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The origin of mutants
Abstract
Nucleic acids are replicated with conspicuous fidelity. Infrequently, however, they undergo changes in sequence, and this process of change (mutation) generates the variability that allows evolution. As the result of studies of bacterial variation, it is now widely believed that mutations arise continuously and without any consideration for their utility. In this paper, we briefly review the source of this idea and then describe some experiments suggesting that cells may have mechanisms for choosing which mutations will occur.
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“Recently there has been evidence that a big role in phenotypic delay may be played by chromosome segregation in quickly dividing cells [21,58].”
From Efficient, robust, and versatile fluctuation data analysis using MLE MUtation Rate calculator (mlemur) (2023) · cites this paper as [21]
In the citing paper
“Simulations performed in the same study suggest that effective polyploidy combined with recessive mutation does not influence mutation rate estimation simply because increased chance of mutation caused by polyploidy cancels out with the phenotypic delay caused by incomplete chromosome segregation [21].”
From Efficient, robust, and versatile fluctuation data analysis using MLE MUtation Rate calculator (mlemur) (2023) · cites this paper as [21]
In the citing paper
“A phenotypic lag (the phenomenon of delayed expression of a scorable phenotype post mutation due to the necessity to accumulate mutant protein product at sufficient level) is also widespread with mutations causing antibiotic resistance, yet rarely accounted for (Figure 1D) [20,21].”
From Efficient, robust, and versatile fluctuation data analysis using MLE MUtation Rate calculator (mlemur) (2023) · cites this paper as [21]
In the citing paper
“Rif R phenotypic lag of in E. coli has been estimated to be 4-5 generations [21].”
From Efficient, robust, and versatile fluctuation data analysis using MLE MUtation Rate calculator (mlemur) (2023) · cites this paper as [21]
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“These results are corroborated by a further large-scale study of children carried out by Broman, Nichols, Shaughnessy, and Kennedy (1987). They examined and followed up approximately 17,000 European and 19,000 African children in the United States from conception to the age of 7 years.”
ResultRasmuson, M. (2002) · Hereditas · doi:10.1034/j.1601-5223.2002.1360101.x · Cited by 8
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“Corresponding author: Elzbieta Grzesiuk, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, A. Pawinskiego 5A, 02-106 Warszawa, Poland; tel.: (48 22) 592 3337; fax: (48 22) 658 4636; e-mail: elag@ibb.waw.pl spontaneous growth-dependent mutations, which appear in the genome randomly before exposure t…”
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“…since the precursors of modern genetics: • Random (De Veies, 1902); • Deliberate by exposure to certain conditions (Pat-terson, 1928; Auerbach et al. , 1947); • Under the pressure of environmental factors: (Cairns et al. , 1988); ■ Natural selection or “survival of the fittest” (Darwin, 1859).”
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Berlik, S. (2007) · Technische Universität Dortmund Eldorado (Technische Universität Dortmund) · doi:10.17877/de290r-148 · Cited by 8
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“The discovery, for example, of adaptive mutations in bacteria ( Cairns, Overbaugh & Miller, 1988 ), has challenged the neodarwinistic view, indicating that randomness in mutations might not be the only way to ensure the genetic changes which are necessary in evolution to adapt to an environment in which continuous cha…”
BackgroundMazzola, G. J., Mortensen, J. E., Miller, L. A., & Poupard, J. A. (2003) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/s0732-8893(02)00526-6 · Cited by 5
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“…the end of Kemp (1994), equivalent to (9) of Pakes (1993), that (5) lim n(n+ I)Pn=m. n--+oo As Kemp observes, (5) implies immediately that P, :=~f=nPj"'m/n as n---+oo, and 'This establishes mathematically the feature of the Luria-Delbruck distribution that was so important in Cairns et al. (1988).”
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“Mutations also occur in non-dividing bacterial cells; these post-replicative mutations are generated by DNA repair or recombination reactions and are called adaptive or stress-induced mutations (22, 23).”
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“There are several empirical studies which support genetic accommodation and adaptive mutation and recombination (Waddington 1953; Rutherford and Lindquist 1998; Cairns et al. 1988; Fischer and Schmid-Hempel 2005; for reviews, see Rosenberg 2001; Parsons 1988; Badyaev 2005).”
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“Mittler and Lenski (1990) replicated the observations of Shapiro (1984) and Cairns et al. (1988), but showed that Lac(Ara) + mutants also arise in starving cultures in solid and liquid media when no sugars are present.”
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Looking backward on a century of mutation research
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“However, this concept has been challenged by the 1988 Cairns study of adaptive mutagenesis [38], which posits that mutations emerge after cells encounter a growth-limiting environment (i.”
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Rousset, L., Alpha‐Bazin, B., Château, A., Armengaud, J., Clavel, T., Berge, O., & Duport, C. (2020) · Environmental Microbiology · doi:10.1111/1462-2920.15203 · Cited by 10
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“This is partly because a lengthier course allows accumulation of more haphazardly-occurring mutations, including the one(s) required for immortality and autonomy, if we accept the notion that tumors, especially cancers, occur as repercussions of mutations that have cell-autonomous modes of action [29-31, 525, 526, 551…”
BackgroundMicrobiological Procedures for Biodegradation Research
Focht, D. (2018) · SSSA Book Series · doi:10.2136/sssabookser5.2.c20 · Cited by 6
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“This experimental vindication of Lamarckism should propel, in our opinion, a reflection on the way in which the debate about directed mutation unfolded since the publication of Cairns et al. (1988).”
