Genomic evolution during a 10,000-generation experiment with bacteria
Open accessAbstract
Molecular methods are used widely to measure genetic diversity within populations and determine relationships among species. However, it is difficult to observe genomic evolution in action because these dynamics are too slow in most organisms. To overcome this limitation, we sampled genomes from populations of Escherichia coli evolving in the laboratory for 10,000 generations. We analyzed the genomes for restriction fragment length polymorphisms (RFLP) using seven insertion sequences (IS) as probes; most polymorphisms detected by this approach reflect rearrangements (including transpositions) rather than point mutations. The evolving genomes became increasingly different from their ancestor over time. Moreover, tremendous diversity accumulated within each population, such that almost every individual had a different genetic fingerprint after 10,000 generations. As has been often suggested, but not previously shown by experiment, the rates of phenotypic and genomic change were discordant, both across replicate populations and over time within a population. Certain pivotal mutations were shared by all descendants in a population, and these are candidates for beneficial mutations, which are rare and difficult to find. More generally, these data show that the genome is highly dynamic even over a time scale that is, from an evolutionary perspective, very brief.
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?
So far there has been little evidence to support the proposition that the overall rate of adaptation or morphological change of a species might influence the molecular clock.
“Although it is possible that the overall rate of adaptation or morphological change of a species might influence the molecular clock, so far there has been little evidence to support this proposition from either experimental studies 19 or comparative analyses 20,21 .”
From The modern molecular clock (2003) · cites this paper as [19]
Given the lack of a relationship between phenotypic evolution and molecular rates, it seems unlikely that the observed faster rate of molecular evolution in more rapidly diversifying lineages is a result of species adapting to new niches.
“Given the lack of a relationship between phenotypic evolution and molecular rates 19-21 , it seems unlikely that the observed faster rate of molecular evolution in more rapidly diversifying lineages is a result of species adapting to new niches.”
From The modern molecular clock (2003) · cites this paper as [19]
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
ANALYZING TABLES OF STATISTICAL TESTS
Rice, W. R. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb04220.x · Cited by 14,361 · see citing works
Molecular Markers, Natural History and Evolution
Avise, J. C. (1994) · Springer eBooks · doi:10.1007/978-1-4615-2381-9 · Cited by 5,210 · see citing works
PAUP (phylogenetic analysis using parsimony)
(2008) · Springer eBooks · doi:10.1007/978-1-4020-6754-9_12413 · Cited by 4,424 · see citing works
The hitch-hiking effect of a favourable gene
Smith, J. M., & Haigh, J. (1974) · Genetical Research · doi:10.1017/s0016672300014634 · Cited by 3,415 · see citing works
Mitochondrial DNA and human evolution
Cann, R. L., Stoneking, M., & Wilson, A. C. (1987) · Nature · doi:10.1038/325031a0 · Cited by 3,100 · see citing works
THE NUMBER OF ALLELES THAT CAN BE MAINTAINED IN A FINITE POPULATION
Kimura, M., & Crow, J. F. (1964) · Genetics · doi:10.1093/genetics/49.4.725 · Cited by 2,690 · see citing works
The hitch-hiking effect of a favourable gene
MAYNARD, J., & Haigh, J. (2007) · Genetics Research · doi:10.1017/s0016672308009579 · Cited by 2,663 · see citing works
The sampling theory of selectively neutral alleles
Ewens, W. J. (1972) · Theoretical Population Biology · doi:10.1016/0040-5809(72)90035-4 · Cited by 2,178 · see citing works
