Quasispecies-like behavior observed in catalytic RNA populations evolving in a test tube
Open accessAbstract
BACKGROUND: During the RNA World, molecular populations were probably very small and highly susceptible to the force of strong random drift. In conjunction with Muller's Ratchet, this would have imposed difficulties for the preservation of the genetic information and the survival of the populations. Mechanisms that allowed these nascent populations to overcome this problem must have been advantageous. RESULTS: Using continuous in vitro evolution experimentation with an increased mutation rate imposed by MnCl2, it was found that clonal 100-molecule populations of ribozymes clearly exhibit certain characteristics of a quasispecies. This is the first time this has been seen with a catalytic RNA. Extensive genotypic sampling from two replicate lineages was gathered and phylogenetic networks were constructed to elucidate the structure of the evolving RNA populations. A common distribution was found in which a mutant sequence was present at high frequency, surrounded by a cloud of mutant with lower frequencies. This is a typical distribution of quasispecies. Most of the mutants in these clouds were connected by short Hamming distance values, indicating their close relatedness. CONCLUSIONS: The quasispecies nature of mutant RNA clouds facilitates the recovery of genotypes under pressure of being removed from the population by random drift. The empirical populations therefore evolved a genotypic resiliency despite a high mutation rate by adopting the characteristics of quasispecies, implying that primordial RNA pools could have used this strategy to avoid extinction.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Quasi-species behavior was recently reported in an in vitro evolution experiment with replicating RNA species.
“Such quasi-species behavior was recently reported in an in vitro evolution experiment with replicating RNA species [11].”
From Towards open-ended evolution in self-replicating molecular systems (2017) · cites this paper as [11]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The genetical theory of natural selection
Fisher, R. A. (1930) · doi:10.5962/bhl.title.27468 · Cited by 17,617 · see citing works
Median-joining networks for inferring intraspecific phylogenies
Bandelt, H. J., Forster, P., & Rohl, A. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026036 · Cited by 11,742 · see citing works
Tuerk, C., & Gold, L. (1990) · Science · doi:10.1126/science.2200121 · Cited by 10,421 · see citing works
In vitro selection of RNA molecules that bind specific ligands
Ellington, A. D., & Szostak, J. W. (1990) · Nature · doi:10.1038/346818a0 · Cited by 9,845 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · see citing works
The origins of order; self organization and selection in evolution
Kauffman, S. A. (1994) · International Journal of Biochemistry · doi:10.1016/0020-711x(94)90119-8 · Cited by 6,753 · see citing works
Gotelli, N., & Colwell, R. K. (2001) · Ecology Letters · doi:10.1046/j.1461-0248.2001.00230.x · Cited by 6,529 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300 · see citing works
Selforganization of matter and the evolution of biological macromolecules
Eigen, M. (1971) · Die Naturwissenschaften · doi:10.1007/bf00623322 · Cited by 3,788 · see citing works
Gilbert, W. (1986) · Nature · doi:10.1038/319618a0 · Cited by 2,721 · see citing works
Group Selection and Kin Selection
Smith, J. M. (1964) · Nature · doi:10.1038/2011145a0 · Cited by 2,020 · see citing works
Gilbert, W. (1986) · Nature · Cited by 1,941 · see citing works
The Hypercycle: A principle of natural self-organization
Eigen, M., & Schuster, P. M. (1979) · Cited by 1,906 · see citing works
The effect of linkage on limits to artificial selection
Hill, W. G., & Robertson, A. (1966) · Genetical Research · doi:10.1017/s0016672300010156 · Cited by 1,823 · see citing works
A principle of natural self-organization: Part A: Emergence of the hypercycle
Eigen, M., & Schuster, P. (1977) · Naturwissenschaften · doi:10.1007/bf00450633 · Cited by 1,752 · see citing works
The effect of linkage on limits to artificial selection
Hill, W. G., & Robertson, A. (2007) · Genetics Research · doi:10.1017/s001667230800949x · Cited by 1,562 · see citing works
