Abstract
Evolution is an on-going process, and it can be studied experimentally in organisms with rapid generations. My team has maintained 12 populations of Escherichia coli in a simple laboratory environment for >25 years and 60 000 generations. We have quantified the dynamics of adaptation by natural selection, seen some of the populations diverge into stably coexisting ecotypes, described changes in the bacteria’s mutation rate, observed the new ability to exploit a previously untapped carbon source, characterized the dynamics of genome evolution and used parallel evolution to identify the genetic targets of selection. I discuss what the future might hold for this particular experiment, briefly highlight some other microbial evolution experiments and suggest how the fields of experimental evolution and microbial ecology might intersect going forward.
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References
Antonovics J . (1976). The input from population genetics: the new ecological genetics. Syst Bot 1: 233–245.
Bachmann H, Fischlechner M, Rabbers I, Barfa N, Branco dos Santos F, Molenaar D et al. (2013). Availability of public goods shapes the evolution of competing metabolic strategies. Proc Natl Acad Sci USA 110: 14302–14307.
Barrick JE, Lenski RE . (2009). Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 74: 119–129.
Barrick JE, Lenski RE . (2013). Genome dynamics during experimental evolution. Nat Rev Gen 14: 827–839.
Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D et al. (2009). Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243–1247.
Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I et al. (2016). Spatiotemporal microbial evolution on antibiotic landscapes. Science 353: 1147–1151.
Bell G . (1997) Selection: The Mechanism of Evolution. Chapman & Hall: New York.
Bell G . (2012). Evolutionary rescue of a green alga kept in the dark. Biol Lett 9: 20120823.
Bendall ML, Stevens SLR, Chan L-K, Malfatti S, Schwientek P, Tremblay J et al. (2016). Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. ISME J 10: 1589–1601.
Blount ZD, Borland CZ, Lenski RE . (2008). Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105: 7899–7906.
Blount ZD, Barrick JE, Davidson CJ, Lenski RE . (2012). Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489: 513–518.
Brockhurst MA, Koskella B . (2013). Experimental coevolution of species interactions. Trends Ecol Evol 28: 367–375.
Buckling A, Maclean RC, Brockhurst MA, Colegrave N . (2009). The Beagle in a bottle. Nature 457: 824–829.
Bull JJ, Molineux IJ, Rice WR . (1991). Selection of benevolence in a host-parasite system. Evolution 45: 875–882.
Burke MK, Dunham JP, Shahrestani P, Thornton KR, Rose MR, Long AD . (2010). Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467: 587–590.
Burch CL, Chao L . (1999). Evolution by small steps and rugged landscapes in the RNA virus φ6. Genetics 151: 921–927.
Chao L, Levin BR, Stewart FM . (1977). A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58: 369–378.
Cooper TF . (2007). Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biol 5: 1899–1905.
Cooper TF, Rozen DE, Lenski RE . (2003). Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci USA 100: 1072–1077.
Cooper VS, Schneider D, Blot M, Lenski RE . (2001). Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of E. coli B. J Bacteriol 183: 2834–2841.
Crozat E, Philippe N, Lenski RE, Geiselmann J, Schneider D . (2005). Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169: 523–532.
Deatherage DE, Barrick JE . (2014). Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 1151: 165–188.
Denef VJ, Mueller RS, Banfield JF . (2010). AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4: 599–610.
Dennehy JJ, Friedenberg NA, Holt RD, Turner PE . (2006). Viral ecology and the maintenance of novel host use. Am Nat 167: 429–439.
de Visser JAGM, Lenski RE . (2002). Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation. BMC Evol Biol 2: 169.
de Visser JAGM, Rozen DE . (2006). Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli. Genetics 172: 2093–2100.
Dionisio F, Conceicao IC, Marques ACR, Fernandes L, Gordo I . (2005). The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett 1: 250–252.
Dixit PD, Pang TY, Studier FW, Maslov S . (2015). Recombinant transfer in the basic genome of Escherichia coli. Proc Natl Acad Sci USA 112: 9070–9075.
Elena SF, Lenski RE . (2003). Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Gen 4: 457–469.
Ensminger AW, Yassin Y, Miron A, Isberg RR . (2012). Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Path 8: e1002731.
Fiegna F, Yu YTN, Kadam SV, Velicer GJ . (2006). Evolution of an obligate social cheater to a superior cooperator. Nature 441: 310–314.
Fox JW, Lenski RE . (2015). From here to eternity–the theory and practice of a really long experiment. PLoS Biol 13: e1002185.
Garland T Jr, Rose MR, eds. (2009) Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. University of California Press: Berkeley, CA, USA.
Gerrish PJ, Lenski RE . (1998). The fate of competing beneficial mutations in an asexual population. Genetica 102/103: 127–144.
Gerstein AC, Chun H-JE, Grant A, Otto SP . (2006). Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2: e145.
Gómez P, Buckling A . (2011). Bacteria-phage antagonistic coevolution in soil. Science 332: 106–109.
Gómez P, Buckling A . (2013). Real-time microbial adaptive diversification in soil. Ecol Lett 16: 650–655.