Lenski, R. E., Rose, M. R., Simpson, S. C., & Tadler, S. C. (1991) · The American Naturalist · doi:10.1086/285289 · Cited by 1,582 · see citing works
Self-citationWilson, A. C., Carlson, S. S., & White, T. J. (1977) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.46.070177.003041 · Cited by 1,305 · see citing works
The “hitchhiking effect” revisited
Kaplan, N. L., Hudson, R. R., & Langley, C. H. (1989) · Genetics · doi:10.1093/genetics/123.4.887 · Cited by 1,076 · see citing works
Lenski, R. E., & Travisano, M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.6808 · Cited by 1,019 · see citing works
Self-citationLevels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster
Begun, D. J., & Aquadro, C. F. (1992) · Nature · doi:10.1038/356519a0 · Cited by 962 · see citing works
Evolution of high mutation rates in experimental populations of E. coli
Sniegowski, P. D., Gerrish, P. J., & Lenski, R. E. (1997) · Nature · doi:10.1038/42701 · Cited by 879 · see citing works
Self-citationThe fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
Self-citationThe fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_12 · Cited by 721 · see citing works
Self-citationTHE AVERAGE NUMBER OF GENERATIONS UNTIL FIXATION OF A MUTANT GENE IN A FINITE POPULATION
Kimura, M., & Ohta, T. (1969) · Genetics · doi:10.1093/genetics/61.3.763 · Cited by 683 · see citing works
Transposable elements as sources of variation in animals and plants
KIDWELL, M. G., & Lisch, D. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7704 · Cited by 597 · see citing works
(1993) · Choice Reviews Online · doi:10.5860/choice.30-4151 · Cited by 568 · see citing works
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520 · see citing works
Self-citationMutation-selection balance and the evolutionary advantage of sex and recombination
Charlesworth, B. (1990) · Genetics Research · doi:10.1017/s0016672300025532 · Cited by 418 · see citing works
Long term trends in the evolution of H(3) HA1 human influenza type A.
Fitch, W. M., Bush, R. M., Bender, C. A., & Cox, N. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7712 · Cited by 394 · see citing works
Exceptional Convergent Evolution in a Virus
Bull, J. J., Badgett, M. R., Wichman, H. A., Huelsenbeck, J. P., Hillis, D. M., Gulati, A., Ho, C., & Molineux, I. J. (1997) · Genetics · doi:10.1093/genetics/147.4.1497 · Cited by 375 · see citing works
Punctuated Evolution Caused by Selection of Rare Beneficial Mutations
Elena, S. F., Cooper, V. S., & Lenski, R. E. (1996) · Science · doi:10.1126/science.272.5269.1802 · Cited by 349 · see citing works
Self-citationSpontaneous point mutations that occur more often when advantageous than when neutral.
Hall, B. G. (1990) · Genetics · doi:10.1093/genetics/126.1.5 · Cited by 326 · see citing works
Periodic Selection in Escherichia Coli
Atwood, K. C., Schneider, L. K., & Ryan, F. J. (1951) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.37.3.146 · Cited by 316 · see citing works
Travisano, M., & Lenski, R. E. (1996) · Genetics · doi:10.1093/genetics/143.1.15 · Cited by 230 · see citing works
Self-citationRole of very slightly deleterious mutations in molecular evolution and polymorphism
Ohta, T. (1976) · Theoretical Population Biology · doi:10.1016/0040-5809(76)90019-8 · Cited by 196 · see citing works
The Myth of Eve: Molecular Biology and Human Origins: F. J. Ayala
Ayala, F. J. (1995) · Science · doi:10.1126/science.270.5244.1930 · Cited by 178 · see citing works
Distribution and Abundance of Insertion Sequences Among Natural Isolates of Escherichia coli
Sawyer, S. A., Dykhuizen, D. E., DuBose, R. F., Green, L., Mhlanga-Mutangadura, T., Wolczyk, D. F., & Hartl, D. L. (1987) · Genetics · doi:10.1093/genetics/115.1.51 · Cited by 144 · see citing works
Insertion sequence-related genetic variation in resting Escherichia coli K-12.
