The population genetics of ecological specialization in evolving Escherichia coli populations
Abstract
When organisms adapt genetically to one environment, they may lose fitness in other environments. Two distinct population genetic processes can produce ecological specialization-mutation accumulation and antagonistic pleiotropy. In mutation accumulation, mutations become fixed by genetic drift in genes that are not maintained by selection; adaptation to one environment and loss of adaptation to another are caused by different mutations. Antagonistic pleiotropy arises from trade-offs, such that the same mutations that are beneficial in one environment are detrimental in another. In general, it is difficult to distinguish between these processes. We analysed the decay of unused catabolic functions in 12 lines of Escherichia coli propagated on glucose for 20,000 generations. During that time, several lines evolved high mutation rates. If mutation accumulation is important, their unused functions should decay more than the other lines, but no significant difference was observed. Moreover, most catabolic losses occurred early in the experiment when beneficial mutations were being rapidly fixed, a pattern predicted by antagonistic pleiotropy. Thus, antagonistic pleiotropy appears more important than mutation accumulation for the decay of unused catabolic functions in these populations.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Due to transcriptional profiling and massive next-generation DNA sequencing, phenotype-genotype correlations can be easily obtained by whole genome re-sequencing.
“Moreover, due to rather new technologies, including transcriptional profiling [30] and massive next-generation DNA sequencing (NGS) [31,32], phenotype-genotype correlations can be easily obtained by whole genome re-sequencing (WGS).”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [31]
Cites
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · 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
Simultaneous Statistical Inference
Miller, R. G. (1981) · Springer series in statistics · doi:10.1007/978-1-4613-8122-8 · Cited by 5,608 · see citing works
The relation of recombination to mutational advance
Muller, H. J. (1964) · Mutation Research · doi:10.1016/0027-5107(64)90047-8 · Cited by 2,512 · see citing works
THE EVOLUTION OF ECOLOGICAL SPECIALIZATION
Futuyma, D. J., & Moreno, G. (1988) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.19.110188.001231 · Cited by 2,313 · 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-citation(1991) · Choice Reviews Online · doi:10.5860/choice.28-5664 · Cited by 1,306 · see citing works
Deleterious mutations and the evolution of sexual reproduction
Kondrashov, A. S. (1988) · Nature · doi:10.1038/336435a0 · Cited by 1,127 · 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-citationEvolution 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-citationAn extracellular Darwinian experiment with a self-duplicating nucleic acid molecule.
Mills, D. R., Peterson, R. L., & Spiegelman, S. (1967) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.58.1.217 · Cited by 648 · see citing works
Diminishing Returns from Mutation Supply Rate in Asexual Populations
G., J. A., de Visser, J. A. G. M., Zeyl, C., Gerrish, P. J., Blanchard, J. L., & Lenski, R. E. (1999) · Science · doi:10.1126/science.283.5400.404 · Cited by 374 · see citing works
Self-citationEstimate of the genomic mutation rate deleterious to overall fitness in E. coll
Kibota, T. T., & Lynch, M. F. (1996) · Nature · doi:10.1038/381694a0 · Cited by 358 · see citing works
A test of evolutionary theories of senescence
Rose, M. R., & Charlesworth, B. (1980) · Nature · doi:10.1038/287141a0 · Cited by 349 · 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-citationA Delayed Wave of Death from Reproduction in Drosophila
Sgrò, C. M., & Partridge, L. (1999) · Science · doi:10.1126/science.286.5449.2521 · Cited by 268 · see citing works
EVOLUTIONARY ADAPTATION TO TEMPERATURE II. THERMAL NICHES OF EXPERIMENTAL LINES OF ESCHERICHIA COLI
Bennett, A. F., & Lenski, R. E. (1993) · Evolution · doi:10.1111/j.1558-5646.1993.tb01194.x · Cited by 204 · see citing works
Self-citationFunchain, P., Yeung, A., Stewart, J. L., Lin, R. H., Slupska, M. M., & Miller, J. H. (2000) · Genetics · doi:10.1093/genetics/154.3.959 · Cited by 198 · see citing works
Fry, J. D. (1990) · The American Naturalist · doi:10.1086/285116 · Cited by 166 · see citing works
Guckert, J. B., Carr, G. J., Johnson, T. D., Hamm, B. G., Davidson, D. H., & Kumagai, Y. (1996) · Journal of Microbiological Methods · doi:10.1016/s0167-7012(96)00948-7 · Cited by 159 · see citing works
Holt, R. D. (1996) · Evolutionary Ecology · doi:10.1007/bf01239342 · Cited by 149 · see citing works
The genomic mutation rate for fitness in Drosophila
Houle, D., Hoffmaster, D. K., Assimacopoulos, S., et al. (1992) · Nature · doi:10.1038/359058a0 · Cited by 131 · see citing works
Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer.
