Garland, T. & Rose, M. R. (eds) Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments (Univ. of California Press, 2009).
Kawecki, T. J. et al. Experimental evolution. Trends Ecol. Evol. 27, 547–560 (2012).
Hartl, D. L. & Clark, A. G. Principles of Population Genetics (Sinauer Associates, Inc., 2007).
Mardis, E. R. Next-generation DNA sequencing methods. Annu. Rev. Genom. Hum. Genet. 9, 387–402 (2008).
Schadt, E. E., Turner, S. & Kasarskis, A. A window into third-generation sequencing. Hum. Mol. Genet. 19, R227–R240 (2010).
Halligan, D. L. & Keightley, P. D. Spontaneous mutation accumulation studies in evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 40, 151–172 (2009).
Lynch, M. et al. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl Acad. Sci. USA 105, 9272–9277 (2008).
Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92–94 (2010).
Keightley, P. D. et al. Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res. 19, 1195–1201 (2009).
Denver, D. R. et al. A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc. Natl Acad. Sci. USA 106, 16310–16314 (2009).
Lind, P. A. & Andersson, D. I. Whole-genome mutational biases in bacteria. Proc. Natl Acad. Sci. USA 105, 17878–17883 (2008).
Lee, H., Popodi, E., Tang, H. & Foster, P. L. Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc. Natl Acad. Sci. USA 109, E2774–E2783 (2012).
Sung, W., Ackerman, M. S., Miller, S. F., Doak, T. G. & Lynch, M. Drift-barrier hypothesis and mutation-rate evolution. Proc. Natl Acad. Sci. USA 109, 18488–18492 (2012).
Drake, J. W. Spontaneous mutation. Annu. Rev. Genet. 25, 125–146 (1991).
Lynch, M. The Origins of Genome Architecture (Sinauer Associates, Inc., 2007).
Friedberg, E. C. et al. DNA Repair and Mutagenesis (American Society for Microbiology Press, 2006).
Bull, J. J., Badgett, M. R., Rokyta, D. & Molineux, I. J. Experimental evolution yields hundreds of mutations in a functional viral genome. J. Mol. Evol. 57, 241–248 (2003).
Domingo-Calap, P., Cuevas, J. M. & Sanjuán, R. The fitness effects of random mutations in single-stranded DNA and RNA bacteriophages. PLoS Genet. 5, e1000742 (2009).
Drake, J. W., Charlesworth, B., Charlesworth, D. & Crow, J. F. Rates of spontaneous mutation. Genetics 148, 1667–1686 (1998).
Springman, R., Keller, T., Molineux, I. J. & Bull, J. J. Evolution at a high imposed mutation rate: adaptation obscures the load in phage T7. Genetics 184, 221–232 (2010).
Ames, B. N., Durston, W. E., Yamasaki, E. & Lee, F. D. Carcinogens are mutagens: a simple test system combining liver homogenates for activation and bacteria for detection. Proc. Natl Acad. Sci. USA 70, 2281–2285 (1973).
Savageau, M. A. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am. Nat. 122, 732–744 (1983).
Orr, H. A. Fitness and its role in evolutionary genetics. Nature Rev. Genet. 10, 531–539 (2009).
Atwood, K. C., Schneider, L. K. & Ryan, F. J. Periodic selection in Escherichia coli. Proc. Natl Acad. Sci. USA 37, 146–155 (1951).
This study is a classic early demonstration of adaptive evolution in experimental populations of bacteria.
Fogle, C. A., Nagle, J. L. & Desai, M. M. Clonal interference, multiple mutations and adaptation in large asexual populations. Genetics 180, 2163–2173 (2008).
Lang, G. I. et al. Pervasive genetic hitchhiking and clonal interference in 40 evolving yeast populations. Nature 500, 571–574 (2013).
This paper presents the most detailed analysis so far of the dynamics of mutations in asexual populations, including the effects of clonal interference, by metagenomic sequencing.
Barrick, J. E. et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243–1247 (2009).
This paper describes the first application of whole-genome sequencing to the LTEE and includes discussions of genetic parallelism, changes in mutation rates and evolution in the optimization regime.
