Abstract
The related bacteriophages phiX174 and G4 were adapted to the inhibitory temperature of 44 degrees and monitored for nucleotide changes throughout the genome. Phage were evolved by serial transfer at low multiplicity of infection on rapidly dividing bacteria to select genotypes with the fastest rates of reproduction. Both phage showed overall greater fitness effects per substitution during the early stages of adaptation. The fitness of phiX174 improved from -0.7 to 5.6 doublings of phage concentration per generation. Five missense mutations were observed. The earliest two mutations accounted for 85% of the ultimate fitness gain. In contrast, G4 required adaptation to the intermediate temperature of 41.5 degrees before it could be maintained at 44 degrees. Its fitness at 44 degrees increased from -2.7 to 3.2, nearly the same net gain as in phiX174, but with three times the opportunity for adaptation. Seventeen mutations were observed in G4: 14 missense, 2 silent, and 1 intergenic. The first 3 missense substitutions accounted for over half the ultimate fitness increase. Although the expected pattern of periodic selective sweeps was the most common one for both phage, some mutations were lost after becoming frequent, and long-term polymorphism was observed. This study provides the greatest detail yet in combining fitness profiles with the underlying pattern of genetic changes, and the results support recent theories on the range of fitness effects of substitutions fixed during adaptation.
Full Text
The Full Text of this article is available as a PDF (161.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adams J., Puskas-Rozsa S., Simlar J., Wilke C. M. Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae. Curr Genet. 1992 Jul;22(1):13–19. doi: 10.1007/BF00351736. [DOI] [PubMed] [Google Scholar]
- Begun D. J., Whitley P. Genetics of alpha-amanitin resistance in a natural population of Drosophila melanogaster. Heredity (Edinb) 2000 Aug;85(Pt 2):184–190. doi: 10.1046/j.1365-2540.2000.00729.x. [DOI] [PubMed] [Google Scholar]
- Bennett A. F., Dao K. M., Lenski R. E. Rapid evolution in response to high-temperature selection. Nature. 1990 Jul 5;346(6279):79–81. doi: 10.1038/346079a0. [DOI] [PubMed] [Google Scholar]
- Bull J. J., Badgett M. R., Wichman H. A. Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol. 2000 Jun;17(6):942–950. doi: 10.1093/oxfordjournals.molbev.a026375. [DOI] [PubMed] [Google Scholar]
- Bull J. J., Badgett M. R., Wichman H. A., Huelsenbeck J. P., Hillis D. M., Gulati A., Ho C., Molineux I. J. Exceptional convergent evolution in a virus. Genetics. 1997 Dec;147(4):1497–1507. doi: 10.1093/genetics/147.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buonagurio D. A., Nakada S., Parvin J. D., Krystal M., Palese P., Fitch W. M. Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science. 1986 May 23;232(4753):980–982. doi: 10.1126/science.2939560. [DOI] [PubMed] [Google Scholar]
- Burch C. L., Chao L. Evolution by small steps and rugged landscapes in the RNA virus phi6. Genetics. 1999 Mar;151(3):921–927. doi: 10.1093/genetics/151.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bush R. M., Bender C. A., Subbarao K., Cox N. J., Fitch W. M. Predicting the evolution of human influenza A. Science. 1999 Dec 3;286(5446):1921–1925. doi: 10.1126/science.286.5446.1921. [DOI] [PubMed] [Google Scholar]
- Dowell C. E. Growth of bacteriophage phiX-174 at elevated temperatures. J Gen Virol. 1980 Jul;49(1):41–50. doi: 10.1099/0022-1317-49-1-41. [DOI] [PubMed] [Google Scholar]
- Elena S. F., Cooper V. S., Lenski R. E. Punctuated evolution caused by selection of rare beneficial mutations. Science. 1996 Jun 21;272(5269):1802–1804. doi: 10.1126/science.272.5269.1802. [DOI] [PubMed] [Google Scholar]
- Escarmís C., Dávila M., Domingo E. Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol. 1999 Jan 15;285(2):495–505. doi: 10.1006/jmbi.1998.2366. [DOI] [PubMed] [Google Scholar]
- Gerrish P. J., Lenski R. E. The fate of competing beneficial mutations in an asexual population. Genetica. 1998;102-103(1-6):127–144. [PubMed] [Google Scholar]
- Godson G. N., Barrell B. G., Staden R., Fiddes J. C. Nucleotide sequence of bacteriophage G4 DNA. Nature. 1978 Nov 16;276(5685):236–247. doi: 10.1038/276236a0. [DOI] [PubMed] [Google Scholar]
- Golding G. B., Dean A. M. The structural basis of molecular adaptation. Mol Biol Evol. 1998 Apr;15(4):355–369. doi: 10.1093/oxfordjournals.molbev.a025932. [DOI] [PubMed] [Google Scholar]
- Helling R. B., Vargas C. N., Adams J. Evolution of Escherichia coli during growth in a constant environment. Genetics. 1987 Jul;116(3):349–358. doi: 10.1093/genetics/116.3.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill W. G., Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed] [Google Scholar]
- Lenski R. E. Bacterial evolution and the cost of antibiotic resistance. Int Microbiol. 1998 Dec;1(4):265–270. [PubMed] [Google Scholar]
- Mitsuhashi S. Drug resistance in bacteria: history, genetics and biochemistry. J Int Med Res. 1993 Jan-Feb;21(1):1–14. doi: 10.1177/030006059302100101. [DOI] [PubMed] [Google Scholar]
- Orr H. A. Adaptation and the cost of complexity. Evolution. 2000 Feb;54(1):13–20. doi: 10.1111/j.0014-3820.2000.tb00002.x. [DOI] [PubMed] [Google Scholar]
- Papadopoulos D., Schneider D., Meier-Eiss J., Arber W., Lenski R. E., Blot M. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3807–3812. doi: 10.1073/pnas.96.7.3807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riehle M. M., Bennett A. F., Long A. D. Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci U S A. 2001 Jan 9;98(2):525–530. doi: 10.1073/pnas.021448998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanger F., Air G. M., Barrell B. G., Brown N. L., Coulson A. R., Fiddes C. A., Hutchison C. A., Slocombe P. M., Smith M. Nucleotide sequence of bacteriophage phi X174 DNA. Nature. 1977 Feb 24;265(5596):687–695. doi: 10.1038/265687a0. [DOI] [PubMed] [Google Scholar]
- Schrag S. J., Perrot V. Reducing antibiotic resistance. Nature. 1996 May 9;381(6578):120–121. doi: 10.1038/381120b0. [DOI] [PubMed] [Google Scholar]
- TESSMAN E. S., TESSMAN I. Genetic recombination in phage S13. Virology. 1959 Apr;7(4):465–467. doi: 10.1016/0042-6822(59)90075-3. [DOI] [PubMed] [Google Scholar]
- Turner P. E., Chao L. Prisoner's dilemma in an RNA virus. Nature. 1999 Apr 1;398(6726):441–443. doi: 10.1038/18913. [DOI] [PubMed] [Google Scholar]
- Wichman H. A., Badgett M. R., Scott L. A., Boulianne C. M., Bull J. J. Different trajectories of parallel evolution during viral adaptation. Science. 1999 Jul 16;285(5426):422–424. doi: 10.1126/science.285.5426.422. [DOI] [PubMed] [Google Scholar]