Szathmáry, E. (1993) · Genetics · doi:10.1093/genetics/133.1.127 · Cited by 121 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Cooper, V. S. Consequences of ecological specialization in experimental long-term evolving populations of Escherichia coli. Thesis, Michigan State Univ. (2000).
Cited by
Sorted by citations
Sex and virulence in Escherichia coli : an evolutionary perspective
Wirth, T., Falush, D., Lan, R., Colles, F. M., Mensa, P., Wieler, L. H., Karch, H., Reeves, P. R., Maiden, M. C. J., Ochman, H., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05172.x · Cited by 2,030 · see citing works
“coli have been detected in laboratory experiments (Sniegowski et al ., 1997; Vulic et al ., 1999; Cooper and Lenski, 2000) and among natural isolates (Denamur et al .”
BackgroundInfluentialEnzyme promiscuity: A mechanistic and evolutionary perspective
Tawfik, O. K. A. D. S. (2010) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-030409-143718 · Cited by 1,355 · see citing works
“Second, expression of redundant mRNA and protein copies carries there exists a selection pressure to inactivate their expression (55, 168).”
BackgroundEvolution 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-citationGenome evolution and adaptation in a long-term experiment with Escherichia coli
Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., Lenski, R. E., & Kim, J. F. (2009) · Nature · doi:10.1038/nature08480 · Cited by 1,184 · see citing works
Self-citationOrganised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P., Bingen, É., Bonacorsi, S., Bouchier, C., Bouvet, O. M. M., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000344 · Cited by 1,177 · see citing works
“The specificity of this pattern of gene loss suggests a footprint of selection through an antagonistic pleiotropy mechanism of adaptation [57] during the very peculiar Shigella intracellular life style.”
BackgroundThe experimental evolution of specialists, generalists, and the maintenance of diversity
Kassen, R. (2002) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2002.00377.x · Cited by 938 · see citing works
“Recently, Cooper & Lenski (2000) provided a critical test of the role of mutation accumulation and antagonistic pleiotropy in generating costs of adaptation.”
BackgroundEnvironmental Escherichia coli: ecology and public health implications—a review
Jang, J., Hur, H., Sadowsky, M., Byappanahalli, M., Yan, T., & Ishii, S. (2017) · Journal of Applied Microbiology · doi:10.1111/jam.13468 · Cited by 755 · see citing works
“coli phenotypic diversity such as carbon metabolism (Cooper and Lenski 2000).”
BackgroundBlount, 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-citationAdaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827 · see citing works
“coli [35], whereas other studies reported improved growth on many non-evolutionary carbon sources after batch selection with gluconeogenic carbon sources [66,67].”
BackgroundKawecki, T. J., Lenski, R. E., Ebert, D., Hollis, B., Olivieri, I., & Whitlock, M. C. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.06.001 · Cited by 807 · see citing works
Self-citationAdaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective
Folkesson, A., Jelsbak, L., Yang, L., Johansen, H. K., Ciofu, O., Høiby, N., & Molin, S. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2907 · Cited by 699 · see citing works
The population genetics of pathogenic Escherichia coli
Denamur, É., Clermont, O., Bonacorsi, S., & Gordon, D. M. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0416-x · Cited by 674 · see citing works
Enzyme promiscuity: evolutionary and mechanistic aspects
Khersonsky, O., Roodveldt, C., & Tawfik, D. S. (2006) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2006.08.011 · Cited by 641 · see citing works
Stress-Induced Mutagenesis in Bacteria
Bjedov, I., Tenaillon, O., Gérard, B., Souza, V., Denamur, É., Radman, M., Taddéi, F., & Matić, I. (2003) · Science · doi:10.1126/science.1082240 · Cited by 588 · see citing works
Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population
Khan, A., Dinh, D. M., Schneider, D., Lenski, R. E., & Cooper, T. F. (2011) · Science · doi:10.1126/science.1203801 · Cited by 581 · see citing works
Self-citationEscherichia coli in the Environment: Implications for Water Quality and Human Health
Ishii, S., & Sadowsky, M. J. (2008) · Microbes and Environments · doi:10.1264/jsme2.23.101 · Cited by 529 · see citing works
Evolution of Ecological Niche Breadth
Sexton, J. P., Montiel, J., Shay, J. E., Stephens, M. R., & Slatyer, R. (2017) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-110316-023003 · Cited by 493 · see citing works
“Other genetic trade-offs are described by antagonistic pleiotropy or mutation accumulation (Cooper & Lenski 2000).”
