Genetics, Vol 138, 227-234, Copyright © 1994

INVESTIGATIONS

Selection Intensity for Codon Bias

D. L. Hartl, E. N. Moriyama and S. A. Sawyer
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138

The patterns of nonrandom usage of synonymous codons (codon bias) in enteric bacteria were analyzed. Poisson random field (PRF) theory was used to derive the expected distribution of frequencies of nucleotides differing from the ancestral state at aligned sites in a set of DNA sequences. This distribution was applied to synonymous nucleotide polymorphisms and amino acid polymorphisms in the gnd and putP genes of Escherichia coli. For the gnd gene, the average intensity of selection against disfavored synonymous codons was estimated as approximately 7.3 X 10(-9); this value is significantly smaller than the estimated selection intensity against selectively disfavored amino acids in observed polymorphisms (2.0 X 10(-8)), but it is approximately of the same order of magnitude. The selection coefficients for optimal synonymous codons estimated from PRF theory were consistent with independent estimates based on codon usage for threonine and glycine. Across 118 genes in E. coli and Salmonella typhimurium, the distribution of estimated selection coefficients, expressed as multiples of the effective population size, has a mean and standard deviation of 0.5 +/- 0.4. No significant differences were found in the degree of codon bias between conserved positions and replacement positions, suggesting that translational misincorporation is not an important selective constraint among synonymous polymorphic codons in enteric bacteria. However, across the first 100 codons of the genes, conserved amino acids with identical codons have significantly greater codon bias than of either synonymous or nonidentical codons, suggesting that there are unique selective constraints, perhaps including mRNA secondary structures, in this part of the coding region.

This article has been cited by other articles:

				E. Huerta-Sanchez, R. Durrett, and C. D. Bustamante Population Genetics of Polymorphism and Divergence Under Fluctuating Selection Genetics, January 1, 2008; 178(1): 325 - 337. [Abstract] [Full Text] [PDF]

				M. A. Gilchrist Combining Models of Protein Translation and Population Genetics to Predict Protein Production Rates from Codon Usage Patterns Mol. Biol. Evol., November 1, 2007; 24(11): 2362 - 2372. [Abstract] [Full Text] [PDF]

				R. J. Soderberg and O. G. Berg Mutational Interference and the Progression of Muller's Ratchet When Mutations Have a Broad Range of Deleterious Effects Genetics, October 1, 2007; 177(2): 971 - 986. [Abstract] [Full Text] [PDF]

				R. D. Hernandez, S. H. Williamson, and C. D. Bustamante Context Dependence, Ancestral Misidentification, and Spurious Signatures of Natural Selection Mol. Biol. Evol., August 1, 2007; 24(8): 1792 - 1800. [Abstract] [Full Text] [PDF]

				N. Stoletzki and A. Eyre-Walker Synonymous Codon Usage in Escherichia coli: Selection for Translational Accuracy Mol. Biol. Evol., February 1, 2007; 24(2): 374 - 381. [Abstract] [Full Text] [PDF]

				A. D. Cutter, J. D. Wasmuth, and M. L. Blaxter The Evolution of Biased Codon and Amino Acid Usage in Nematode Genomes Mol. Biol. Evol., December 1, 2006; 23(12): 2303 - 2315. [Abstract] [Full Text] [PDF]

				C. C. Burns, J. Shaw, R. Campagnoli, J. Jorba, A. Vincent, J. Quay, and O. Kew Modulation of Poliovirus Replicative Fitness in HeLa Cells by Deoptimization of Synonymous Codon Usage in the Capsid Region. J. Virol., April 1, 2006; 80(7): 3259 - 3272. [Abstract] [Full Text] [PDF]

				G. Shinar, E. Dekel, T. Tlusty, and U. Alon Rules for biological regulation based on error minimization. PNAS, March 14, 2006; 103(11): 3999 - 4004. [Abstract] [Full Text] [PDF]

				L. Loewe, B. Charlesworth, C. Bartolome, and V. Noel Estimating Selection on Nonsynonymous Mutations Genetics, February 1, 2006; 172(2): 1079 - 1092. [Abstract] [Full Text] [PDF]

				S. A. Shabalina, A. Y. Ogurtsov, and N. A. Spiridonov A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res., January 1, 2006; 34(8): 2428 - 2437. [Abstract] [Full Text] [PDF]

				M. L. Christianson Codon usage patterns distort phylogenies from or of DNA sequences Am. J. Botany, August 1, 2005; 92(8): 1221 - 1233. [Abstract] [Full Text] [PDF]