Naas, T., Blot, M., Fitch, W. M., & Arber, W. (1994) · Genetics · doi:10.1093/genetics/136.3.721 · Cited by 144 · see citing works
Self-citationCORRELATED RATES OF MOLECULAR AND MORPHOLOGICAL EVOLUTION
Omland, K. E. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb01461.x · Cited by 141 · see citing works
Shaffer, H. B., Clark, J. M., & Kraus, F. (1991) · Systematic Biology · doi:10.1093/sysbio/40.3.284 · Cited by 132 · see citing works
Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12.
Naas, T., Blot, M., Fitch, W., & Arber, W. (1995) · Molecular biology and evolution · doi:10.1093/oxfordjournals.molbev.a040198 · Cited by 102 · see citing works
Self-citationWallis, M. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02337353 · Cited by 94 · see citing works
Shaffer, H. B., Clark, J. M., & Kraus, F. (1991) · Systematic Zoology · doi:10.2307/2992323 · Cited by 93 · see citing works
Transposable elements and adaptation of host bacteria
Blot, M. (1994) · Genetica · doi:10.1007/bf01435235 · Cited by 79 · see citing works
Self-citationIntraclonal Polymorphism in Bacteria
Rainey, P. B., Thompson, I. P., & Moxon, E. R. (1993) · Advances in microbial ecology · doi:10.1007/978-1-4615-2858-6_6 · Cited by 52 · see citing works
Differential activity of a transposable element in Escherichia coli colonies
Shapiro, J. A., & Higgins, N. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.11.5975-5986.1989 · Cited by 52 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- [4]Lenski, R. E. & Travisano, M. (1994) Proc. Natl. Acad. Sci. USA 91, 6808-6814.
- [13]Fitch, W. M., Bush, R. M., Bender, C. A. & Cox, N. J. (1997) Proc. Natl. Acad. Sci. USA 94, 7712-7718.
- [16]Atwood, K. C., Schneider, L. K. & Ryan, F. J. (1951) Proc. Natl. Acad. Sci. USA 37, 146-155.
- [18]Gerrish, P. J. (1998) Ph.D. dissertation (Michigan State University, East Lansing).
- [25]Kidwell, M. & Lisch, D. (1997) Proc. Natl. Acad. Sci. USA 94, 7704-7711.
Cited by
Sorted by citations
Evolution 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 · see citing works
Self-citationBlount, Z. D., Borland, C. Z., & Lenski, R. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803151105 · Cited by 840 · see citing works
Self-citationProkaryotic Evolution in Light of Gene Transfer
Gogarten, J. P., Doolittle, W. F., & Lawrence, J. G. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004046 · Cited by 986 · see citing works
Bromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615 · see citing works
Dunham, M. J., Badrane, H., Ferea, T., Adams, J., Brown, P. O., Rosenzweig, F., & Botstein, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242624799 · Cited by 564 · see citing works
Single-Cell Microbiology: Tools, Technologies, and Applications
Brehm‐Stecher, B. F., & Johnson, E. (2004) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.68.3.538-559.2004 · Cited by 503 · see citing works
Genome-wide analysis of a long-term evolution experiment with Drosophila
Burke, M. K., Dunham, J. P., Shahrestani, P., Thornton, K. R., Rose, M. R., & Long, A. D. (2010) · Nature · doi:10.1038/nature09352 · Cited by 448 · see citing works
The impact of insertion sequences on bacterial genome plasticity and adaptability
Vandecraen, J., Chandler, M., Aertsen, A., & Houdt, R. V. (2017) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2017.1303661 · Cited by 450 · see citing works
Rules of Engagement: Interspecies Interactions that Regulate Microbial Communities
Little, A. E. F., Robinson, C. J., Peterson, S. B., Raffa, K. F., & Handelsman, J. (2008) · Annual Review of Microbiology · doi:10.1146/annurev.micro.030608.101423 · Cited by 402 · see citing works