BackgroundCooper, T. F., Rozen, D. E., & Lenski, R. E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0334340100 · Cited by 440 · see citing works
Self-citationGlobal phenotypic characterization of bacteria
Bochner, B. R. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00149.x · Cited by 442 · see citing works
“In”
BackgroundEvolution of mutation rates in bacteria
Denamur, É., & Matić, I. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05150.x · Cited by 402 · see citing works
“For example, an adaptive mutation in one environment can be deleterious in another [a phenomenon called ‘antagonistic pleiotropy’ (Cooper and Lenski, 2000)].”
BackgroundAdami, C. (2002) · BioEssays · doi:10.1002/bies.10192 · Cited by 397 · see citing works
The dynamics of evolutionary stasis
Eldredge, N., Thompson, J. N., Brakefield, P. M., Sergey Gavrilets, B., Jablonski, D., Jackson, J. B. C., Lenski, R. E., Lieberman, B. S., McPeek, M. A., & Miller, W. L. (2005) · Paleobiology · doi:10.1666/0094-8373(2005)031[0133:tdoes]2.0.co;2 · Cited by 370 · see citing works
“Consistent with the expectation that most mutations that are locally adaptive would not be globally advantageous , lines of E. coli adapted to a glucose-containing environment for 20,000 generations tend to have reduced performance on a range of other substrates (Cooper and Lenski 2000).”
BackgroundSelf-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
“An IS150 insertion within b2875 and an IS186 insertion within menC (unpublished data) had been characterised in clones called S, isolated from a long-term experimental evolution using E. coli (Cooper and Lenski, 2000; Lenski et al., 1991; Rozen and Lenski, 2000).”
BackgroundMolecular ecology of global change
Reusch, T. B. H., & Wood, T. E. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03454.x · Cited by 316 · see citing works
“Distinguishing between these proximate mechanisms is imperative for predicting evolutionary trajectories in the face of environmental change (Cooper & Lenski 2000).”
BackgroundEnvironmental fluctuations and their effects on microbial communities, populations and individuals
Nguyen, J., Lara‐Gutiérrez, J., & Stocker, R. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa068 · Cited by 324 · see citing works
Tests 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-citationMutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load
Wielgoss, S., Barrick, J. E., Tenaillon, O., Wiser, M. J., Dittmar, W. J., Cruveiller, S., Chane-Woon-Ming, B., Médigue, C., Lenski, R. E., & Schneider, D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219574110 · Cited by 292 · see citing works
Self-citationAn experimental test of evolutionary trade-offs during temperature adaptation
Bennett, A. F., & Lenski, R. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702117104 · Cited by 285 · see citing works
Self-citationThe Nature and Dynamics of Bacterial Genomes
Ochman, H., & Dávalos, L. M. (2006) · Science · doi:10.1126/science.1119966 · Cited by 274 · 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
“functions during the evolution experiment (8).”
BackgroundMethodSelf-citationThe molecular basis of phenotypic convergence
Rosenblum, E. B., Parent, C. E., & Brandt, E. E. (2014) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-120213-091851 · Cited by 256 · see citing works
“The importance of negative pleiotropy has been demonstrated repeatedly in experimental evolution studies (e.g., Cooper & Lenski 2000, Ostrowski et al. 2008).”