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 · see citing works
Muller, H. (1932) · American Naturalist · doi:10.1086/280418 · Cited by 1,242 · see citing works
Eigen, M., McCaskill, J., & Schuster, P. (1988) · The Journal of Physical Chemistry · doi:10.1021/j100335a010 · Cited by 670 · see citing works
Robustness and evolvability: a paradox resolved
Wagner, A. (2008) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2007.1137 · Cited by 669 · see citing works
Evolution of digital organisms at high mutation rates leads to survival of the flattest
Wilke, C. O., Wang, J. L., Ofria, C., Lenski, R. E., & Adami, C. (2001) · Nature · doi:10.1038/35085569 · Cited by 636 · see citing works
The Mutational Meltdown in Asexual Populations
Lynch, M., Bürger, R., Butcher, D. L., & Gabriel, W. (1993) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a111354 · Cited by 633 · see citing works
Eigen, M. (1993) · Scientific American · doi:10.1038/scientificamerican0793-42 · Cited by 576 · see citing works
Neutral evolution of mutational robustness
van Nimwegen, E., Crutchfield, J. P., & Huynen, M. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9716 · Cited by 568 · see citing works
Nucleotide sequence heterogeneity of an RNA phage population
Domingo, E., Sabo, D. L., Taniguchi, T., & Weissmann, C. (1978) · Cell · doi:10.1016/0092-8674(78)90223-4 · Cited by 565 · see citing works
Directed Evolution of Nucleic Acid Enzymes
Joyce, G. F. (2004) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.73.011303.073717 · Cited by 515 · see citing works
Current Protocols in Nucleic Acid Chemistry
(2001) · John Wiley & Sons, Inc. eBooks · doi:10.1002/0471142700 · Cited by 472 · see citing works
Kauffman, S. A. (1991) · Scientific American · doi:10.1038/scientificamerican0891-78 · Cited by 427 · see citing works
Selection for Robustness in Mutagenized RNA Viruses
Sanjuán, R., Cuevas, J. M., Furió, V., Holmes, E. C., & Moyá, A. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0030093 · Cited by 369 · see citing works
Viruses as Quasispecies: Biological Implications
Domingo, E., Martín, V., Perales, C., Grande-Pérez, A., García-Arriaza, J., & Arias, A. (2006) · Current Topics in Microbiology and Immunology · doi:10.1007/3-540-26397-7_3 · Cited by 290 · see citing works
Evolvability of an RNA virus is determined by its mutational neighbourhood
Burch, C. L., & Chao, L. (2000) · Nature · doi:10.1038/35020564 · Cited by 276 · see citing works
The origins of life: from the birth of life to the origin of language
(1999) · Choice Reviews Online · doi:10.5860/choice.37-0933 · Cited by 270 · see citing works
On the nature of virus quasispecies
Eigen, M. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)20011-3 · Cited by 258 · see citing works
Fidelity of HIV-1 reverse transcriptase copying RNA in vitro
Ji, J., & Loeb, L. A. (1992) · Biochemistry · doi:10.1021/bi00119a002 · Cited by 208 · see citing works
Continuous in Vitro Evolution of Catalytic Function
Wright, M. C., & Joyce, G. F. (1997) · Science · doi:10.1126/science.276.5312.614 · Cited by 207 · see citing works
Nowak, M. A. (1992) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(92)90145-2 · Cited by 192 · see citing works
Codoñer, F. M., Daròs, J., Solé, R. V., & Elena, S. F. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020136 · Cited by 185 · see citing works
Bull, J. J., Ancel, L. W., & Lachmann, M. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010061 · Cited by 182 · see citing works
Biebricher, C. Κ., & Eigen, M. (2006) · Springer eBooks · doi:10.1007/3-540-26397-7_1 · Cited by 174 · see citing works
Real ribozymes suggest a relaxed error threshold
Kun, Á., Santos, M., & Szathmáry, E. (2005) · Nature Genetics · doi:10.1038/ng1621 · Cited by 151 · see citing works
Quasispecies Theory in Virology
Domingo, E. (2002) · Journal of Virology · doi:10.1128/jvi.76.1.463-465.2002 · Cited by 150 · see citing works
Stages of emerging life —Five principles of early organization
Eigen, M., & Schuster, P. M. (1982) · Journal of Molecular Evolution · doi:10.1007/bf02100223 · Cited by 149 · see citing works
Eigen, M., & Schuster, P. (1979) · Springer eBooks · doi:10.1007/978-3-642-67247-7_1 · Cited by 135 · see citing works
Is the Quasispecies Concept Relevant to RNA Viruses?
