for variability of disease severity during virus outbreaks, since genetic bottlenecks must often occur during respiratory droplet transmissions and during spread of low-yield RNA viruses from one body site to another (as with human immunodeficiency virus). Likewise, the lower-probability generation of increased-fitness clones during repeated genetic bottleneck transfers of RNA viruses in nature might also affect disease pathogenesis in infected individuals and in host populations. Whenever genetic bottlenecks of RNA viruses occur, enhanced biological differences among viral subpopulations may result.
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“Thus, selection of beneficial mutations requires breaking the linkage between detrimental and beneficial mutations (Chao, 1990, Duarte et al., 1992) and avoiding competition between beneficial mutations (“clonal interference” effect) (Fisher, 1930, Lenski et al., 1998, Roze and Barton, 2006, Worobey and Holmes, 1999).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Duarte et al., 1992
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Cites
THE EVOLUTIONARY ADVANTAGE OF RECOMBINATION
Felsenstein, J. (1974) · Genetics · doi:10.1093/genetics/78.2.737 · Cited by 1,711
Rapid Evolution of RNA Genomes
Holland, J. J., Spindler, K. R., Horodyski, F. M., Grabau, E. A., Nichol, S. T., & VandePol, S. (1982) · Science · doi:10.1126/science.7041255 · Cited by 1,478
Self-citationGreen, J. B. A., & Smith, J. C. (1990) · Nature · doi:10.1038/347391a0 · Cited by 500
Fitness of RNA virus decreased by Muller’s ratchet
Chao, L. (1990) · Nature · doi:10.1038/348454a0 · Cited by 488
Lefrançois, L., & Lyles, D. S. (1982) · Virology · doi:10.1016/0042-6822(82)90125-8 · Cited by 283
Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses
Holland, J. J., de la Torre, J. C., Clarke, D. K., & Duarte, E. A. (1991) · Journal of Virology · doi:10.1128/jvi.65.6.2960-2967.1991 · Cited by 272
Self-citationGenetic variation in AIDS viruses
Coffin, J. M. (1986) · Cell · doi:10.1016/0092-8674(86)90851-2 · Cited by 270
Strauss, J. H., & Strauss, E. G. (1988) · Annual Review of Microbiology · doi:10.1146/annurev.mi.42.100188.003301 · Cited by 238
The Mutation Rate and Variability of Eukaryotic Viruses: An Analytical Review
Smith, D. B., & Inglis, S. C. (1987) · Journal of General Virology · doi:10.1099/0022-1317-68-11-2729 · Cited by 149
Lefrançois, L., & Lyles, D. S. (1982) · Virology · doi:10.1016/0042-6822(82)90126-x · Cited by 140
Research works printed but not linked: 4
- Domingo, E., Holland, J. J. & Ahlquist, P. (CRC, Boca Raton, FL), pp. 3-36.
- Domingo, E., Holland, J. J. & Ahlquist, P. (CRC, Boca Raton, FL), Vol. 3, pp. 211-245.
- Zimmern, D. (1988) in RNA Genetics, eds. Domingo, E., Holland, J. J. & Ahlquist, P. (CRC, Boca Raton, FL), Vol. 2, pp. 211-240.
- Holland, J. J. & Cords, C. E. (1964) Proc. Natl. Acad. Sci. USA 51, 1082-1085.
Cited by
Sorted by citations
RNA VIRUS MUTATIONS AND FITNESS FOR SURVIVAL
Domingo, E., & Holland, J. J. (1997) · Annual Review of Microbiology · doi:10.1146/annurev.micro.51.1.151 · Cited by 1,514
Self-citationEvolution Experiments with Microorganisms: The Dynamics and Genetic Bases of Adaptation
Elena, S. F., & Lenski, R. E. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1088 · Cited by 1,386
Domingo, E., Sheldon, J., & Perales, C. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05023-11 · Cited by 1,009
Self-citationV ARIABILITY AND G ENETIC S TRUCTURE OF P LANT V IRUS P OPULATIONS
García‐Arenal, F., Fraile, A., & Malpica, J. M. (2001) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.39.1.157 · Cited by 631
The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus.