BackgroundAdaptive laboratory evolution principles and applications in industrial biotechnology
Mavrommati, M., Daskalaki, A., Papanikolaou, S., & Aggelis, G. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107795 · Cited by 269 · see citing works
Diversity in times of adversity: probabilistic strategies in microbial survival games
Wolf, D. M., Vazirani, V. V., & Arkin, A. P. (2005) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2004.11.020 · Cited by 270 · see citing works
“…for this view of microbes as single - celled stockbrokers might be found in observations that stress phenotypes introduce a trade - off between a fitness advantage under stress with a fitness defect under more favorable conditions ( Cooper and Lenski , 2000 ; Kish - ony and Leibler , 2003 ).”
Escherichia coli in disguise: molecular origins of Shigella
Lan, R., & Reeves, P. R. (2002) · Microbes and Infection · doi:10.1016/s1286-4579(02)01637-4 · Cited by 266 · see citing works
Coevolutionary arms races between bacteria and bacteriophage
Weitz, J. S., Hartman, H., & Levin, S. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504062102 · Cited by 261 · see citing works
Lázár, V., Nagy, I., Spohn, R., Csörgő, B., Györkei, Á., Nyerges, Á., Horváth, B., Vörös, A., Busa‐Fekete, R., Hrtyan, M., et al. (2014) · Nature Communications · doi:10.1038/ncomms5352 · Cited by 250 · see citing works
“we show that (1) convergent molecular evolution is prevalent across antibiotic treatments,”
BackgroundKvitek, D. J., & Sherlock, G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003972 · Cited by 228 · see citing works
“coli evolving by serial transfer [49] showed that the rate of loss of unused functions in parallel evolving populations was consistent with AP, rather than MA, suggesting that AP may be widespread, and that when evolving in a consistent (though not necessarily constant) environment that due to the fitness cost of unne…”
BackgroundThe 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
“This cost (in which a mutation is beneficial in one environment but deleterious in another) is known as antagonistic pleiotropy and forms one of two potential costs of adaptation—the other arising from mutations that are neutral in the environment of selection but deleterious elsewhere (26, 91).”
BackgroundDiversity and productivity peak at intermediate dispersal rate in evolving metacommunities
Venail, P. A., MacLean, R. C., Bouvier, T., Brockhurst, M. A., Hochberg, M. E., & Mouquet, N. (2008) · Nature · doi:10.1038/nature06554 · Cited by 214 · see citing works
Experimental EvolutionConcepts, Methods, and Applications of Selection Experiments
Garland, T., & Rose, M. R. (2009) · University of California Press eBooks · doi:10.1525/california/9780520247666.001.0001 · Cited by 218 · see citing works
Pleiotropic Costs of Niche Expansion in the RNA Bacteriophage Φ6
Duffy, S., Turner, P. E., & Burch, C. L. (2005) · Genetics · doi:10.1534/genetics.105.051136 · Cited by 207 · see citing works
“…of adaptation; however, these studies often cannot rule out a role for mutation accumulation (Novella et al. 1995; Reboud and Bell 1997; Weaver et al. 1999; Cooper and Lenski 2000; Crill et al. 2000; Turner and Elena 2000; MacLean and Bell 2002; for a review see Ebert 2000; but see Kassen 2002).”
BackgroundDifferent Levels of Catabolite Repression Optimize Growth in Stable and Variable Environments
New, A. M., Cerulus, B., Govers, S. K., Perez-Samper, G., Zhu, B., Boogmans, S., Xavier, J. B., & Verstrepen, K. J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001764 · Cited by 188 · see citing works
“In ecological theory, both of these ‘‘fine-grained’’ and ‘‘temporally fluctuating’’ environments are predicted to favor generalist growth strategies, with reduced variability in fitness across different environments [1,4–6,27,39,40].”
BackgroundStudier, F. W., Daegelen, P., Lenski, R. E., Maslov, S., & Kim, J. F. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.09.021 · Cited by 200 · see citing works
Self-citationTHE FITNESS EFFECT OF MUTATIONS ACROSS ENVIRONMENTS: A SURVEY IN LIGHT OF FITNESS LANDSCAPE MODELS
Martin, G., & Lenormand, T. (2006) · Evolution · doi:10.1111/j.0014-3820.2006.tb01878.x · Cited by 199 · see citing works
“There is also evidence for antagonistic pleiotropy (Cooper and Lenski 2000; Gazave et al. 2001; MacLean et al. 2004).”