Genome Sequences of Escherichia coli B strains REL606 and BL21(DE3)
Jeong, H., Barbe, V., Lee, C. H., Vallenet, D., Yu, D. S., Choi, S.-H., Couloux, A., Lee, S., Yoon, S. H., Cattolico, L., et al. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.09.052 · Cited by 385 · see citing works
Self-citationExperimental evolution and the dynamics of adaptation and genome evolution in microbial populations
Lenski, R. E. (2017) · The ISME Journal · doi:10.1038/ismej.2017.69 · Cited by 367 · see citing works
Self-citationImprovement of pCVD442, a suicide plasmid for gene allele exchange in bacteria
Philippe, N., Alcaraz, J., Coursange, E., Geiselmann, J., & Schneider, D. (2004) · Plasmid · doi:10.1016/j.plasmid.2004.02.003 · Cited by 370 · see citing works
Self-citationTests of parallel molecular evolution in a long-term experiment with Escherichia coli
Woods, R. J., Schneider, D., Winkworth, C. L., Riley, M. A., & Lenski, R. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602917103 · Cited by 316 · see citing works
Self-citationEvolutionary Engineering of Industrially Important Microbial Phenotypes
Sauer, U. (2001) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-45300-8_7 · Cited by 297 · see citing works
Cooper, V. S., Schneider, D., Blot, M., & Lenski, R. E. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.9.2834-2841.2001 · Cited by 277 · see citing works
Self-citationRumen microbial (meta)genomics and its application to ruminant production
Morgavi, D. P., Kelly, W. J., Janssen, P. H., & Attwood, G. T. (2012) · animal · doi:10.1017/s1751731112000419 · Cited by 278 · see citing works
Fong, S. S., Joyce, A. R., & Palsson, B. Ø. (2005) · Genome Research · doi:10.1101/gr.3832305 · Cited by 265 · see citing works
Role of Genomic Typing in Taxonomy, Evolutionary Genetics, and Microbial Epidemiology
van Belkum, A., Struelens, M. J., de Visser, J. A. G. M., Verbrugh, H. A., & Tibayrenc, M. (2001) · Clinical Microbiology Reviews · doi:10.1128/cmr.14.3.547-560.2001 · Cited by 258 · see citing works
Fitness effects of advantageous mutations in evolving Escherichia coli populations
Imhof, M., & Schlötterer, C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.3.1113 · Cited by 250 · see citing works
Causes of Insertion Sequences Abundance in Prokaryotic Genomes
Touchon, M., & Rocha, E. P. C. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm014 · Cited by 241 · see citing works
The fixation probability of beneficial mutations
Patwa, Z., & Wahl, L. M. (2008) · Journal of The Royal Society Interface · doi:10.1098/rsif.2008.0248 · Cited by 232 · see citing works
Redfield, R. J. (2001) · Nature Reviews Genetics · doi:10.1038/35084593 · Cited by 230 · see citing works
Gene Transfer in Bacteria: Speciation without Species?
Lawrence, J. G. (2002) · Theoretical Population Biology · doi:10.1006/tpbi.2002.1587 · Cited by 220 · see citing works
The Ecology and Genetics of Microbial Diversity
Kassen, R., & Rainey, P. B. (2004) · Annual Review of Microbiology · doi:10.1146/annurev.micro.58.030603.123654 · Cited by 217 · see citing works
Beneficial mutations and the dynamics of adaptation in asexual populations
Sniegowski, P., & Gerrish, P. J. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0290 · Cited by 213 · see citing works
Adaptation of cells to new environments
Brooks, A. N., Turkarslan, S., Beer, K. D., Lo, F. Y., & Baliga, N. S. (2010) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.136 · Cited by 197 · see citing works
