Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 23, 2008, Pages 7899-7906

  Blount, Zachary D ^a   Borland, Christina Z ^a   Lenski, Richard E ^a  

^a Michigan State University ^*  (United States)

Author keywords

Adaptation; Experimental evolution; Mutation; Selection

Indexed keywords

CITRIC ACID; GLUCOSE; ARABINOSE;

ADAPTATION; ARTICLE; ESCHERICHIA COLI; EVOLUTION; GROWTH CURVE; MUTATION; MUTATION RATE; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; BIOLOGICAL MODEL; CELL CLONE; ECOSYSTEM; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE;

ESCHERICHIA COLI;

ARABINOSE; CITRIC ACID; CLONE CELLS; ECOSYSTEM; ESCHERICHIA COLI; EVOLUTION; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; SELECTION (GENETICS);

EID: 45849093668     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0803151105     Document Type: Article

References (67)

1. Mani GS, Clarke BC (1990) Mutational order: A major stochastic process in evolution. Proc R Soc London B 240:29-37.
2. 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.
3. Cooper VS, Lenski RE (2000) The population genetics of ecological specialization in evolving E. coli populations. Nature 407:736-739.
4. Cooper TF, Remold SK, Lenski RE, Schneider D (2008) Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli. PLoS Genet 4:e35.
5. Jacob F (1977) Evolution and tinkering. Science 196:1161-1166.
6. Wright S (1988) Surfaces of selective value revisited. Am Nat 131:115-123.
7. Yedid G, Bell G (2002) Macroevolution simulated with autonomously replicating computer programs. Nature 420:810-812.
8. Weinreich DM, Watson RA, Chao L (2005) Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165-1174.
9. Weinreich DM, Delaney NF, DePristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
10. Lewontin RC (1966) Is nature probable or capricious? BioScience 16:25-27.
11. Gould SJ (1985) The paradox of the first tier:Anagenda for paleobiology. Paleobiology 11:2-12.
12. Jablonski D (1986) Background and mass extinctions: The alternation of macroevolutionary regimes. Science 231:129-133.
13. Gould SJ (1989) Wonderful Life (Norton, New York).
14. Gould, SJ (2002) The Structure of Evolutionary Theory (Belknap, Cambridge, MA).
15. Beatty J (2006) Replaying life's tape. J Philos 7:336-362.
16. Conway Morris S (2003) Life's Solution (Cambridge Univ Press, Cambridge, UK).
17. Van Valen LM (1991) How far does contingency rule? Evol Theory 10:47-52.
18. Dawkins R (1996) The Blind Watchmaker (Norton, New York).
19. Vermeij GJ (2006) Historical contingency and the purported uniqueness of evolutionary innovations. Proc Natl Acad Sci USA 103:1804-1809.
20. Travisano M, Mongold JA, Bennett AF, Lenski RE (1995) Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267:87-90.
21. Mongold JA, Bennett AF, Lenski RE (1999) Evolutionary adaptation to temperature. VII. Extension of the upper thermal limit of Escherichia coli. Evolution 53:386-394.
22. Lenski RE (2004) Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breed Rev 24:225-265.
23. 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.
24. 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.
25. Lenski RE, Mongold JA (2000) in Scaling in Biology, eds Brown J, West G (Oxford Univ Press, Oxford, UK), pp 221-235.
26. Novak M, Pfeiffer T, Lenski RE, Sauer U, Bonhoeffer S (2006) Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am Nat 168:242-251.
27. 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.
28. 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.
29. Pelosi L, et al. (2006) Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173:1851-1869.
30. 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 103:9107-9122.
31. Cooper VS, Schneider S, 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.
32. Lenski RE, Winkworth CL, Riley MA (2003) Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J Mol Evol 56:498-508.
33. Sniegowski PD, Gerrish PJ, Lenski RE (1997) Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387:703-705.
34. Travisano M, Vasi F, Lenski RE (1995) Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49:189-200.