BackgroundDesigning and engineering evolutionary robust genetic circuits
Sleight, S. C., Bartley, B., Lieviant, J. A., & Sauro, H. M. (2010) · Journal of Biological Engineering · doi:10.1186/1754-1611-4-12 · Cited by 194 · see citing works
“There are also examples of chromosomal genes that have lost function over evolutionary time when not under selection [25,26] and so encoding synthetic circuits into the chromosome will only delay this problem.”
BackgroundExperimental 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
“…in competition for a shared energy resource (Lenski et al. 1991; Lenski and Travisano 1994; Vasi et al. 1994; Travisano et al. 1995; Elena et al. 1996; Travisano and Lenski 1996; Elena and Lenski 1997; Cooper and Lenski 2000; Cooper et al. 2003; Lenski 2004; Crozat et al. 2005; Rozen et al. 2005).”
BackgroundSelf-citationMarkussen, T., Marvig, R. L., Gómez‐Lozano, M., Aanæs, K., Burleigh, A. E., Høiby, N., Johansen, H. K., Molin, S., & Jelsbak, L. (2014) · mBio · doi:10.1128/mbio.01592-14 · Cited by 180 · 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
The Genomic Landscape and Evolutionary Resolution of Antagonistic Pleiotropy in Yeast
Qian, W., Ma, D., Xiao, C., Wang, Z., & Zhang, J. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.017 · Cited by 174 · see citing works
“Early artificial-selection experiments showed that improving one trait often worsens another, suggesting that AP is not uncommon (Mather and Harrison, 1949; Rice, 1992; Cooper and Lenski, 2000; Ostrowski et al., 2005).”
BackgroundWielgoss, S., Barrick, J. E., Tenaillon, O., Cruveiller, S., Chane-Woon-Ming, B., Médigue, C., Lenski, R. E., & Schneider, D. (2011) · G3 Genes Genomes Genetics · doi:10.1534/g3.111.000406 · Cited by 177 · see citing works
“Here, we resequenced genomes of 19 clones that were sampled from 8 populations (Table 1 and supporting information, Table S1) that did not evolve elevated mutation rates early in the experiment (Cooper and Lenski 2000; Sniegowski et al. 1997).”
MethodSelf-citationGenome-wide Mutational Diversity in an Evolving Population of Escherichia coliPreprint
Barrick, J. E., & Lenski, R. E. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.018 · Cited by 174 · see citing works
Self-citationDynamics 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-citationThe evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens
MacLean, R. C., Bell, G., & Rainey, P. B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307195101 · Cited by 162 · see citing works
Understanding specialism when the jack of all trades can be the master of all
Remold, S. K. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1990 · Cited by 162 · see citing works
The cost of gene expression underlies a fitness trade-off in yeast
Lang, G. I., Murray, A. W., & Botstein, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901620106 · Cited by 160 · see citing works
Microbial diversity — exploration of natural ecosystems and microbiomes
Gibbons, S. M., & Gilbert, J. A. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.10.003 · Cited by 158 · see citing works
Cooper, V. S., Bennett, A. F., & Lenski, R. E. (2001) · Evolution · doi:10.1554/0014-3820(2001)055[0889:eotdog]2.0.co;2 · Cited by 157 · see citing works
Self-citationHunger Artists: Yeast Adapted to Carbon Limitation Show Trade-Offs under Carbon Sufficiency
Wenger, J. W., Piotrowski, J., Nagarajan, S., Chiotti, K., Sherlock, G., & Rosenzweig, F. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002202 · Cited by 154 · see citing works
“serially diluted for 20,000 generations in minimal medium containing glucose as the sole carbon source exhibit reduced fitness on a variety of alternative carbon sources”
BackgroundLarge 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
“In doing so, the cells may save energy, thereby providing a competitive advantage; even without that benefit, any unused functions will tend to decay or be deleted by ongoing mutations (20, 52, 53).”
BackgroundSelf-citationEvolution of Drug Resistance in <i>Candida Albicans</i>
Cowen, L. E., Anderson, J. B., & Kohn, L. M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160907 · Cited by 151 · see citing works
“Also, adaptation of a population to one environment may result in a decrease in fitness in another environment (a trade-off ) (21, 26).”