Conrad, T. M., Joyce, A. R., Applebee, M. K., Barrett, C. L., Xie, B., Gao, Y., & Palsson, B. Ø. (2009) · Genome biology · doi:10.1186/gb-2009-10-10-r118 · Cited by 196 · see citing works
New insights into bacterial adaptation through in vivo and in silico experimental evolution
Hindré, T., Knibbe, C., Beslon, G., & Schneider, D. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2750 · Cited by 184 · see citing works
Self-citationExperimental Tests for an Evolutionary Trade-off between Growth Rate and Yield in E. coli
Novak, M., Pfeiffer, T., Lenski, R. E., Sauer, U., & Bonhoeffer, S. (2006) · The American Naturalist · doi:10.1086/506527 · Cited by 184 · see citing works
Self-citationClonal Adaptive Radiation in a Constant Environment
Maharjan, R. P., Seeto, S., McRobb, L. S., & Ferenci, T. (2006) · Science · doi:10.1126/science.1129865 · Cited by 186 · see citing works
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 180 · see citing works
Dynamics of insertion sequence elements during experimental evolution of bacteria
Schneider, D., & Lenski, R. E. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2003.12.008 · Cited by 165 · see citing works
Self-citationPhenogenetic Drift and the Evolution of Genotype–Phenotype Relationships
Weiss, K. M., & Fullerton, S. M. (2000) · Theoretical Population Biology · doi:10.1006/tpbi.2000.1460 · Cited by 165 · see citing works
Ryall, B., Eydallin, G., & Ferenci, T. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05028-11 · Cited by 160 · see citing works
Operon formation is driven by co-regulation and not by horizontal gene transfer.Preprint
Price, M., Huang, K. H., Arkin, A., & Alm, E. (2005) · Genome Research · doi:10.1101/gr.3368805 · Cited by 178 · see citing works
Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with Escherichia coli
Raeside, C., Gaffé, J., Deatherage, D. E., Tenaillon, O., Briska, A. M., Ptashkin, R. N., Cruveiller, S., Médigue, C., Lenski, R. E., Barrick, J. E., et al. (2014) · mBio · doi:10.1128/mbio.01377-14 · Cited by 148 · see citing works
Self-citationMechanisms of Stationary Phase Mutation: A Decade of Adaptive Mutation
Foster, P. L. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.57 · Cited by 182 · see citing works
Tree thinking for all biology: the problem with reading phylogenies as ladders of progress
Omland, K. E., Cook, L. G., & Crisp, M. D. (2008) · BioEssays · doi:10.1002/bies.20794 · Cited by 145 · see citing works
Evolution of global regulatory networks during a long‐term experiment with<i>Escherichia coli</i>
Philippe, N., Crozat, E., Lenski, R. E., & Schneider, D. (2007) · BioEssays · doi:10.1002/bies.20629 · Cited by 145 · see citing works
Self-citationEvaluating the Impact of Population Bottlenecks in Experimental Evolution
Wahl, L. M., Gerrish, P. J., & Saika‐Voivod, I. (2002) · Genetics · doi:10.1093/genetics/162.2.961 · Cited by 144 · see citing works
Riemann, L., Leitet, C., Pommier, T., Simu, K., Holmfeldt, K., Larsson, U., & Hagström, Å. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01983-07 · Cited by 142 · see citing works
Schneider, D., Duperchy, E., Coursange, E., Lenski, R. E., & Blot, M. (2000) · Genetics · doi:10.1093/genetics/156.2.477 · Cited by 138 · see citing works
Self-citationRobustness as an evolutionary principle
Bornholdt, S., & Sneppen, K. (2000) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2000.1280 · Cited by 132 · see citing works
Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection
Crozat, E., Philippe, N., Lenski, R. E., Geiselmann, J., & Schneider, D. (2004) · Genetics · doi:10.1534/genetics.104.035717 · Cited by 133 · see citing works