Wagner, A. The Origins of Evolutionary Innovations (Oxford Univ. Press, 2011).
Velicer, G. J. et al. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc. Natl Acad. Sci. USA 103, 8107–8112 (2006).
This study is the first to use whole-genome sequencing to discover the genetic basis of an innovative change in the lifestyle of an organism that occurred during an evolution experiment.
Yu, Y.-T. N., Yuan, X. & Velicer, G. J. Adaptive evolution of an sRNA that controls Myxococcus development. Science 328, 993 (2010).
Marchetti, M. et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8, e1000280 (2010).
Ratcliff, W. C., Denison, R. F., Borrello, M. & Travisano, M. Experimental evolution of multicellularity. Proc. Natl Acad. Sci. USA 109, 1595–1600 (2012).
Mortlock, R. P. (ed.) Microorganisms as Model Systems for Studying Evolution (Plenum Press, 1984).
Blount, Z. D., Borland, C. Z. & Lenski, R. E. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl Acad. Sci. USA 105, 7899–7906 (2008).
Blount, Z. D., Barrick, J. E., Davidson, C. J. & Lenski, R. E. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489, 513–518 (2012).
This paper describes the genetic basis of the evolution of citrate use in the LTEE, including the potentiation, actualization and refinement stages of this innovation.
Conrad, T. M., Lewis, N. E. & Palsson, B. O. Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol. 7, 509 (2011).
Minty, J. J. et al. Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Microb. Cell Fact. 10, 18 (2011).
Blaby, I. K. et al. Experimental evolution of a facultative thermophile from a mesophilic ancestor. Appl. Environ. Microbiol. 78, 144–155 (2012).
Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457–461 (2012).
This study uses whole-genome sequencing of a large number of independently evolved populations to examine the diversity of alternative genetic pathways that lead to improved fitness at high temperature.
Harris, D. R. et al. Directed evolution of ionizing radiation resistance in Escherichia coli. J. Bacteriol. 191, 5240–5252 (2009).
Zhang, Q. et al. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333, 1764–1767 (2011).
This study shows that migration between populations living in environments with different selection strengths can speed up adaptation.
Pepin, K. M. & Wichman, H. A. Experimental evolution and genome sequencing reveal variation in levels of clonal interference in large populations of bacteriophage ΦX174. BMC Evol. Biol. 8, 85 (2008).
Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature 387, 703–705 (1997).
Brown, C. T. et al. Whole genome sequencing and phenotypic analysis of mutations found in Bacillus subtilis following evolution under relaxed selection for sporulation. Appl. Env. Microbiol. 77, 6867–6877 (2011).
Aguilar, C. et al. Genetic changes during a laboratory adaptive evolution process that allowed fast growth in glucose to an Escherichia coli strain lacking the major glucose transport system. BMC Genomics 13, 385 (2012).
Mao, E. F., Lane, L., Lee, J. & Miller, J. H. Proliferation of mutators in a cell population. J. Bact. 179, 417–422 (1997).
Lenski, R. E. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breed. Rev. 24, 225–265 (2004).
Desai, M. M. & Fisher, D. S. The balance between mutators and nonmutators in asexual populations. Genetics 188, 997–1014 (2011).
Sniegowski, P. D., Gerrish, P. J., Johnson, T. & Shaver, A. The evolution of mutation rates: separating causes from consequences. BioEssays 22, 1057–1066 (2000).
Wielgoss, S. et al. Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc. Natl Acad. Sci. USA 110, 222–227 (2013).
McDonald, M. J., Hsieh, Y.-Y., Yu, Y.-H., Chang, S.-L. & Leu, J.-Y. The evolution of low mutation rates in experimental mutator populations of Saccharomyces cerevisiae. Curr. Biol. 22, 1235–1240 (2012).
Denamur, E. et al. Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103, 711–721 (2000).
Woods, R. J. et al. Second-order selection for evolvability in a large Escherichia coli population. Science 331, 1433–1436 (2011).
This study uses replay experiments to demonstrate that antagonistic epistasis can lead some genotypes towards an adaptive cul-de-sac and eventual extinction.
Darwin, C. The Origin of Species by Means of Natural Selection (John Murray, 1859).
Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. Evolutionary consequences of niche construction and their implications for ecology. Proc. Natl Acad. Sci. USA 96, 10242–10247 (1999).
Rozen, D. E., Schneider, D. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. XIII. Phylogenetic history of a balanced polymorphism. J. Mol. Evol. 61, 171–180 (2005).
Le Gac, M., Plucain, J., Hindré, T., Lenski, R. E. & Schneider, D. Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA 109, 9487–9492 (2012).
Rozen, D. E., Philippe, N., Arjan De Visser, J., Lenski, R. E. & Schneider, D. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol. Lett. 12, 34–44 (2009).
Barrick, J. E. & Lenski, R. E. Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 74, 119–129 (2009).
Zambrano, M. M., Siegele, D. A., Almirón, M., Tormo, A. & Kolter, R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259, 1757–1760 (1993).
Finkel, S. E. Long-term survival during stationary phase: evolution and the GASP phenotype. Nature Rev. Microbiol. 4, 113–120 (2006).
Treves, D. S., Manning, S. & Adams, J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15, 789–797 (1998).
Maharjan, R., Seeto, S., Notley-McRobb, L. & Ferenci, T. Clonal adaptive radiation in a constant environment. Science 313, 514–517 (2006).
Maharjan, R. P. et al. The multiplicity of divergence mechanisms in a single evolving population. Genome Biol. 13, R41 (2012).
This paper uses whole-genome sequencing to uncover extensive genetic diversity in populations that are evolving in chemostats.
Saxer, G., Doebeli, M. & Travisano, M. The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment. PLoS ONE 5, e14184 (2010).
Herron, M. D. & Doebeli, M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11, e1001490 (2013).
This study examines whole-population genetic dynamics in a system that diversified into two ecotypes which coexisted owing to different strategies for nutrient use.
Korona, R., Nakatsu, C. H., Forney, L. J. & Lenski, R. E. Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc. Natl Acad. Sci. USA 91, 9037–9041 (1994).
Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).
Traverse, C. C., Mayo-Smith, L. M., Poltak, S. R. & Cooper, V. S. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc. Natl Acad. Sci. USA 110, E250–E259 (2013).
This study characterizes the mutational pathways by which ecotypes from a primary niche evolved to displace ecotypes that were established in other niches.
Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010).
This study uses whole-genome sequencing of a bacteriophage to observe Red Queen dynamics.
Pal, C., Maciá, M. D., Oliver, A., Schachar, I. & Buckling, A. Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450, 1079–1081 (2007).
Meyer, J. R. et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335, 428–432 (2012).
This paper characterizes multistep genetic pathways that lead to an innovative host–receptor shift in bacteriophage populations and shows that the shift is contingent on the evolutionary trajectory of the bacterial host populations.
Muller, H. Genetic aspects of sex. Am. Nat. 66, 118–138 (1932).
Cooper, T. F. Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biol. 5, e225 (2007).
This study uses knowledge of the genetic targets of selection to show that plasmid-mediated recombination accelerates adaptive evolution by overcoming clonal interference.
Burke, M. K. et al. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587–590 (2010).
This paper presents one of the first analyses based on whole-genome sequencing to characterize experimentally evolved populations of a sexual multicellular organism.
Zhou, D. et al. Experimental selection of hypoxia-tolerant Drosophila melanogaster. Proc. Natl Acad. Sci. USA 108, 2349–2354 (2011).
This paper uses extensive sequencing to identify targets of selection in another set of experimentally evolved populations of a sexual multicellular organism.
Izutsu, M. et al. Genome features of “Dark-fly”, a Drosophila line reared long-term in a dark environment. PLoS ONE 7, e33288 (2012).
Ferenci, T. et al. Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J. Bacteriol. 191, 4025–4029 (2009).
Nahku, R. et al. Stock culture heterogeneity rather than new mutational variation complicates short-term cell physiology studies of Escherichia coli K-12 MG1655 in continuous culture. Microbiology 157, 2604–2610 (2011).
Hobman, J. L. et al. Comparative genomic hybridization detects secondary chromosomal deletions in Escherichia coli K-12 MG1655 mutants and highlights instability in the flhDC region. J. Bacteriol. 189, 8786–8792 (2007).