				L. Zhu and C. D. Bustamante A Composite-Likelihood Approach for Detecting Directional Selection From DNA Sequence Data Genetics, July 1, 2005; 170(3): 1411 - 1421. [Abstract] [Full Text] [PDF]

				A. Wagner Energy Constraints on the Evolution of Gene Expression Mol. Biol. Evol., June 1, 2005; 22(6): 1365 - 1374. [Abstract] [Full Text] [PDF]

				S. H. Williamson, R. Hernandez, A. Fledel-Alon, L. Zhu, R. Nielsen, and C. D. Bustamante Simultaneous inference of selection and population growth from patterns of variation in the human genome PNAS, May 31, 2005; 102(22): 7882 - 7887. [Abstract] [Full Text] [PDF]

				H. Qin, W. B. Wu, J. M. Comeron, M. Kreitman, and W.-H. Li Intragenic Spatial Patterns of Codon Usage Bias in Prokaryotic and Eukaryotic Genomes Genetics, December 1, 2004; 168(4): 2245 - 2260. [Abstract] [Full Text] [PDF]

				S. Williamson, A. Fledel-Alon, and C. D. Bustamante Population Genetics of Polymorphism and Divergence for Diploid Selection Models With Arbitrary Dominance Genetics, September 1, 2004; 168(1): 463 - 475. [Abstract] [Full Text] [PDF]

				J. M. Comeron Selective and Mutational Patterns Associated With Gene Expression in Humans: Influences on Synonymous Composition and Intron Presence Genetics, July 1, 2004; 167(3): 1293 - 1304. [Abstract] [Full Text] [PDF]

				S. L. Chen, W. Lee, A. K. Hottes, L. Shapiro, and H. H. McAdams Codon usage between genomes is constrained by genome-wide mutational processes PNAS, March 9, 2004; 101(10): 3480 - 3485. [Abstract] [Full Text] [PDF]

				J. T. Herbeck, D. J. Funk, P. H. Degnan, and J. J. Wernegreen A Conservative Test of Genetic Drift in the Endosymbiotic Bacterium Buchnera: Slightly Deleterious Mutations in the Chaperonin groEL Genetics, December 1, 2003; 165(4): 1651 - 1660. [Abstract] [Full Text] [PDF]

				J. A. Perez, A. Munte, J. Rozas, C. Segarra, and M. Aguade Nucleotide Polymorphism in the RpII215 Gene Region of the Insular Species Drosophila guanche: Reduced Efficacy of Weak Selection on Synonymous Variation Mol. Biol. Evol., November 1, 2003; 20(11): 1867 - 1875. [Abstract] [Full Text] [PDF]

				J. B. Plotkin and J. Dushoff Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus PNAS, June 10, 2003; 100(12): 7152 - 7157. [Abstract] [Full Text] [PDF]

				J. L. Cherry Selection in a Subdivided Population With Local Extinction and Recolonization Genetics, June 1, 2003; 164(2): 789 - 795. [Abstract] [Full Text] [PDF]

				M. W. Hahn, J. E. Stajich, and G. A. Wray The Effects of Selection Against Spurious Transcription Factor Binding Sites Mol. Biol. Evol., June 1, 2003; 20(6): 901 - 906. [Abstract] [Full Text] [PDF]

				J. Wakeley Polymorphism and Divergence for Island-Model Species Genetics, January 1, 2003; 163(1): 411 - 420. [Abstract] [Full Text] [PDF]

				L. Duret, M. Semon, G. Piganeau, D. Mouchiroud, and N. Galtier Vanishing GC-Rich Isochores in Mammalian Genomes Genetics, December 1, 2002; 162(4): 1837 - 1847. [Abstract] [Full Text] [PDF]

				O. G. Berg and C. G. Kurland Evolution of Microbial Genomes: Sequence Acquisition and Loss Mol. Biol. Evol., December 1, 2002; 19(12): 2265 - 2276. [Abstract] [Full Text] [PDF]

				M. Lunzer, A. Natarajan, D. E. Dykhuizen, and A. M. Dean Enzyme Kinetics, Substitutable Resources and Competition: From Biochemistry to Frequency-Dependent Selection in lac Genetics, September 1, 2002; 162(1): 485 - 499. [Abstract] [Full Text] [PDF]