Self-citationLenski, R. E., Winkworth, C. L., & Riley, M. A. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-002-2423-0 · Cited by 131 · see citing works
Self-citationLenski, R. E., Wiser, M. J., Ribeck, N., Blount, Z. D., Nahum, J., Morris, J., Zaman, L., Turner, C. B., Wade, B. D., Maddamsetti, R., et al. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.2292 · Cited by 127 · see citing works
Self-citationFlynn, K. M., Cooper, T. F., Moore, F. B. ‐., & Cooper, V. S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003426 · Cited by 126 · see citing works
Profiles of Adaptation in Two Similar Viruses
Holder, K. K., & Bull, J. J. (2001) · Genetics · doi:10.1093/genetics/159.4.1393 · Cited by 126 · see citing works
Grünberger, A., Paczia, N., Probst, C., Schendzielorz, G., Eggeling, L., Noack, S., Wiechert, W., & Kohlheyer, D. (2012) · Lab on a Chip · doi:10.1039/c2lc40156h · Cited by 124 · see citing works
Consuegra, J., Gaffé, J., Lenski, R. E., Hindré, T., Barrick, J. E., Tenaillon, O., & Schneider, D. (2021) · Nature Communications · doi:10.1038/s41467-021-21210-7 · Cited by 116 · see citing works
Self-citationEvolutionary genomics of ecological specialization
Zhong, S., Khodursky, A. B., Dykhuizen, D. E., & Dean, A. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404397101 · Cited by 112 · see citing works
Pélosi, L., Kühn, L., Guetta, D., Garin, J., Geiselmann, J., Lenski, R. E., & Schneider, D. (2006) · Genetics · doi:10.1534/genetics.105.049619 · Cited by 110 · see citing works
Self-citationBacterial Physiology, Regulation and Mutational Adaptation in a Chemostat Environment
Ferenci, T. (2007) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(07)53003-1 · Cited by 104 · see citing works
Selection for Gene Clustering by Tandem Duplication
Reams, A. B., & Neidle, E. L. (2004) · Annual Review of Microbiology · doi:10.1146/annurev.micro.58.030603.123806 · Cited by 104 · see citing works
Ooka, T., Ogura, Y., Asadulghani, M., Ohnishi, M., Nakayama, K., Terajima, J., Watanabe, H., & Hayashi, T. (2009) · Genome Research · doi:10.1101/gr.089615.108 · Cited by 93 · see citing works
Positive Selection of Synonymous Mutations in Vesicular Stomatitis Virus
Novella, I. S., Zárate, S., Metzgar, D., & Ebendick-Corpus, B. E. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.08.003 · Cited by 92 · see citing works
Herold, S., Siebert, J., Huber, A., & Schmidt, H. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.3.931-944.2005 · Cited by 86 · see citing works
Gene inversion potentiates bacterial evolvability and virulence
Merrikh, C. N., & Merrikh, H. (2018) · Nature Communications · doi:10.1038/s41467-018-07110-3 · Cited by 86 · see citing works
The dynamic clonal genome and its adaptive potential
Lushai, G., Loxdale, H. D., & Allen, J. A. (2003) · Biological Journal of the Linnean Society · doi:10.1046/j.1095-8312.2003.00189.x · Cited by 85 · see citing works
Replication and Mutation on Neutral Networks
Reidys, C. M. (2001) · Bulletin of Mathematical Biology · doi:10.1006/bulm.2000.0206 · Cited by 86 · see citing works
The biological improbability of a clone
Lushai, G., & Loxdale, H. D. (2002) · Genetics Research · doi:10.1017/s0016672301009582 · Cited by 82 · see citing works
Bongers, R. S., Hoefnagel, M. H. N., Starrenburg, M. J. C., Siemerink, M. A. J., Arends, J. G. A., Hugenholtz, J., & Kleerebezem, M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.15.4499-4507.2003 · Cited by 79 · see citing works
Rozen, D. E., Schneider, D., & Lenski, R. E. (2005) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0322-2 · Cited by 78 · see citing works
