Long-Term Experimental Evolution in Escherichia coli. XIII. Phylogenetic History of a Balanced Polymorphism (original) (raw)
Abstract
We investigated the phylogenetic history of a balanced polymorphism that evolved in an experimental population of Escherichia coli. Previous work showed that two ecologically and morphologically distinct types, designated L (large) and S (small), arose by generation 6000 and coexisted for more than 12,000 generations thereafter. Here, we performed RFLP analyses using Insertion Sequence elements to resolve the phylogenetic history of L and S. Specifically, we sought to determine whether the derived S morph was monophyletic, indicating a long history of coexistence with L or, alternatively, S was repeatedly regenerated from L, indicating a series of periods with only transiently stable coexistence. Phylogenetic analysis of some 200 clones collected throughout the history of this population demonstrates that S is monophyletic. We then performed competition assays using clones of both morphs from different generations to determine whether either or both lineages continued to undergo genetic adaptation. Indeed, both lineages continued to adapt, and their continued evolution contributed to fluctuations in their relative abundance over evolutionary time. Based on their phylogenetic history and independent evolutionary trajectories, S and L fulfill Cohan’s criteria for being different asexual species.
Access this article
Subscribe and save
- Starting from 10 chapters or articles per month
- Access and download chapters and articles from more than 300k books and 2,500 journals
- Cancel anytime View plans
Buy Now
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Instant access to the full article PDF.
Similar content being viewed by others
References
- KC Atwood LK Schneider FJ Ryan (1951)ArticleTitlePeriodic selection in Escherichia coli Proc Natl Acad Sci USA 37 146–155Occurrence Handle14808170
PubMed Google Scholar - M Blot (1994)ArticleTitleTransposable elements and adaptation of host bacteria_Genetica_ 93 5–12Occurrence Handle10.1007/BF01435235Occurrence Handle7813917
Article PubMed Google Scholar - M Blot B Hauer G Monnet (1994)ArticleTitleThe Tn5 bleomycin resistance gene confers improved survival and growth advantage on Escherichia coli Mol Gen Genet 242 595–601Occurrence Handle10.1007/BF00285283Occurrence Handle7510018
Article PubMed Google Scholar - A Buckling PB Rainey (2002)ArticleTitleAntagonistic coevolution between a bacterium and a bacteriophage_Proc Roy Soc London B_ 269 931–936Occurrence Handle10.1098/rspb.2001.1945
Article Google Scholar - JJ Bull MR Badgett HA Wichman JP Huelsenbeck DM Hillis A Gulati C Ho IJ Molineux (1997)ArticleTitleExceptional convergent evolution in a virus_Genetics_ 147 1497–1507Occurrence Handle9409816
PubMed Google Scholar - FM Cohan (2002)ArticleTitleWhat are bacterial species_Annu Rev Microbiol_ 56 457–487Occurrence Handle10.1146/annurev.micro.56.012302.160634Occurrence Handle12142474
Article PubMed Google Scholar - VS Cooper RE Lenski (2000)ArticleTitleThe population genetics of ecological specialization in evolving E. coli populations_Nature_ 407 736–739Occurrence Handle10.1038/35037572Occurrence Handle11048718
Article PubMed Google Scholar - VS Cooper D Schneider M Blot RE Lenski (2001)ArticleTitleMechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B_J Bacteriol_ 183 2834–2841Occurrence Handle10.1128/JB.183.9.2834-2841.2001Occurrence Handle11292803
Article PubMed Google Scholar - JAGM VisserParticlede ADL Akkermans RF Hoekstra WM VosParticlede (2004)ArticleTitleInsertion-sequence-mediated mutations isolated during adaptation to growth and starvation in Lactococcus lactis Genetics 168 1145–1157Occurrence Handle10.1534/genetics.104.032136Occurrence Handle15579676
Article PubMed Google Scholar - SF Elena RE Lenski (1997)ArticleTitleLong-term experimental evolution in Escherichia coli. VII. Mechanisms maintaining genetic variability within populations_Evolution_ 51 1058–1067
Google Scholar - M Friesen G Saxer M Travisano M Doebeli (2004)ArticleTitleExperimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli Evolution 58 245–260Occurrence Handle15068343
PubMed Google Scholar - PJ Gerrish RE Lenski (1998)ArticleTitleThe fate of competing beneficial mutations in an asexual population_Genetica_ 102/103 127–144Occurrence Handle10.1023/A:1017067816551
Article Google Scholar - RB Helling CN Vargas J Adams (1988)ArticleTitleEvolution of Escherichia coli during growth in a constant environment_Genetics_ 116 349–358