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
“To examine this possibility, the growth rate and yield of the evolved populations and the ancestor were quantified on a wide range of substrates, including 64 that were informative.((19)) The resulting data showed numerous significant and parallel declines in the catabolic breadth of the evolved bacteria, indicative o…”
BackgroundResultInfluentialSelf-citationThe reverse evolution from multicellularity to unicellularity during carcinogenesis
Chen, H., Lin, F., Xing, K., & He, X. (2015) · Nature Communications · doi:10.1038/ncomms7367 · Cited by 150 · see citing works
Phenotypic Plasticity, Costs of Phenotypes, and Costs of Plasticity
Callahan, H. S., Maughan, H., & Steiner, U. K. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1438.008 · Cited by 144 · see citing works
“The decay of metabolic breadth over evolutionary time was documented in populations of the bacterium Escherichia coli, where it was found that the decay was attributable to tradeoffs, such that selection favored phenotypic decay (Cooper & Lenski 2000).”
BackgroundLeiby, N., & Marx, C. J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001789 · Cited by 141 · see citing works
“Respiration Assays Indicated Broad Declines in Function Across Substrates, Including Those Where Adaptation Occurred As a first step to readdressing specialization in the LTEE populations, we sought to replicate the Biolog respiration results at 20k presented by Cooper and Lenski [4], as well as extend this analysis t…”
BackgroundMethodInfluentialEXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON
Reusch, T. B. H., & Boyd, P. W. (2012) · Evolution · doi:10.1111/evo.12035 · Cited by 137 · see citing works
“…is currently unresolved and depends on the genetic interactions of genes conferring fitness in these two environments (epistasis) as well as on the fitness landscape, a visualization of fitness (third dimension) as a function of two conditions (Cooper and Lenski 2000; Buckling et al. 2003).”
BackgroundFitness Evolution and the Rise of Mutator Alleles in Experimental Escherichia coli Populations
Shaver, A. C., Dombrowski, P. G., Sweeney, J. Y., Treis, T., Zappala, R. M., & Sniegowski, P. (2002) · Genetics · doi:10.1093/genetics/162.2.557 · Cited by 138 · see citing works
Day, W. A., Fernández, R. E., & Maurelli, A. T. (2001) · Infection and Immunity · doi:10.1128/iai.69.12.7471-7480.2001 · Cited by 136 · see citing works
“A subset of traits (encoded by antivirulence genes) antagonizes the function of virulence and ancestral factors required for growth and survival in host tissues (6, 40).”
BackgroundMetabolic specialization and the assembly of microbial communities
Johnson, D. R., Goldschmidt, F., Lilja, E., & Ackermann, M. (2012) · The ISME Journal · doi:10.1038/ismej.2012.46 · Cited by 134 · see citing works
Deatherage, D. E., Kepner, J., Bennett, A. F., Lenski, R. E., & Barrick, J. E. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616132114 · Cited by 134 · see citing works
“The loss of performance in alternative environments, where selection has not acted to maintain performance, is especially important in populations that evolve hypermutability because many mutations can accumulate that are neutral or nearly so in the current environment but where each has some chance of reducing fitnes…”
BackgroundSelf-citationLong-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
“The superhelix density in vivo is also affected bysince it affects many processes in bacteria including other DNA-binding proteins (Lilley 1986; Bliska and Cozreplication, repair, transcription, recombination, and zarelli 1987). transposition.”
BackgroundSelf-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
“During these 20,000 generations, the average fitness of the evolved populations increased by about 70% relative to that of their ancestor, based on competition experiments performed in the same environment (Cooper and Lenski 2000).”
BackgroundMethodInfluentialSelf-citationCooper, T. F., & Lenski, R. E. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-11 · Cited by 129 · see citing works
“Moreover, the patterns of correlated responses in 12 populations, again founded from the same ancestral strain, indicate that pleiotropic effects of beneficial mutations have been more important than mutation accumulation by drift or hitchhiking in explaining patterns of phenotypic evolution over 20,000 generations [1…”
BackgroundSelf-citationTao, Y., Ruan, J., Yeh, S., Lu, X., Wang, Y., Zhai, W., Cai, J., Ling, S., Gong, Q., Chong, Z., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108715108 · Cited by 129 · see citing works
“coli (34, 35) [and, to some extent, humans (36, 37) and Drosophila (38)].”
BackgroundFeliziani, S., Marvig, R. L., Luján, A. M., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004651 · Cited by 127 · see citing works
“Total catabolic function was calculated as described previously [95].”