Pósfai, G. et al. Emergent properties of reduced-genome Escherichia coli. Science 312, 1044–1046 (2006).
Studier, F. W., Daegelen, P., Lenski, R. E., Maslov, S. & Kim, J. F. Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21(DE3) and comparison of the E. coli B and K-12 genomes. J. Mol. Biol. 394, 653–680 (2009).
Gibson, D. G. et al. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329, 52–56 (2010).
Isaacs, F. J. et al. Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333, 348–353 (2011).
Yang, L. et al. Evolutionary dynamics of bacteria in a human host environment. Proc. Natl Acad. Sci. USA 108, 7481–7486 (2011).
Lieberman, T. D. et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nature Genet. 43, 1275–1280 (2011).
This study uses whole-genome sequencing to investigate adaptation of a bacterial pathogen during a multi-decade outbreak in a human population; although this is not based on an experiment, it relies on inferential approaches similar to those used in experimental evolution.
Sprouffske, K., Merlo, L. M. F., Gerrish, P. J., Maley, C. C. & Sniegowski, P. D. Cancer in light of experimental evolution. Curr. Biol. 22, R762–R771 (2012).
Loewe, L. & Hill, W. G. The population genetics of mutations: good, bad and indifferent. Phil. Trans. R. Soc. 365, 1153–1167 (2010).
Eyre-Walker, A. & Keightley, P. D. The distribution of fitness effects of new mutations. Nature Rev. Genet. 8, 610–618 (2007).
De Visser, J. A. G. M., Cooper, T. F. & Elena, S. F. The causes of epistasis. Phil. Trans. R. Soc. 278, 3617–3624 (2011).
Kondrashov, F. A. & Kondrashov, A. S. Measurements of spontaneous rates of mutations in the recent past and the near future. Phil. Trans. R. Soc. 365, 1169–1176 (2010).
Khan, A. I., Dinh, D. M., Schneider, D., Lenski, R. E. & Cooper, T. F. Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332, 1193–1196 (2011).
Chou, H.-H., Chiu, H.-C., Delaney, N. F., Segrè, D. & Marx, C. J. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332, 1190–1192 (2011).
Kvitek, D. J. & Sherlock, G. Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet. 7, e1002056 (2011).
Philippe, N., Crozat, E., Lenski, R. E. & Schneider, D. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. BioEssays 29, 846–860 (2007).
Wagner, A. Neutralism and selectionism: a network-based reconciliation. Nature Rev. Genet. 9, 965–974 (2008).
Heard, S. & Hauser, D. Key evolutionary innovations and their ecological mechanisms. Histor. Biol. 10, 151–173 (1995).
Lenski, R. E. & Travisano, M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl Acad. Sci. USA 91, 6808–6814 (1994).
Carroll, S. M. & Marx, C. J. Evolution after introduction of a novel metabolic pathway consistently leads to restoration of wild-type physiology. PLoS Genet. 9, e1003427 (2013).
Wichman, H. A., Badgett, M. R., Scott, L. A., Boulianne, C. M. & Bull, J. J. Different trajectories of parallel evolution during viral adaptation. Science 285, 422–424 (1999).
This paper is one of the first to use whole-genome sequencing to examine the nature of genetic changes during an adaptive evolution experiment.
Woods, R., Schneider, D., Winkworth, C. L., Riley, M. A. & Lenski, R. E. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA 103, 9107–9112 (2006).
Bull, J. J. et al. Exceptional convergent evolution in a virus. Genetics 147, 1497–1507 (1997).
Crozat, E. et al. Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Mol. Biol. Evol. 27, 2113–2128 (2010).
Jerome, J. P. et al. Standing genetic variation in contingency loci drives the rapid adaptation of Campylobacter jejuni to a novel host. PLoS ONE 6, e16399 (2011).
Lee, M.-C. & Marx, C. J. Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet. 8, e1002651 (2012).
Cooper, V. S., Schneider, D., Blot, M. & Lenski, R. E. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183, 2834–2841 (2001).
Paquin, C. E. & Adams, J. Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306, 368–370 (1983).