Sanjuán, R., Moya, A., & Elena, S. F. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400146101 · Cited by 582
Origin and Evolution of Viruses
Holland, J. J., & Domingo, E. (1998) · Virus Genes · doi:10.1023/a:1007989407305 · Cited by 524
Self-citationWeaver, S. C., & Vasilakis, N. (2009) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2009.02.003 · Cited by 523
Denison, M. R., Graham, R. L., Donaldson, E., Eckerle, L. D., & Baric, R. S. (2011) · RNA Biology · doi:10.4161/rna.8.2.15013 · Cited by 501
Spontaneous Mutation Accumulation Studies in Evolutionary Genetics
Halligan, D. L., & Keightley, P. D. (2009) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.39.110707.173437 · Cited by 484
Bull, J. J. (1994) · Evolution · doi:10.1111/j.1558-5646.1994.tb02185.x · Cited by 456
Basic concepts in RNA virus evolution
Domingo, E., Escarmı́s, C., Sevilla, N., Moyá, A., Elena, S. F., Quer, J., Novella, I. S., & Holland, J. J. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.8.8666162 · Cited by 448
Self-citationCompounds with Therapeutic Potential against Novel Respiratory 2019 Coronavirus
Martı́nez, M. Á. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00399-20 · Cited by 452
Domingo, E., & Perales, C. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008271 · Cited by 350
Self-citationEvolution of foot-and-mouth disease virus
Domingo, E., Escarmı́s, C., Baranowski, É., Ruiz-Jarabo, C. M., Carrillo, E. C., Núñez, J. I., & Sobrino, F. (2003) · Virus Research · doi:10.1016/s0168-1702(02)00259-9 · Cited by 321
Self-citationHELPER-DEPENDENT VECTOR TRANSMISSION OF PLANT VIRUSES
Pirone, T. P., & Blanc, S. (1996) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.34.1.227 · Cited by 305
Theory of lethal mutagenesis for viruses
Bull, J. J., Sanjuán, R., & Wilke, C. O. (2007) · Journal of Virology · doi:10.1128/jvi.01624-06 · Cited by 281
Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses
Chare, E. R., Gould, E. A., & Holmes, E. C. (2003) · Journal of General Virology · doi:10.1099/vir.0.19277-0 · Cited by 273
Exponential increases of RNA virus fitness during large population transmissions.
Novella, I. S., Duarte, E. A., Elena, S. F., Moyá, A., Domingo, E., & Holland, J. J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.13.5841 · Cited by 271
Self-citationWeaver, S. C., Brault, A. C., Kang, W., & Holland, J. J. (1999) · Journal of Virology · doi:10.1128/jvi.73.5.4316-4326.1999 · Cited by 266
Self-citationGenetic Diversity in RNA Virus Quasispecies Is Controlled by Host-Virus Interactions
Schneider, W. L., & Roossinck, M. J. (2001) · Journal of Virology · doi:10.1128/jvi.75.14.6566-6571.2001 · Cited by 264
Maisnier‐Patin, S., & Andersson, D. I. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2004.01.019 · Cited by 259
Bacteriophage Adsorption Rate and Optimal Lysis Time
Shao, Y., & Wang, I. (2008) · Genetics · doi:10.1534/genetics.108.090100 · Cited by 229
Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence
Yeh, M. T., Bujaki, E., Dolan, P. T., Smith, M., Wahid, R., Konz, J., Weiner, A. J., Bandyopadhyay, A. S., Van Damme, P., De Coster, I., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.04.003 · Cited by 221
Genetic Bottlenecks Reduce Population Variation in an Experimental RNA Virus Population
Li, H., & Roossinck, M. J. (2004) · Journal of Virology · doi:10.1128/jvi.78.19.10582-10587.2004 · Cited by 215
Variation and evolution of plant virus populations