Holmes, E. C., & Moyá, A. (2002) · Journal of Virology · doi:10.1128/jvi.76.1.460-462.2002 · Cited by 124 · see citing works
Self-assembly of a group I intron from inactive oligonucleotide fragments
Hayden, E. J., & Lehman, N. (2006) · Chemistry & Biology · doi:10.1016/j.chembiol.2006.06.014 · Cited by 117 · see citing works
Self-citationLehman, N., & Wayne, R. K. (1991) · Genetics · doi:10.1093/genetics/128.2.405 · Cited by 103 · see citing works
Self-citationExtreme heterogeneity in populations of vesicular stomatitis virus
Steinhauer, D. A., de la Torre, J. C., Meier, E., & Holland, J. J. (1989) · Journal of Virology · doi:10.1128/jvi.63.5.2072-2080.1989 · Cited by 99 · see citing works
Molecular mechanisms of manganese mutagenesis.
El‐Deiry, W. S., Downey, K. M., & So, A. G. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.23.7378 · Cited by 96 · see citing works
Evolution in vitro: analysis of a lineage of ribozymes
Lehman, N., & Joyce, G. F. (1993) · Current Biology · doi:10.1016/0960-9822(93)90019-k · Cited by 68 · see citing works
Self-citationManganese cations increase the mutation rate of human immunodeficiency virus type 1 ex vivo
Vartanian, J., Sala, M., Henry, M., Wain–Hobson, S., & Meyerhans, A. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-8-1983 · Cited by 67 · see citing works
Non-unity molecular heritability demonstrated by continuous evolution in vitro
Schmitt, T., & Lehman, N. (1999) · Chemistry & Biology · doi:10.1016/s1074-5521(00)80005-8 · Cited by 56 · see citing works
Self-citationFitness Landscape of Human Immunodeficiency Virus Type 1 Protease Quasispecies
Fernández, G., Clotet, B., & Martı́nez, M. Á. (2006) · Journal of Virology · doi:10.1128/jvi.01594-06 · Cited by 51 · see citing works
Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution
Voytek, S. B., & Joyce, G. F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707490104 · Cited by 50 · see citing works
Sequence analysis of RNA species synthesized by Q.beta. replicase without template
Biebricher, C. Κ., & Luce, R. (1993) · Biochemistry · doi:10.1021/bi00069a021 · Cited by 48 · see citing works
The three-dimensional architecture of the class I ligase ribozyme
Bergman, N. H., Lau, N. C., Lehnert, V., Westhof, É., & Bartel, D. P. (2004) · RNA · doi:10.1261/rna.5177504 · Cited by 47 · see citing works
Replication and Evolution of Short-chained RNA Species Replicated by Q ReplicasePreprint
Biebricher, C. Κ. (1987) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1987.052.01.035 · Cited by 45 · see citing works
Orgel, L. E. (1979) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1979.0077 · Cited by 43 · see citing works
On the early emergence of reverse transcription: Theoretical basis and experimental evidence
Lazcano, A., Valverde, V., Hern�ndez, G., Gariglio, P., Fox, G. E., & Or�, J. (1992) · Journal of Molecular Evolution · doi:10.1007/bf00160213 · Cited by 43 · see citing works
Probability of Fixation of an Advantageous Mutant in a Viral Quasispecies
Wilke, C. O. (2003) · Genetics · doi:10.1093/genetics/163.2.467 · Cited by 41 · see citing works
Assessing the Likelihood of Recurrence during RNA Evolution in Vitro
Lehman, N. (2004) · Artificial Life · doi:10.1162/106454604322875887 · Cited by 35 · see citing works
Self-citationSchlosser, K., & Li, Y. (2005) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0346-7 · Cited by 31 · see citing works
Mauro Santos, A., Zintzaras, E., & Szathm�ry, E. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-2642-7 · Cited by 28 · see citing works
Lehman, N., Donne, M. D., West, M. L., & Dewey, T. G. (2000) · Journal of Molecular Evolution · doi:10.1007/s002390010051 · Cited by 26 · see citing works