Google Scholar - RE Lenski (2004)ArticleTitlePhenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli Plant Breed Rev 24 225–265
Google Scholar - RE Lenski M Travisano (1994)ArticleTitleDynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations_Proc Natl Acad Sci USA_ 91 6808–6814Occurrence Handle8041701
PubMed Google Scholar - RE Lenski MR Rose SC Simpson SC Tadler (1991)ArticleTitleLong-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations_Am Nat_ 138 1315–1341Occurrence Handle10.1086/285289
Article Google Scholar - BR Levin (1981)ArticleTitlePeriodic selection, infectious gene exchange and the genetic structure of Escherichia coli populations_Genetics_ 99 1–23Occurrence Handle7042453
PubMed Google Scholar - E Mayr (1944) Systematics and the origin of species from the viewpoint of a zoologist Columbia University Press New York
Google Scholar - H Ochman AS Gerber DL Hartl (1987)ArticleTitleGenetic applications of an inverse polymerase chain reaction_Genetics_ 120 621–623
Google Scholar - D Papadopoulos D Schneider J Meier-Eiss W Arber RE Lenski M Blot (1999)ArticleTitleGenomic evolution during a 10,000-generation experiment with bacteria_Proc Natl Acad Sci USA_ 96 3807–3812Occurrence Handle10.1073/pnas.96.7.3807Occurrence Handle10097119
Article PubMed Google Scholar - PB Rainey M Travisano (1998)ArticleTitleAdaptive radiation in a heterogeneous environment_Nature_ 394 69–72Occurrence Handle10.1038/27900Occurrence Handle9665128
Article PubMed Google Scholar - PB Rainey A Buckling R Kassen M Travisano (2000)ArticleTitleThe emergence and maintenance of diversity: insights from experimental bacterial populations_Trends Ecol Evol_ 15 243–247Occurrence Handle10.1016/S0169-5347(00)01871-1Occurrence Handle10802550
Article PubMed Google Scholar - WR Rice (1989)ArticleTitleAnalyzing tables of statistical tests_Evolution_ 43 223–225
Google Scholar - RF Rosenzweig RR Sharp DS Treves J Adams (1994)ArticleTitleMicrobial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli Genetics 137 903–917Occurrence Handle7982572
PubMed Google Scholar - DE Rozen RE Lenski (2000)ArticleTitleLong-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism_Am Nat_ 155 24–35Occurrence Handle10.1086/303299Occurrence Handle10657174
Article PubMed Google Scholar - J Sambrook EF Fitsch T Maniatis (1989) Molecular cloning Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
Google Scholar - D Schneider E Duperchy E Coursange RE Lenski M Blot (2000)ArticleTitleLong-term experimental evolution in Escherichia coli. IX. Characterization of Insertion Sequence-mediated mutations and rearrangements_Genetics_ 156 477–488Occurrence Handle11014799
PubMed Google Scholar - FM Stewart BR Levin (1972)ArticleTitlePartitioning of resources and the outcome of interspecific competition: a model and some general considerations_Am Nat_ 107 171–198Occurrence Handle10.1086/282825
Article Google Scholar - DL Swofford (1998) PAUP: phylogenetic analysis using parsimony Sinauer Sunderland, MA
Google Scholar - DS Treves S Manning J Adams (1998)ArticleTitleRepeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli Mol Biol Evol 15 789–797Occurrence Handle9656481
PubMed Google Scholar
Acknowledgments
This collaborative project began in the laboratory of Prof. Michel Blot (Université Joseph Fourier, Grenoble), who died before our work was completed. We dedicate this paper to his memory. We thank V. Cooper, A. de Visser, M. Habets, S. Remold, and two anonymous reviewers for helpful comments on the manuscript and N. Hajela for her valuable assistance in the laboratory. Funding was provided by the U.S. National Science Foundation and by the French CNRS.
Author information
Author notes
- Daniel E. Rozen
Present address: Department of Biology, Emory University, Atlanta, GA, 30322, USA
Authors and Affiliations
- Ecology, Evolutionary Biology, and Behavior Program, Michigan State University, East Lansing, MI, 48824, USA
Daniel E. Rozen - Laboratoire Adaptation et Pathogénie des Microorganismes, Université Joseph Fourier, CNRS UMR5163, Institut Jean Roget, 38700, La Tronche, France
Dominique Schneider - Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA
Richard E. Lenski
Authors
- Daniel E. Rozen
- Dominique Schneider
- Richard E. Lenski
Corresponding author
Correspondence toRichard E. Lenski.
Additional information
[Reviewing Editor: Niles Lehman]
Rights and permissions
About this article
Cite this article
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). https://doi.org/10.1007/s00239-004-0322-2
- Received: 11 November 2004
- Accepted: 01 February 2005
- Published: 27 June 2005
- Issue date: August 2005
- DOI: https://doi.org/10.1007/s00239-004-0322-2