Good BH, Desai MM . (2016). Evolution of mutation rates in rapidly adapting asexual populations. Genetics 204: 1249–1266.
Grant PR, Grant BR . (2014) 40 Years of Evolution: Darwin’s Finches on Daphne Major Island. Princeton University Press: Princeton, NJ, USA.
Großkopf T, Consuegra J, Gaffé J, Willison J, Lenski RE, Soyer OS et al. (2016). Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment. BMC Evol Biol 16: 163.
Hegreness M, Shoresh N, Hartl D, Kishony R . (2006). An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311: 1615–1617.
Hillesland KL, Stahl DA . (2010). Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci USA 107: 2124–2129.
Hoang KL, Morran LT, Gerardo NM . (2016). Experimental evolution as an underutilized tool for studying beneficial animal–microbe interactions. Front Microbiol 7: 1444.
Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR et al. (2015). Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nat Comm 6: 8155.
Kacar B, Tran LI, Ge X, Sanyal S, Gaucher EA . (2017). Experimental evolution of Escherichia coli harboring an ancient translation protein. J Mol Evol 84: 69–84.
Kao KC, Sherlock G . (2008). Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Gen 40: 1499–1504.
Kassen R . (2014) Experimental Evolution and the Nature of Biodiversity. Roberts: Denver, CO, USA.
Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC . (2012). Experimental evolution. Trends Ecol Evol 27: 547–560.
Kerr B, Neuhauser C, Bohannan BJM, Dean AM . (2006). Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons'. Nature 442: 75–78.
Khan AI, Dinh DM, Schneider D, Lenski RE, Cooper TF . (2011). Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332: 1193–1196.
Kryazhimskiy S, Rice DP, Jerison ER, Desai MM . (2014). Global epistasis makes adaptation predictable despite sequence-level stochasticity. Science 344: 1519–1522.
Kuzdzal-Fick JJ, Fox SA, Strassmann JE, Queller DC . (2011). High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science 334: 1548–1551.
Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D et al. (2013). Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571–574.
Le Gac M, Plucain J, Hindré T, Lenski RE, Schneider D . (2012). Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proc Natl Acad Sci USA 109: 9487–9492.
Lenski RE, Travisano M . (1994). Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci USA 91: 6808–6814.
Lenski RE, Rose MR, Simpson SC, Tadler SC . (1991). Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138: 1315–1341.
Levy SF, Blundell JR, Venkataram S, Petrov DA, Fisher DS, Sherlock G . (2015). Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519: 181–186.
Lieberman TD, Michel J-B, Aingaran M, Potter-Bynoe G, Roux D, Davis MR et al. (2011). Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Gen 43: 1275–1280.
Lindsey HA, Gallie J, Taylor S, Kerr B . (2013). Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494: 463–467.
Losos JB, Jackman TR, Larson A, de Queiroz K, Rodríguez-Schettino L . (1998). Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115–2118.
Maddamsetti R, Lenski RE, Barrick JE . (2015). Adaptation, clonal interference, and frequency-dependent interactions in a long-term evolution experiment with Escherichia coli. Genetics 200: 619–631.
Meyer JR, Kassen R . (2007). The effects of competition and predation on diversification in a model adaptive radiation. Nature 446: 432–435.
Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, Lenski RE . (2012). Repeatability and contingency in the evolution of a key innovation in phage Lambda. Science 335: 428–432.
Meyer JR, Dobias DT, Medina SJ, Servilio L, Gupta A, Lenski RE . (2016). Ecological speciation of bacteriophage Lambda in allopatry and sympatry. Science 354: 1301–1304.
Moore FBG, Woods R . (2006). Tempo and constraint of adaptive evolution in Escherichia coli (Enterobacteriaceae, Enterobacteriales). Biol J Linn Soc 88: 403–411.
Moore FBG, Rozen DE, Lenski RE . (2000). Pervasive compensatory adaptation in Escherichia coli. Proc R Soc Lond B 267: 515–522.
Ochman H, Elwyn S, Moran NA . (1999). Calibrating bacterial evolution. Proc Natl Acad Sci USA 96: 12638–12643.
Paquin CE, Adams J . (1983). Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306: 368–371.
Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M . (1999). Genomic evolution during a 10 000-generation experiment with bacteria. Proc Natl Acad Sci USA 96: 3807–3812.
Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR et al. (2010). Antagonistic coevolution accelerates molecular evolution. Nature 464: 275–278.
Pelosi L, Kühn L, Guetta D, Garin J, Geiselmann J, Lenski RE et al. (2006). Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173: 1851–1869.
Poltak SR, Cooper VS . (2011). Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 5: 369–378.
Quandt EM, Deatherage DE, Ellington AD, Georgiou G, Barrick JE . (2014). Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli. Proc Natl Acad Sci USA 111: 2217–2222.
Quandt EM, Gollihar J, Blount ZD, Ellington AD, Georgiou G, Barrick JE . (2015). Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment. eLife 4: e09696.
Raeside C, Gaffé J, Deatherage DE, Tenaillon O, Briska A, Ptashkin RN et al. (2014). Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. mBio 5: e01377–14.