Self-citationAccumulation of Deleterious Mutations in Small Abiotic Populations of RNA
Soll, S. J., Arenas, C. D., & Lehman, N. (2006) · Genetics · doi:10.1534/genetics.106.066142 · Cited by 21 · see citing works
Self-citationBagby, S. C., Bergman, N. H., Shechner, D. M., Yen, C. C., & Bartel, D. P. (2009) · RNA · doi:10.1261/rna.1912509 · Cited by 19 · see citing works
Schlosser, K., Lam, J. C. F., & Li, Y. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp222 · Cited by 16 · see citing works
Replicability and Recurrence in the Experimental Evolution of a Group I Ribozyme
Hanczyc, M. M., & Dorit, R. L. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026386 · Cited by 16 · see citing works
Stages of Emerging Life — Five Principles of Early Organization
Eigen, M., & Schuster, P. M. (1982) · Springer eBooks · doi:10.1007/978-94-009-4718-4_13 · Cited by 10 · see citing works
In Vitro Selection of Functional Oligonucleotides and the Origins of Biochemical Activity
Carothers, J. M., & Szostak, J. W. (2006) · Wiley eBooks · doi:10.1002/3527608192.ch1 · Cited by 9 · see citing works
The Continuous Evolution In Vitro Technique
Arenas, C. D., & Lehman, N. (2010) · Current Protocols in Nucleic Acid Chemistry · doi:10.1002/0471142700.nc0907s40 · Cited by 6 · see citing works
Self-citationHolmes, E. C. (2005) · Nature Genetics · doi:10.1038/ng0905-923 · Cited by 6 · see citing works
Quantitative analysis of mutation and selection in self-replicating RNA
Biebricher, C. Κ. (1992) · Advances in Space Research · doi:10.1016/0273-1177(92)90172-t · Cited by 6 · see citing works
Flagged first, then by citations
2 of the 75 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Domingo, E., Sheldon, J., & Perales, C. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05023-11 · Cited by 1,009 · see citing works
Prebiotic Systems Chemistry: New Perspectives for the Origins of Life
Ruiz-Mirazo, K., Briones, C., & de la Escosura, A. (2014) · Chemical Reviews · doi:10.1021/cr2004844 · Cited by 930 · see citing works
Formamide and the origin of life
Saladino, R., Crestini, C., Pino, S., Costanzo, G., & Di Mauro, E. (2012) · Physics of Life Reviews · doi:10.1016/j.plrev.2011.12.002 · Cited by 296 · see citing works
Chemical Fueling Enables Molecular Complexification of Self‐Replicators**
Yang, S., Schaeffer, G., Mattia, E., Markovitch, O., Liu, K., Hussain, A. S., Ottelé, J., Sood, A., & Otto, S. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202016196 · Cited by 86 · see citing works
Towards open-ended evolution in self-replicating molecular systems
Duim, H., & Otto, S. (2017) · Beilstein Journal of Organic Chemistry · doi:10.3762/bjoc.13.118 · Cited by 72 · see citing works
Rethinking quasispecies theory: from fittest type to cooperative consortia
Villarreal, L. P., & Witzany, G. (2013) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v4.i4.79 · Cited by 49 · see citing works
Crucial steps to life: From chemical reactions to code using agents
Witzany, G. (2015) · Biosystems · doi:10.1016/j.biosystems.2015.12.007 · Cited by 35 · see citing works
From Formamide to RNA, the Path Is Tenuous but Continuous
Pino, S., Šponer, J. E., Costanzo, G., Saladino, R., & Mauro, E. D. (2015) · Life · doi:10.3390/life5010372 · Cited by 33 · see citing works
Limits of neutral drift: lessons from the in vitro evolution of two ribozymes
Petrie, K. L., & Joyce, G. F. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9642-z · Cited by 27 · see citing works
Mutant Spectra in Virus Behavior
Perales, C., Lorenzo-Redondo, R., López‐Galíndez, C., Martı́nez, M. Á., & Domingo, E. (2010) · Future Virology · doi:10.2217/fvl.10.61 · Cited by 27 · see citing works