BackgroundGuest-Editorial Introduction: Converging Evolutionary Patterns in Life and Culture
Gontier, N. (2016) · Evolutionary Biology · doi:10.1007/s11692-016-9389-0 · Cited by 6
“…puts emphasis on the variation bias that intentional teaching brings forth); and also biologists debate whether or not genetic mutations (Cairns et al. 1988), lateral gene transfers (Popa et al. 2011), eco-evo-devo phenomena such as phenotypic plasticity (West-Eberhard 2003) and niche…”
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“This possibility harkens to the ”directed mutation” controversy (Cairns et al., 1988; McKenzie et al., 2001; McKenzie and Rosenberg, 2001; Andersson et al., 1998; Hendrickson et al., 2002), although in this instance, the mutations are not ”directed.””
BackgroundStationary phase-induction of G → T mutations in Escherichia coli
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“Introduction27 Cairns et al.[1] noted that reversions ofEscherichia28 coli auxotrophs to prototrophy occurred more rapidly29 under selective conditions than in the absence of30 selection.”
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“In adaptive evolution, cells seem to be able to actively select useful mutations and give up useless mutations [237, 253].”
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“In the 1980s, this was developed further with the discovery of adaptive mutations (Shapiro, 1984; Cairns et al., 1988; Rosenberg, 2001).”
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“The Proposal of Directed Mutation John Cairns at Harvard University [Cairns et al., 1988] and Barry Hall at the University of Rochester [Hall, 1991] proposed and argued in favor of the concept of directed mutation.”
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“Reverse transcriptase and Lamarckian scenarios of evolution MICHEL MORANGE Centre Cavaillès, République des Savoirs: Lettres, Sciences, Philosophie USR 3608, Ecole Normale Supérieure, 29 Rue d’Ulm, 75230 Paris Cedex 05, France (Fax, 33-144-323941; Email, morange@biologie.ens.fr)”
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“Finally, an increase in tolerance of individual cells to the effect of the aarV158 mutation and their subsequent selection could occur during the so-called rapid adaptive mutagenesis (hyper mutagenesis), which has been described for prokaryotes [19, 20] and is assumed for eukaryotes [19].”
BackgroundOccurrence of leu+ revertants under starvation cultures in Escherichia coli is growth-dependent
Jin, J., Gao, P., & Mao, Y. (2002) · BMC Genetics · doi:10.1186/1471-2156-3-6 · Cited by 5
“According to the hypothesis of adaptive mutation by Cairns et al, the distribution of mutations under selection should follow Poisson pattern [1].”
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“Adaptive mutation (also known as directed mutation) is de®ned as the preferential appearance of mutations that are advantageous under selective conditions (Cairns et al. 1988).”
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“Since the publication of the study by Cairns et al. (1988), the possible existence of so-called ``directed mutagenesis'' has been the subject of intensive debate.”
BackgroundLeakiness of genetic markers and susceptibility to post-plating mutagenesis inEscherichia coli
Jayaraman, R. (1995) · Journal Genetika · doi:10.1007/bf02932195 · Cited by 5
“The main claim of Cairns et al. (1988) was that when Lac- E. coli was under”
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Regulatory processes and the origins of spontaneous mutations.
Macphee, D. (1994) · Mutation research · doi:10.1016/0027-5107(94)90283-6 · Cited by 5
Enhancing Evolutionary Computation Using Analogues of Biological Mechanisms
Paton, R. (1994) · Evolutionary Computing, AISB Workshop · doi:10.1007/3-540-58483-8_5 · Cited by 5
Holliday, R., & Rosenberger, R. (1988) · Nature · doi:10.1038/336526a0 · Cited by 5
Grafen, A. (1988) · Nature · doi:10.1038/336525b0 · Cited by 5
Simpson, D. H., & Scott, P. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803814-7.00007-1 · Cited by 9
Herpes simplex virus and the rheumatic diseases
Denman, A., Pelton, B., Hylton, W., Palmer, R., & Topper, R. (2004) · Rheumatology International · doi:10.1007/bf00271871 · Cited by 5
Obtaining Strains of Saccharomyces Tolerant to High Temperatures and Ethanol
Peres, M. F. S., de Sousa, S. R., & Laluce, C. (2001) · doi:10.1385/1-59259-029-2:355 · Cited by 5
Metadata
- Authors
- Cairns, J., Overbaugh, J., & Miller, S.
- Affiliations
- Harvard University (US)
- Venue
- Nature
- Published
- 1988-09
- Volume
- 335
- Issue
- 6186
- Pages
- 142-145
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2043748488
- Cited by
- 1,025
- References
- 0
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 12 · 2023: 13 · 2022: 14 · 2021: 10 · 2020: 22 · 2019: 20 · 2018: 30 · 2017: 19 · 2016: 23 · 2015: 14 · 2014: 29 · 2013: 23 · 2012: 29
- FWCI
- 25.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy of Biology and Scientific Explanation
- Keywords
- genetic mutations, bacterial variation, mutation rate, genetic variation, evolution
- MeSH terms
- Arabinose, Escherichia coli, Biological Evolution, Genes, Bacterial, Lactose, Models, Genetic, Mutation, Operon, Selection, Genetic, Genetic Variation
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