Rainey PB, Travisano M . (1998). Adaptive radiation in a heterogeneous environment. Nature 394: 69–72.
Ratcliff WC, Denison RF, Borrello M, Travisano M . (2012). Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109: 1595–1600.
Rosenzweig RF, Sharp RR, Treves DS, Adams J . (1994). Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137: 903–917.
Rozen DE, Lenski RE . (2000). Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. Am Nat 155: 24–35.
Scheinin M, Riebesell U, Rynearson TA, Lohbeck KT, Collins S . (2015). Experimental evolution gone wild. J Roy Soc Interface 12: 20150056.
Schlüter L, Lohbeck KT, Gröger JP, Riebesell U, Reusch TBH . (2016). Long-term dynamics of adaptive evolution in a globally important phytoplankton species to ocean acidification. Sci Adv 2: e1501660.
Schneider D, Duperchy E, Coursange E, Lenski RE, Blot M . (2000). Long-term experimental evolution in Escherichia coli. IX. Characterization of IS-mediated mutations and rearrangements. Genetics 156: 477–488.
Schrag SJ, Perrot V, Levin BR . (1997). Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc Lond B 264: 1287–1291.
Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabo G et al. (2012). Population genomics of early events in the ecological differentiation of bacteria. Science 336: 48–51.
Sniegowski PD, Gerrish PJ, Lenski RE . (1997). Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387: 703–705.
Sota M, Yano H, Hughes JM, Daughdrill GW, Abdo Z, Forney LJ et al. (2010). Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein. ISME J 4: 1568–1580.
Soto W, Punke EB, Nishiguchi MK . (2012). Evolutionary perspectives in a mutualism of sepiolid squid and bioluminescent bacteria: combined usage of microbial experimental evolution and temporal population genetics. Evolution 66: 1308–1321.
Tagkopoulos I, Liu Y-C, Tavazoie S . (2008). Predictive behavior within microbial genetic networks. Science 320: 1313–1317.
Tenaillon O, Taddei F, Radman M, Matic I . (2001). Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res Microbiol 152: 11–16.
Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD et al. (2012). The molecular diversity of adaptive convergence. Science 335: 457–461.
Tenaillon O, Barrick JE, Ribeck N, Deatherage DE, Blanchard JL, Dasgupta A et al. (2016). Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536: 165–170.
Toprak E, Veres A, Michel J-B, Chait R, Hartl DL, Kishony R . (2012). Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Gen 44: 101–105.
Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS . (2013). Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci USA 110: E250–E259.
Turner CB . (2015) Experimental Evolution and Ecological Consequences: New Niches and Changing Soichiometry PhD. Michigan State University: East Lansing, Michigan.
Turner CB, Blount ZD, Lenski RE . (2015). Replaying evolution to test the cause of extinction of one ecotype in an experimentally evolved population. PLoS One 10: e0142050.
Van Ditmarsch D, Boyle KE, Sakhtah H, Oyler JE, Nadell CD, Déziel E et al. (2013). Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria. Cell Rep 4: 697–708.
Vasi F, Travisano M, Lenski RE . (1994). Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am Nat 144: 432–456.
Velicer GJ, Raddatz G, Keller H, Deiss S, Lanz C, Dinkelacker I et al. (2006). Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc Natl Acad Sci USA 103: 8107–8112.
Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ . (1999). Different trajectories of parallel evolution during viral adaptation. Science 285: 422–424.
Wichman HA, Scott LA, Yarber CD, Bull JJ . (2000). Experimental evolution recapitulates natural evolution. Phil Trans Roy Soc Lond 355: 1677–1684.
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT et al. (2016). Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J 10: 2557–2568.
Wielgoss S, Barrick JE, Tenaillon O, Wiser MJ, Dittmar WJ, Cruveiller S et al. (2013). Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc Natl Acad Sci USA 110: 222–227.
Wilke CO, Lenski RE, Adami C . (2003). Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3: 3.
Wiser MJ, Ribeck N, Lenski RE . (2013). Long-term dynamics of adaptation in asexual populations. Science 342: 1364–1367.
Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE . (2006). Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci USA 103: 9107–9112.
Woods RJ, Barrick JE, Cooper TF, Shrestha U, Kauth MR, Lenski RE . (2011). Second-order selection for evolvability in a large Escherichia coli population. Science 331: 1433–1436.
Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R . (1993). Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259: 1757–1760.
Acknowledgements
Thanks to everyone who has participated in the LTEE over the years including especially the unsung heroes—the technicians and lab managers Sue Simpson, Lynette Ekunwe and especially Neerja Hajela. Thanks also to Mike Wiser, Rohan Maddamsetti, Jeff Barrick, Zach Blount and Olivier Tenaillon for preparing figures, and to two reviewers for their helpful comments. The LTEE has been supported by grants from the National Science Foundation (currently DEB-1451740 and cooperative agreement DBI-0939454) and by the John Hannah Endowment at Michigan State University.
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Lenski, R. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J 11, 2181–2194 (2017). https://doi.org/10.1038/ismej.2017.69
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DOI: https://doi.org/10.1038/ismej.2017.69