				G. Marais and G. Piganeau Hill-Robertson Interference is a Minor Determinant of Variations in Codon Bias Across Drosophila melanogaster and Caenorhabditis elegans Genomes Mol. Biol. Evol., September 1, 2002; 19(9): 1399 - 1406. [Abstract] [Full Text] [PDF]

				S. Williamson and M. E. Orive The Genealogy of a Sequence Subject to Purifying Selection at Multiple Sites Mol. Biol. Evol., August 1, 2002; 19(8): 1376 - 1384. [Abstract] [Full Text] [PDF]

				F. Rabenstein, D. L. Seifers, J. Schubert, R. French, and D. C. Stenger Phylogenetic relationships, strain diversity and biogeography of tritimoviruses J. Gen. Virol., April 1, 2002; 83(4): 895 - 906. [Abstract] [Full Text] [PDF]

				V. Dvornyk, O. Vinogradova, and E. Nevo Long-term microclimatic stress causes rapid adaptive radiation of kaiABC clock gene family in a cyanobacterium, Nostoc linckia, from ""Evolution Canyons"" I and II, Israel PNAS, February 6, 2002; (2002) 261699498. [Abstract] [Full Text] [PDF]

				C. D. Bustamante, R. Nielsen, and D. L. Hartl A Maximum Likelihood Method for Analyzing Pseudogene Evolution: Implications for Silent Site Evolution in Humans and Rodents Mol. Biol. Evol., January 1, 2002; 19(1): 110 - 117. [Abstract] [Full Text] [PDF]

				C. D. Bustamante, J. Wakeley, S. Sawyer, and D. L. Hartl Directional Selection and the Site-Frequency Spectrum Genetics, December 1, 2001; 159(4): 1779 - 1788. [Abstract] [Full Text] [PDF]

				N. G. C. Smith and A. Eyre-Walker Nucleotide Substitution Rate Estimation in Enterobacteria: Approximate and Maximum-Likelihood Methods Lead to Similar Conclusions Mol. Biol. Evol., November 1, 2001; 18(11): 2124 - 2126. [Full Text] [PDF]

				G. Marais, D. Mouchiroud, and L. Duret Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes PNAS, April 18, 2001; (2001) 91427698. [Abstract] [Full Text]

				G. A. T. McVean and J. Vieira Inferring Parameters of Mutation, Selection and Demography From Patterns of Synonymous Site Evolution in Drosophila Genetics, January 1, 2001; 157(1): 245 - 257. [Abstract] [Full Text]

				A. Llopart and M. Aguadé Nucleotide Polymorphism at the RpII215 Gene in Drosophila subobscura: Weak Selection on Synonymous Mutations Genetics, July 1, 2000; 155(3): 1245 - 1252. [Abstract] [Full Text]

				G. A. T. McVean and B. Charlesworth The Effects of Hill-Robertson Interference Between Weakly Selected Mutations on Patterns of Molecular Evolution and Variation Genetics, June 1, 2000; 155(2): 929 - 944. [Abstract] [Full Text]

				H. Akashi Inferring the Fitness Effects of DNA Mutations From Polymorphism and Divergence Data: Statistical Power to Detect Directional Selection Under Stationarity and Free Recombination Genetics, January 1, 1999; 151(1): 221 - 238. [Abstract] [Full Text]

				B. R. Morton and J. A. Levin The atypical codon usage of the plant psbA gene may be the remnant of an ancestral bias PNAS, October 14, 1997; 94(21): 11434 - 11438. [Abstract] [Full Text] [PDF]

				J. R. Powell and E. N. Moriyama Evolution of codon usage bias in Drosophila PNAS, July 22, 1997; 94(15): 7784 - 7790. [Abstract] [Full Text] [PDF]

				S. M. Rich, S. A. Sawyer, and A. G. Barbour Antigen polymorphism in Borrelia hermsii, a clonal pathogenic bacterium PNAS, December 18, 2001; 98(26): 15038 - 15043. [Abstract] [Full Text] [PDF]

				G. Marais, D. Mouchiroud, and L. Duret Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes PNAS, May 8, 2001; 98(10): 5688 - 5692. [Abstract] [Full Text] [PDF]

				V. Dvornyk, O. Vinogradova, and E. Nevo Long-term microclimatic stress causes rapid adaptive radiation of kaiABC clock gene family in a cyanobacterium, Nostoc linckia, from "Evolution Canyons" I and II, Israel PNAS, February 19, 2002; 99(4): 2082 - 2087. [Abstract] [Full Text] [PDF]