García‐Arenal, F., Fraile, A., & Malpica, J. M. (2003) · International Microbiology · doi:10.1007/s10123-003-0142-z · Cited by 211
Influenza A Virus Transmission Bottlenecks Are Defined by Infection Route and Recipient Host
Varble, A., Albrecht, R. A., Backes, S., Crumiller, M., Bouvier, N. M., Sachs, D. M., García‐Sastre, A., & tenOever, B. R. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.09.020 · Cited by 208
Mutation rate of SARS-CoV-2 and emergence of mutators during experimental evolution
Amicone, M., Borges, V., Alves, M. J., Isidro, J., Zé‐Zé, L., Duarte, S., Vieira, L., Guiomar, R., Gomes, J. P., & Gordo, I. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac010 · Cited by 217
Malim, M. H., & Emerman, M. (2001) · Cell · doi:10.1016/s0092-8674(01)00234-3 · Cited by 201
Troyer, R. M., Collins, K. R., Abraha, A., Fraundorf, E., Moore, D. M., Krizan, R. W., Toossi, Z., Colebunders, R., Jensen, M. A., Mullins, J. I., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.14.9006-9018.2005 · Cited by 198
Vasilakis, N., Deardorff, E. R., Kenney, J. L., Rossi, S. L., Hanley, K. A., & Weaver, S. C. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000467 · Cited by 191
Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution
den Bergh, B. V., Swings, T., Fauvart, M., & Michiels, J. J. (2018) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00008-18 · Cited by 200
Muller's ratchet decreases fitness of a DNA-based microbe.
Andersson, D. I., & Hughes, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.2.906 · Cited by 180
Carrasco, P., de la Iglesia, F., & Elena, S. F. (2007) · Journal of Virology · doi:10.1128/jvi.00524-07 · Cited by 185
Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses
Clarke, D. K., Duarte, E. A., Moyá, A., Elena, S. F., Domingo, E., & Holland, J. J. (1993) · Journal of Virology · doi:10.1128/jvi.67.1.222-228.1993 · Cited by 177
Self-citationThe evolution of RNA viruses: A population genetics view
Moyá, A., Elena, S. F., Bracho, M. A., Miralles, R., & Barrio, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.13.6967 · Cited by 178
Biebricher, C. Κ., & Eigen, M. (2006) · Springer eBooks · doi:10.1007/3-540-26397-7_1 · Cited by 178
Rouzine, I. M., Rodrigo, A., & Coffin, J. M. (2001) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.65.1.151-185.2001 · Cited by 173
Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens
Bergstrom, C. T., McElhany, P., & Real, L. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5095 · Cited by 178
Evolution of microbes and viruses: a paradigm shift in evolutionary biology?
Koonin, E. V., & Wolf, Y. I. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00119 · Cited by 177
Baranowski, É., Ruiz-Jarabo, C. M., Sevilla, N., Andreu, D., Beck, E., & Domingo, E. (2000) · Journal of Virology · doi:10.1128/jvi.74.4.1641-1647.2000 · Cited by 170
Self-citationFraile, A., Alonso‐Prados, J. L., Aranda, M. A., Bernal, J. J., Malpica, J. M., & García‐Arenal, F. (1997) · Journal of Virology · doi:10.1128/jvi.71.2.934-940.1997 · Cited by 165
Estimation of the number of virus particles transmitted by an insect vector
Moury, B., Fabre, F., & Senoussi, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702739104 · Cited by 164
RNA Recombination Enhances Adaptability and Is Required for Virus Spread and Virulence
Xiao, Y., Rouzine, I. M., Bianco, S., Acevedo, A., Goldstein, E. F., Farkov, M., Brodsky, L., & Andino, R. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.03.009 · Cited by 157
The red queen reigns in the kingdom of RNA viruses.