35. Koser SA (1924) Correlation of citrate-utilization by members of the colon-aerogenes group with other differential characteristics and with habitat. J Bacteriol 9:59-77.
36. Scheutz F, Strockbine NA (2005) Genus I. Escherichia, Castellani and Chalmers 1919, Bergey's Manual of Systematic Bacteriology, Volume Two: The Proteobacteria, eds Garrity GM, Brenner DJ, Kreig NR, Staley JR (Springer, New York), pp 607-624.
37. Frost GE, Rosenberg H (1973) The inducible citrate-dependent iron transport system in Escherichia coli K-12. Biochim Biophys Acta 330:90-101.
38. Hussein S, Hantke K, Braun V (1981) Citrate-dependent iron transport system in Escherichia coli K-12. Eur J Biochem 117:431-437.
39. Lara FJS, Stokes JL (1952) Oxidation of citrate by Escherichia coli. J Bacteriol 63:415-420.
40. Lutgens M, Gottschalk G (1980) Why a co-substrate is required for anaerobic growth of Escherichia coli on citrate. J Gen Microbiol 199:63-70.
41. Hall BG (1982) Chromosomal mutation for citrate utilization by Escherichia coli K-12. J Bacteriol 151:269-273.
42. Reynolds CH, Silver S (1983) Citrate utilization by Escherichia coli: Plasmid- and chromosome-encoded systems. J Bacteriol 156:1019-1024.
43. Pos KM, Dimroth P, Bott M (1998) The Escherichia coli citrate carrier CitT: A member of a novel eubacterial transporter family related to the 2-oxoglutarate-malate translocator from spinach chloroplasts. J Bacteriol 180:4160-4165.
44. Ishiguro N, Oka C, Sato G (1978) Isolation of citrate positive variants of Escherichia coli from domestic pigeons, pigs, cattle, and horses. Appl Environ Microbiol 36:217-222.
45. Ishiguro N, Oka C, Hanazawa Y, Sato G (1979) Plasmids in Escherichia coli controlling citrate-utilizing ability. Appl Environ Microbiol 38:956-964.
46. Foote MJ (1998) Contingency and convergence. Science 280:2068-2069.
47. Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102/103:127-144.
48. Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491-511.
49. Whitlock MC (2005) Combining probability from independent tests: The weighted Z-method is superior to Fisher's approach. J Evol Biol 18:1368-1373.
50. Elena SF, Cooper VS, Lenski RE (1996) Punctuated evolution caused by selection of rare beneficial mutations. Science 272:1802-1804.
51. Drake JW (1991) A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci USA 88:7160-7164.
52. Lederberg S (1966) Genetics of host-controlled restriction and modification of deoxyribonucleic acid in Escherichia coli. J Bacteriol 91:1029-1036.
53. Schneider D, et al. (2002) Genomic comparisons among Escherichia coli strains B, K-12, and O157:H7 using IS elements as molecular markers. BMC Microbiol 2:18.
54. Papadopoulos D, et al. (1999) Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci USA 96:3807-3812.
55. 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.
56. Schneider D, Lenski RE (2004) Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol 155:319-327.
57. Velicer GJ, et al. (2006) Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc Natl Acad Sci USA 103:8107-8112.
58. Herring CD, et al. (2006) Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38:1406-1412.
59. Hegreness M, Kishony R (2007) Analysis of genetic systems using experimental evolution and whole-genome sequencing. Genome Biol 8:201.
60. Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origin of complex features. Nature 423:139-144.
61. Mortlock RP, ed (1984) Microorganisms as Model Systems for Studying Evolution (Plenum, New York).
62. Lenski RE (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. II. Compensation for maladaptive pleiotropic effects associated with resistance to virus T4. Evolution 42:433-440.
63. Bouma JE, Lenski RE (1988) Evolution of a bacteria/plasmid association. Nature 335:351-352.
64. Schrag SJ, Perrot V, Levin BR (1997) Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc London B 264:1287-1291.
65. Lenski RE (1997) The cost of antibiotic resistance - from the perspective of a bacterium. Ciba Found Symp 207:131-140.
66. Bjorkman J, Hughes D, Andersson DI (1998) Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci USA 95:3949-3953.
67. Mayr E (1942) Systematics and the Origin of Species from the Viewpoint of a Zoologist (Columbia Univ Press, New York).