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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.
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“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]
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BackgroundMethodInfluentialSelf-citationCooper, T. F., & Lenski, R. E. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-11 · Cited by 129
“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 131
“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
“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 128
“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
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
“…‘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
“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 114
“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 120
“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
“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 114
“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 112
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 113
“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
“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
“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 109
“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
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
Liu, D., & Trumble, J. T. (2007) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2007.00521.x · Cited by 102
“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
Yang, S. P., Sleight, S. C., & Sauro, H. M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks972 · Cited by 102
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
Ψ-Φ: Exploring the outer limits of bacterial pseudogenesPreprint
Lerat, E., & Ochman, H. (2004) · Genome Research · doi:10.1101/gr.2925604 · Cited by 104
“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
Lan, R., Lumb, B., Ryan, D., et al. (2001) · Infection and Immunity · doi:10.1128/iai.69.10.6303-6309.2001 · Cited by 98
“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 105
Hendry, A. P. (2001) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-010-0585-2_31 · Cited by 96
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
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
Metadata
- 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 of Biology and Scientific Explanation
- 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
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