Self-citationDynamics of Genome Architecture in Rhizobium sp. Strain NGR234
Mavingui, P., Flores, M., Guo, X., Dávila, G., Perret, X., Broughton, W. J., & Palacios, R. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.1.171-176.2002 · Cited by 73 · see citing works
Flores, M., Mavingui, P., Perret, X., Broughton, W. J., Romero, D., Hernández, G., Dávila, G., & Palacios, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.16.9138 · Cited by 68 · see citing works
McRobb, L. S., & Ferenci, T. (2000) · Genetics · doi:10.1093/genetics/156.4.1493 · Cited by 67 · see citing works
Philippe, N., Pélosi, L., Lenski, R. E., & Schneider, D. (2008) · Journal of Bacteriology · doi:10.1128/jb.01419-08 · Cited by 65 · see citing works
Self-citationSchneider, D., Duperchy, E., Depeyrot, J., Coursange, E., Lenski, R. E., & Blot, M. (2002) · BMC Microbiology · doi:10.1186/1471-2180-2-18 · Cited by 65 · see citing works
Self-citationZinser, E. R., Schneider, D., Blot, M., & Kolter, R. (2003) · Genetics · doi:10.1093/genetics/164.4.1271 · Cited by 63 · see citing works
Self-citationBromham, L. D., & Woolfit, M. (2004) · Systematic Biology · doi:10.1080/10635150490522278 · Cited by 64 · see citing works
EPISTASIS BETWEEN NEW MUTATIONS AND GENETIC BACKGROUND AND A TEST OF GENETIC CANALIZATION
Elena, S. F., & Lenski, R. E. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00824.x · Cited by 61 · see citing works
Self-citationCrozat, E., Winkworth, C., Gaffe, J., Hallin, P. F., Riley, M. A., Lenski, R. E., & Schneider, D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq099 · Cited by 62 · see citing works
Self-citationPredicting evolution from genomics: experimental evolution of bacteriophage T7
Bull, J. J., & Molineux, I. J. (2008) · Heredity · doi:10.1038/sj.hdy.6801087 · Cited by 59 · see citing works
Models of Experimental Evolution: The Role of Genetic Chance and Selective Necessity
Wahl, L. M., & Krakauer, D. C. (2000) · Genetics · doi:10.1093/genetics/156.3.1437 · Cited by 60 · see citing works
Lenski, R. E. (2003) · Plant breeding reviews · doi:10.1002/9780470650288.ch8 · Cited by 60 · see citing works
Self-citationFerenci, T. (2007) · Heredity · doi:10.1038/sj.hdy.6801077 · Cited by 58 · see citing works
Catalyzing Bacterial Speciation: Correlating Lateral Transfer with Genetic Headroom
Lawrence, J. G. (2001) · Systematic Biology · doi:10.1080/10635150120286 · Cited by 58 · see citing works
Riley, M. S., Cooper, V. S., Lenski, R. E., Forney, L. J., & Marsh, T. L. (2001) · Microbiology · doi:10.1099/00221287-147-4-995 · Cited by 58 · see citing works
Self-citationKiewitz, C., Larbig, K. D., Klockgether, J., Weinel, C., & Tümmler, B. (2000) · Microbiology · doi:10.1099/00221287-146-10-2365 · Cited by 58 · see citing works
Fitness Effects of Mutations in Bacteria
Gordo, I., Perfeito, L., & Sousa, A. (2011) · Microbial Physiology · doi:10.1159/000332747 · Cited by 57 · see citing works
Moissl‐Eichinger, C., Rudolph, C., Rachel, R., Koch, М. A., & Huber, R. (2003) · Archives of Microbiology · doi:10.1007/s00203-003-0580-1 · Cited by 55 · see citing works
Maharjan, R. P., Seeto, S., & Ferenci, T. (2006) · Journal of Bacteriology · doi:10.1128/jb.01414-06 · Cited by 55 · see citing works
Emergence of homeostasis and “noise imprinting” in an evolution model
Stern, M. D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.19.10746 · Cited by 53 · see citing works
Sikorski, J., Möhle, M., & Wackernagel, W. (2002) · Environmental Microbiology · doi:10.1046/j.1462-2920.2002.00325.x · Cited by 52 · see citing works
Can fast early rates reconcile molecular dates with the Cambrian explosion?