Clarke, D. K., Duarte, E. A., Elena, S. F., Moyá, A., Domingo, E., & Holland, J. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.11.4821 · Cited by 157
Self-citationMatters of Size: Genetic Bottlenecks in Virus Infection and Their Potential Impact on Evolution
Zwart, M. P., & Elena, S. F. (2015) · Annual Review of Virology · doi:10.1146/annurev-virology-100114-055135 · Cited by 156
Drastic Fitness Loss in Human Immunodeficiency Virus Type 1 upon Serial Bottleneck Events
Yuste, E., Sánchez‐Palomino, S., Casado, C., Domingo, E., & López‐Galíndez, C. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.2745-2751.1999 · Cited by 156
Self-citationStochastic processes strongly influence HIV-1 evolution during suboptimal protease-inhibitor therapy
Nijhuis, M., Boucher, C. A., Schipper, P. J., Leitner, T., Schuurman, R., & Albert, J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14441 · Cited by 156
Evolutionary Influences in Arboviral Disease
Weaver, S. C. (2006) · Current topics in microbiology and immunology · doi:10.1007/3-540-26397-7_10 · Cited by 154
Escarmı́s, C., Dávila, M., & Domingo, E. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2366 · Cited by 153
Self-citationLequime, S., Fontaine, A., Gouilh, M. A., Moltini-Conclois, I., & Lambrechts, L. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006111 · Cited by 146
Mechanisms of genetic robustness in RNA viruses
Elena, S. F., Carrasco, P., Daròs, J., & Sanjuán, R. (2006) · EMBO Reports · doi:10.1038/sj.embor.7400636 · Cited by 147
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Fraile, A., Escriu, F., Aranda, M. A., Malpica, J. M., Gibbs, A. J., & García‐Arenal, F. (1997) · Journal of Virology · doi:10.1128/jvi.71.11.8316-8320.1997 · Cited by 143
Novella, I. S., Elena, S. F., Moyá, A., Domingo, E., & Holland, J. J. (1995) · Journal of Virology · doi:10.1128/jvi.69.5.2869-2872.1995 · Cited by 142
Self-citationGrubaugh, N. D., Weger‐Lucarelli, J., Murrieta, R. A., Fauver, J. R., Garcia-Luna, S., Prasad, A. N., Black, W. C., & Ebel, G. D. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.03.002 · Cited by 146
Gavrilin, G. V., Cherkasova, E. A., Lipskaya, G. Y., Kew, O. M., & Agol, V. I. (2000) · Journal of Virology · doi:10.1128/jvi.74.16.7381-7390.2000 · Cited by 138
Subclonal components of consensus fitness in an RNA virus clone
Duarte, E. A., Novella, I. S., Ledesma, S., Clarke, D. K., Moyá, A., Elena, S. F., Domingo, E., & Holland, J. J. (1994) · Journal of Virology · doi:10.1128/jvi.68.7.4295-4301.1994 · Cited by 137
Self-citationDomingo, E., Menéndez‐Arias, L., & Holland, J. J. (1997) · Reviews in Medical Virology · doi:10.1002/(sici)1099-1654(199707)7:2 · Cited by 133
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Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence
Weaver, S. C., Forrester, N. L., Liu, J., & Vasilakis, N. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00482-8 · Cited by 132
Cucumber mosaic virus , a model for RNA virus evolution
Roossinck, M. J. (2001) · Molecular Plant Pathology · doi:10.1046/j.1364-3703.2001.00058.x · Cited by 131
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Elena, S. F., & Sanjuán, R. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095637 · Cited by 131
Schneider, W. L., & Roossinck, M. J. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3130-3134.2000 · Cited by 127
Partial Genetic Characterization of West Nile Virus Strains, New York State, 2000
Ebel, G. D., Dupuis, A. P., Ngo, K. A., Nicholas, D., Kauffman, E. B., Jones, S. A., Young, D. M., Maffei, J. G., Shi, P., Bernard, K. A., et al. (2001) · Emerging infectious diseases · doi:10.3201/eid0704.010408 · Cited by 123
Borrego, B., Novella, I. S., Giralt, E., Andreu, D., & Domingo, E. (1993) · Journal of Virology · doi:10.1128/jvi.67.10.6071-6079.1993 · Cited by 121