MethodFlynn, 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
“coli populations, including the population that was the source of the mutations used in our experiments, declined substantially during long-term evolution in a constant environment with a single carbon source [39,43,44].”
BackgroundSelf-citationPLEIOTROPIC EFFECTS OF BENEFICIAL MUTATIONS IN ESCHERICHIA COLI
Ostrowski, E. A., Rozen, D. E., & Lenski, R. E. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb00944.x · Cited by 124 · see citing works
Self-citationSteiner, F. M., Schlick-Steiner, B. C., VanDerWal, J. J., et al. (2008) · Diversity and Distributions · doi:10.1111/j.1472-4642.2008.00472.x · Cited by 118 · see citing works
“…‘unused’ parts of a fundamental niche – the ecological niche is a set of inherited traits, subject to selective pressure to reduce unused traits (Fong et al., 1995), which notion is supported by theoretical (Holt & Gomulkiewicz, 1997) and experimental (Cooper & Lenski, 2000; Kassen, 2002) research.”
BackgroundThe dynamics of adaptation on correlated fitness landscapes
Kryazhimskiy, S., Tkačik, G., & Plotkin, J. B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905497106 · Cited by 120 · see citing works
“Although data are scarce, a long-term evolution experiment in Escherichia coli has found that adaptation continues to proceed even after 20,000 generations in a constant environment (10).”
BackgroundUtrilla, J., O’Brien, E. J., Chen, K., McCloskey, D., Cheung, J., Wang, H. H., Armenta‐Medina, D., Feist, A. M., & Palsson, B. Ø. (2016) · Cell Systems · doi:10.1016/j.cels.2016.04.003 · Cited by 112 · see citing works
“Several mechanisms can give rise to pleiotropy and some have been demonstrated (Cooper and Lenski, 2000; Leiby and Marx, 2014; Remold, 2012).”
BackgroundWhy Genes Evolve Faster on Secondary Chromosomes in Bacteria
Cooper, V. S., Vohr, S. H., Wrocklage, S. C., & Hatcher, P. J. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000732 · Cited by 116 · see citing works
“Exactly why these genes are or become more dispensable has prompted much speculation: secondary chromosomes have been thought to be niche-specific and thus only conditionally useful in dynamic environments [12], which could cause genes on secondary chromosomes to be lost frequently by drift (because they are useless)…”
BackgroundSelf-citationExperimental Evolution of Pseudomonas fluorescens in Simple and Complex Environments
Barrett, R. D. H., MacLean, R. C., & Bell, G. (2005) · The American Naturalist · doi:10.1086/444440 · Cited by 111 · see citing works
“These are mutations that obstruct the utilization of a particular substrate or substrates; they are neutral in media that lack the substrate but deleterious when the substrate is present (Kawecki 1994; Fry 1996; Whitlock 1996; Kawecki et al. 1997; Cooper and Lenski 2000).”
An evolutionary view of plant tissue culture: somaclonal variation and selection
Wang, Q.-M., & Wang, L. (2012) · Plant Cell Reports · doi:10.1007/s00299-012-1281-5 · Cited by 111 · see citing works
“Considering many groups now carrying out the evolutionary experiments on asexual microorganisms which offer powerful systems for experimental evolution (Cooper and Lenski 2000; Lenski et al. 1991; Travisano and Lenski 1996; Zambrano et al. 1993), we boldly apply the”
InfluentialPélosi, 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-citationLimits to adaptation in asexual populations
de Visser, J. A. G. M., & Rozen, D. E. (2005) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2005.00879.x · Cited by 108 · see citing works
“We tested whether similar nontransitive interactions, indicating a changing environment, could explain the declining rate of adaptation of one of 12 E. coli populations that had been adapting to a simple and presumably constant laboratory environment for 20 000 generations (Cooper & Lenski, 2000).”
BackgroundAdaptive radiation in microbial microcosms
MacLean, R. C. (2005) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2005.00931.x · Cited by 108 · see citing works
“Cooper & Lenski (2000) found that the evolution of specialization on glucose in E. coli was accompanied by a cost, in terms of the inability to consume a wide range of unused carbon sources.”
Molecular and cellular bases of adaptation to a changing environment in microorganisms
Bleuven, C., & Landry, C. R. (2016) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2016.1458 · Cited by 104 · see citing works
“The various parameters involved may include changes in pH [9], in inter- and intraspecific competition [10] and in nutrients and resources availability [11].”