Chemical Fueling Enables Molecular Complexification of Self‐Replicators**
Yang, S., Schaeffer, G., Mattia, E., Markovitch, O., Liu, K., Hussain, A. S., Ottelé, J., Sood, A., & Otto, S. (2021) · Angewandte Chemie · doi:10.1002/ange.202016196 · Cited by 24 · see citing works
Social Networking of Quasi-Species Consortia drive Virolution via Persistence
Villarreal, L. P., Witzany, G., & Telos-Philosophische Praxis, B. (2021) · AIMS Microbiology · doi:10.3934/microbiol.2021010 · Cited by 22 · see citing works
Quasispecies in population of compositional assemblies
Gross, R., Fouxon, I., Lancet, D., & Markovitch, O. (2014) · BMC Evolutionary Biology · doi:10.1186/s12862-014-0265-1 · Cited by 20 · see citing works
Complexity through Recombination: From Chemistry to Biology
Lehman, N., Arenas, C. D., White, W. A., & Schmidt, F. J. (2010) · Entropy · doi:10.3390/e13010017 · Cited by 13 · see citing works
Self-citationCommunication as the Main Characteristic of Life
Witzany, G. (2018) · CRC Press eBooks · doi:10.1201/b22230-9 · Cited by 11 · see citing works
In vitroselections with RNAs of variable length converge on a robust catalytic core
Popović, M., Ellingson, A. Q., Chu, T. P., Wei, C., Pohorille, A., & Ditzler, M. A. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1238 · Cited by 7 · see citing works
van Meer, V., Pawęska, J. T., Swanepoel, R., Grobbelaar, A., & Bastos, A. D. (2024) · Pathogens · doi:10.3390/pathogens13030261 · Cited by 5 · see citing works
Partitioning the Fitness Components of RNA Populations Evolving In Vitro
Arenas, C. D., & Lehman, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084454 · Cited by 5 · see citing works
Self-citationCrucial steps to life: From chemical reactions to code using agents
Witzany, U. (2016) · Cited by 1 · see citing works
Ribozyme Mutagenic Evolution: Mechanisms of Survival
Arenas, C. D., Ardaševa, A., Miller, J., Mikheyev, A. S., & Yokobayashi, Y. (2021) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-021-09617-0 · Cited by 1 · see citing works
Correction: Partitioning the Fitness Components of RNA Populations Evolving In Vitro
Arenas, C. D., & Lehman, N. (2014) · PLoS ONE · doi:10.1371/annotation/e97dcbca-dd1b-45cb-a9a0-c2d5c9ff88f3
Self-citationEvolving an Enzyme From a Non-Catalytic Sequence
Gysbers, R. (2015) · MacSphere (McMaster University) · doi:10.71548/15737
Gysbers, R. (2015)
Evolutionary Dynamics in Molecular Populations of Ligase Ribozymes
Arenas, C. D. (2000) · doi:10.15760/etd.44
- Authors
- Diaz Arenas, C., & Lehman, N.
- Affiliations
- Portland State University (US)
- Corresponding author
- Lehman, Niles
- ORCID
- Lehman, Niles
- Venue
- BMC Evolutionary Biology
- Published
- 2010
- Volume
- 10
- Issue
- 1
- Pages
- 80
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC2850355
- OpenAlex
- W2049026145
- Cited by
- 25
- References
- 75
- Citations by year
- 2024: 1 · 2021: 4 · 2020: 1 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 4 · 2014: 3 · 2013: 3 · 2012: 1
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Evolutionary Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PDXScholar (Portland State University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (0315286)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- quasispecies, ribozymes, in vitro evolution, RNA world, Muller's ratchet, genetic drift, high mutation rate, manganese chloride, phylogenetic networks, Hamming distance
- MeSH terms
- Base Sequence, Genotype, Molecular Sequence Data, Mutation, Nucleic Acid Conformation, Phylogeny, RNA, Catalytic, Sequence Analysis, RNA, Evolution, Molecular, Genetic Drift
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review