Self-citationPfeiffer, J. K., & Kirkegaard, K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600834103 · Cited by 119
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Dynamic Mutation–Selection Balance as an Evolutionary Attractor
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Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture
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Smith, D. R., Adams, A. P., Kenney, J. L., Wang, E., & Weaver, S. C. (2007) · Virology · doi:10.1016/j.virol.2007.10.011 · Cited by 110
Novella, I. S., Clarke, D. K., Quer, J., Duarte, E. A., Lee, C. H., Weaver, S. C., Elena, S. F., Moyá, A., Domingo, E., & Holland, J. J. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.6805-6809.1995 · Cited by 109
Self-citationLázaro, E., Escarmı́s, C., Pérez‐Mercader, J., Manrubia, S. C., & Domingo, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1332668100 · Cited by 109
Self-citationInsights into Arbovirus Evolution and Adaptation from Experimental Studies
Ciota, A. T., & Kramer, L. D. (2010) · Viruses · doi:10.3390/v2122594 · Cited by 112
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Domingo, E., Escarmı́s, C., Lázaro, E., & Manrubia, S. C. (2004) · Virus Research · doi:10.1016/j.virusres.2004.11.003 · Cited by 106
Self-citationBonneau, K. R., Mullens, B. A., & MacLachlan, N. J. (2001) · Journal of Virology · doi:10.1128/jvi.75.17.8298-8305.2001 · Cited by 105
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Forrester, N. L., Coffey, L. L., & Weaver, S. C. (2014) · Viruses · doi:10.3390/v6103991 · Cited by 100
High mutation rates, bottlenecks, and robustness of RNA viral quasispecies
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Self-citationWhitaker, R. J., Grogan, D. W., & Taylor, J. W. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi233 · Cited by 103
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Population Bottlenecks in Quasispecies Dynamics
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Hidden Virulence Determinants in a Viral Quasispecies In Vivo
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Self-citationViral quasispecies and the problem of vaccine-escape and drug-resistant mutants
Domingo, E., Menéndez‐Arias, L., Quiñones‐Mateu, M. E., Holguín, Á., Gutiérrez‐Rivas, M., Martı́nez, M. Á., Quer, J., Novella, I. S., & Holland, J. J. (1997) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-8861-5_4 · Cited by 74
Self-citationElena, S. F., & Moyá, A. (1999) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1999.00110.x · Cited by 74
Metadata
- Authors
- Duarte, E., Clarke, D., Moya, A., Domingo, E., & Holland, J.
- Affiliations
- University of California San Diego (US)
- Department of Biology, University of California, San Diego, La Jolla 92093-0116.
- ORCID
- Domingo, E
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1992-07
- Volume
- 89
- Issue
- 13
- Pages
- 6015-6019
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC402129
- OpenAlex
- W2055633360
- Cited by
- 331
- References
- 21
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 9 · 2018: 7 · 2017: 7 · 2016: 12 · 2015: 7 · 2014: 13 · 2013: 10 · 2012: 14
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (AI-14627)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Mathematics › Applied Mathematics › Mathematical and Theoretical Epidemiology and Ecology Models
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- Muller's ratchet, RNA viruses, vesicular stomatitis virus, population bottleneck, fitness loss, relative fitness, disease severity variability, virus transmission
- MeSH terms
- Animals, Cells, Cultured, Genetics, Population, Cricetinae, HeLa Cells, Humans, Mutation, RNA Viruses, Vesicular stomatitis Indiana virus, Virus Replication, In Vitro Techniques
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