BackgroundNext‐generation sequencing as a tool to study microbial evolution
Brockhurst, M. A., Colegrave, N., & Rozen, D. E. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04835.x · Cited by 105 · see citing works
“How repeatable are patterns of adaptation (Lenski & Travisano 1994; Wichman et al. 1999; Cooper & Lenski 2000)?”
BackgroundThe fate of microbial mutators
de Visser, J. A. G. M. (2002) · Microbiology · doi:10.1099/00221287-148-5-1247 · Cited by 105 · see citing works
The biology of digital organisms
Wilke, C. O., & Adami, C. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02612-5 · Cited by 103 · see citing works
Liu, D., & Trumble, J. T. (2007) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2007.00521.x · Cited by 102 · see citing works
“Two distinct genetic processes commonly have been reported to produce ecological specialization in new environments: mutation accumulation and antagonistic pleiotropy (Cooper & Lenski, 2000) [but see also Lee (2002) for a discussion of additive genetic variance].”
BackgroundIn Vivo Molecular Evolution Reveals Biophysical Origins of Organismal Fitness
Couñago, R. M., Chen, S. S., & Shamoo, Y. E. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.04.012 · Cited by 102 · see citing works
Yang, S. P., Sleight, S. C., & Sauro, H. M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks972 · Cited by 102 · see citing works
On the experimental evolution of specialization and diversity in heterogeneous environments
Jasmin, J., & Kassen, R. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01021.x · Cited by 99 · see citing works
Ψ-Φ: Exploring the outer limits of bacterial pseudogenesPreprint
Lerat, E., & Ochman, H. (2004) · Genome Research · doi:10.1101/gr.2925604 · Cited by 100 · see citing works
“2002) and to a population structure that promotes the maintenance of deleterious mutations (Andersson and Hughes 1996; Cooper and Lenski 2000; Mira et al. 2001).”
BackgroundSpeciation as an active force in promoting genetic evolution
Venditti, C., & Pagel, M. D. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.06.010 · Cited by 98 · see citing works
Lan, R., Lumb, B., Ryan, D., et al. (2001) · Infection and Immunity · doi:10.1128/iai.69.10.6303-6309.2001 · Cited by 98 · see citing works
“Cooper and Lenski (9) reported that during the evolution of E.”
BackgroundLOPEZ, S., Rousset, F., Shaw, F. H., Shaw, R. G., & Ronce, O. (2009) · Conservation Biology · doi:10.1111/j.1523-1739.2009.01326.x · Cited by 96 · see citing works
Hendry, A. P. (2001) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-010-0585-2_31 · Cited by 96 · see citing works
Environment determines evolutionary trajectory in a constrained phenotypic space
Fraebel, D. T., Mickalide, H., Schnitkey, D., Merritt, J., Kuhlman, T. E., & Kuehn, S. (2017) · eLife · doi:10.7554/elife.24669 · Cited by 95 · see citing works
Are adaptation costs necessary to build up a local adaptation pattern?
Magalhães, S., Blanchet, E., Egas, M., et al. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-182 · Cited by 95 · see citing works
- Authors
- Cooper, V. S., & Lenski, R. E.
- Affiliations
- Michigan State University (US)
- Corresponding author
- Cooper, Vaughn S.
- Venue
- Nature
- Published
- 2000-10
- Volume
- 407
- Issue
- 6805
- Pages
- 736-739
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1480307447
- Cited by
- 519
- References
- 23
- Citations by year
- 2026: 11 · 2025: 18 · 2024: 8 · 2023: 23 · 2022: 20 · 2021: 20 · 2020: 22 · 2019: 19 · 2018: 13 · 2017: 20 · 2016: 16 · 2015: 17 · 2014: 29 · 2013: 27 · 2012: 32
- FWCI
- 8.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Natural Science Foundation of China
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Cultural Studies › Language and cultural evolution
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
- Keywords
- ecological specialization, antagonistic pleiotropy, mutation accumulation, Escherichia coli, fitness trade-offs, mutation rate evolution, genetic drift
- MeSH terms
- Adaptation, Physiological, Ecology, Escherichia coli, Genes, Bacterial, Glucose, Models, Biological, Mutation, Evolution, Molecular
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