Bromham, L. D., & Hendy, M. D. (2000) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2000.1108 · Cited by 50 · see citing works
Modeling Genetic Networks and Their Evolution: A Complex Dynamical Systems Perspective
Bornholdt, S. (2001) · Biological Chemistry · doi:10.1515/bc.2001.161 · Cited by 51 · see citing works
Evolutionary Dynamics of Insertion Sequences in Helicobacter pylori
Kalia, A., Mukhopadhyay, A. K., Dailide, G., Ito, Y., Azuma, T., Wong, B. C. Y., & Berg, D. E. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.22.7508-7520.2004 · Cited by 51 · see citing works
Revisiting the Design of the Long-Term Evolution Experiment with Escherichia coli
Lenski, R. E. (2023) · Journal of Molecular Evolution · doi:10.1007/s00239-023-10095-3 · Cited by 50 · see citing works
Self-citationInsertion Sequence-Driven Evolution of Escherichia coli in Chemostats
Gaffé, J., McKenzie, C., Maharjan, R. P., Coursange, E., Ferenci, T., & Schneider, D. (2011) · Journal of Molecular Evolution · doi:10.1007/s00239-011-9439-2 · Cited by 50 · see citing works
Self-citationAlam, S., Brailsford, S. R., Adams, S., Allison, C., SHEEHY, E. C., Zoitopoulos, L., Kidd, E. A. M., & Beighton, D. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.8.3330-3336.2000 · Cited by 50 · see citing works
Zaman, T. U., Albladi, M., Siddique, M. I., Johani, S. M. A., & Balkhy, H. H. (2018) · Infection and Drug Resistance · doi:10.2147/idr.s161146 · Cited by 48 · see citing works
Insertion Sequences show diverse recent activities in Cyanobacteria and Archaea
Zhou, F., Olman, V. N., & Xu, Y. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-36 · Cited by 46 · see citing works
Sleight, S. C., Orlic, C., Schneider, D., & Lenski, R. E. (2008) · Genetics · doi:10.1534/genetics.108.091330 · Cited by 46 · see citing works
Self-citationVogt, G. (2018) · Journal of Biosciences · doi:10.1007/s12038-018-9741-x · Cited by 43 · see citing works
Zelder, O., & Hauer, B. (2000) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00084-9 · Cited by 44 · see citing works
de Visser, J. A. G. M., Akkermans, A. D. L., Hoekstra, R. F., & de Vos, W. M. (2004) · Genetics · doi:10.1534/genetics.104.032136 · Cited by 44 · see citing works
Armbruster, C. R., Marshall, C. W., Garber, A. I., Melvin, J. A., Zemke, A. C., Moore, J., Zamora, P. F., Li, K., Fritz, I. L., Manko, C. D., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109829 · Cited by 37 · see citing works
Molecular Clocks and Explosive Radiations
Bromham, L. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-0002-7 · Cited by 40 · see citing works
Stanek, M. T., Cooper, T. F., & Lenski, R. E. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-302 · Cited by 42 · see citing works
Self-citationWhat can DNA Tell us About the Cambrian Explosion?
Bromham, L. D. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.148 · Cited by 42 · see citing works
- Authors
- Papadopoulos, D., Schneider, D., Meier-Eiss, J., Arber, W., Lenski, R. E., & Blot, M.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1999-03-30
- Volume
- 96
- Issue
- 7
- Pages
- 3807-3812
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC22376
- OpenAlex
- W2049065348
- Cited by
- 234
- References
- 39
- Citations by year
- 2026: 1 · 2023: 4 · 2022: 5 · 2021: 4 · 2020: 7 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 4 · 2014: 9 · 2013: 5 · 2012: 10
- FWCI
- 10.56
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- genome evolution, Escherichia coli, restriction fragment length polymorphism, insertion sequences, transposition, genome rearrangement, genetic diversity, beneficial mutations, genome dynamics
- MeSH terms
- Cell Division, Escherichia coli, Biological Evolution, Models, Genetic, Phylogeny, Time, Genome, Bacterial
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