Skip Navigation

This Article
Right arrow FREE Full Text (PDF) Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (340)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Shields, D. C.
Right arrow Articles by Wright, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shields, D. C.
Right arrow Articles by Wright, F.
Social Bookmarking
 Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Molecular Biology and Evolution, Vol 5, 704-716, Copyright © 1988 by Society for Molecular Biology and Evolution


ORIGINAL ARTICLE

"Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons

DC Shields, PM Sharp, DG Higgins and F Wright
Department of Genetics, Trinity College, Dublin, Ireland.

The patterns of synonymous codon usage in 91 Drosophila melanogaster genes have been examined. Codon usage varies strikingly among genes. This variation is associated with differences in G+C content at silent sites, but (unlike the situation in mammalian genes) these differences are not correlated with variation in intron base composition and so are not easily explicable in terms of mutational biases. Instead, those genes with high G+C content at silent sites, resulting from a strong "preference" for a particular subset of the codons that are mostly C- ending, appear to be the more highly expressed genes. This suggests that G+C content is reduced in sequences where selective constraints are weaker, as indeed seen in a pseudogene. These and other data discussed are consistent with the effects of translational selection among synonymous codons, as seen in unicellular organisms. The existence of selective constraints on silent substitutions, which may vary in strength among genes, has implications for the use of silent molecular clocks.
Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
Genome ResHome page
P. Andolfatto
Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome
Genome Res., December 1, 2007; 17(12): 1755 - 1762.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Heger and C. P. Ponting
Variable Strength of Translational Selection Among 12 Drosophila Species
Genetics, November 1, 2007; 177(3): 1337 - 1348.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. D. Jensen, V. L. Bauer DuMont, A. B. Ashmore, A. Gutierrez, and C. F. Aquadro
Patterns of Sequence Variability and Divergence at the diminutive Gene Region of Drosophila melanogaster: Complex Patterns Suggest an Ancestral Selective Sweep
Genetics, October 1, 2007; 177(2): 1071 - 1085.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
S. Casillas, A. Barbadilla, and C. M. Bergman
Purifying Selection Maintains Highly Conserved Noncoding Sequences in Drosophila
Mol. Biol. Evol., October 1, 2007; 24(10): 2222 - 2234.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
C. Diaz-Castillo and K. G. Golic
Evolution of Gene Sequence in Response to Chromosomal Location
Genetics, September 1, 2007; 177(1): 359 - 374.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
F. G. Jorgensen, M. H. Schierup, and A. G. Clark
Heterogeneity in Regional GC Content and Differential Usage of Codons and Amino Acids in GC-Poor and GC-Rich Regions of the Genome of Apis mellifera
Mol. Biol. Evol., February 1, 2007; 24(2): 611 - 619.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. K. Choi, S. C. Kim, J. Seo, S. Kim, and J. Bhak
Impact of Transcriptional Properties on Essentiality and Evolutionary Rate
Genetics, January 1, 2007; 175(1): 199 - 206.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
R. Nielsen, V. L. Bauer DuMont, M. J. Hubisz, and C. F. Aquadro
Maximum Likelihood Estimation of Ancestral Codon Usage Bias Parameters in Drosophila
Mol. Biol. Evol., January 1, 2007; 24(1): 228 - 235.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
D. C. Presgraves
Intron Length Evolution in Drosophila
Mol. Biol. Evol., November 1, 2006; 23(11): 2203 - 2213.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. A. Sawyer, F. Sandrelli, C. Pasetto, A. A. Peixoto, E. Rosato, R. Costa, and C. P. Kyriacou
The period Gene Thr-Gly Polymorphism in Australian and African Drosophila melanogaster Populations: Implications for Selection
Genetics, September 1, 2006; 174(1): 465 - 480.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
D. L. Halligan and P. D. Keightley
Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison
Genome Res., July 1, 2006; 16(7): 875 - 884.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
H. Akashi, W.-Y. Ko, S. Piao, A. John, P. Goel, C.-F. Lin, and A. P. Vitins
Molecular Evolution in the Drosophila melanogaster Species Subgroup: Frequent Parameter Fluctuations on the Timescale of Molecular Divergence
Genetics, March 1, 2006; 172(3): 1711 - 1726.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Nozawa, T. Aotsuka, and K. Tamura
A Novel Chimeric Gene, siren, With Retroposed Promoter Sequence in the Drosophila bipectinata Complex
Genetics, December 1, 2005; 171(4): 1719 - 1727.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
V. B. DuMont and C. F. Aquadro
Multiple Signatures of Positive Selection Downstream of Notch on the X Chromosome in Drosophila melanogaster
Genetics, October 1, 2005; 171(2): 639 - 653.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
E. S. Balakirev, V. R. Chechetkin, V. V. Lobzin, and F. J. Ayala
Entropy and GC Content in the {beta}-esterase Gene Cluster of the Drosophila melanogaster Subgroup
Mol. Biol. Evol., October 1, 2005; 22(10): 2063 - 2072.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
N. D. Singh, J. C. Davis, and D. A. Petrov
X-Linked Genes Evolve Higher Codon Bias in Drosophila and Caenorhabditis
Genetics, September 1, 2005; 171(1): 145 - 155.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
Z. Gu, L. David, D. Petrov, T. Jones, R. W. Davis, and L. M. Steinmetz
Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae
PNAS, January 25, 2005; 102(4): 1092 - 1097.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. E. Hirsh, H. B. Fraser, and D. P. Wall
Adjusting for Selection on Synonymous Sites in Estimates of Evolutionary Distance
Mol. Biol. Evol., January 1, 2005; 22(1): 174 - 177.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. I. Kalmykova, D. A. Kwon, Ya. M. Rozovsky, N. Hueber, P. Capy, C. Maisonhaute, and V. A. Gvozdev
Selective Expansion of the Newly Evolved Genomic Variants of Retrotransposon 1731 in the Drosophila Genomes
Mol. Biol. Evol., December 1, 2004; 21(12): 2281 - 2289.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
S. Subramanian and S. Kumar
Gene Expression Intensity Shapes Evolutionary Rates of the Proteins Encoded by the Vertebrate Genome
Genetics, September 1, 2004; 168(1): 373 - 381.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
Nucleic Acids ResHome page
S. Casillas and A. Barbadilla
PDA: a pipeline to explore and estimate polymorphism in large DNA databases
Nucleic Acids Res., July 1, 2004; 32(suppl_2): W166 - W169.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
N. Bierne and A. Eyre-Walker
The Genomic Rate of Adaptive Amino Acid Substitution in Drosophila
Mol. Biol. Evol., July 1, 2004; 21(7): 1350 - 1360.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
J.-V. Chamary and L. D. Hurst
Similar Rates but Different Modes of Sequence Evolution in Introns and at Exonic Silent Sites in Rodents: Evidence for Selectively Driven Codon Usage
Mol. Biol. Evol., June 1, 2004; 21(6): 1014 - 1023.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
V. B. DuMont, J. C. Fay, P. P. Calabrese, and C. F. Aquadro
DNA Variability and Divergence at the Notch Locus in Drosophila melanogaster and D. simulans: A Case of Accelerated Synonymous Site Divergence
Genetics, May 1, 2004; 167(1): 171 - 185.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
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]


Home page
Genome ResHome page
D. L. Halligan, A. Eyre-Walker, P. Andolfatto, and P. D. Keightley
Patterns of Evolutionary Constraints in Intronic and Intergenic DNA of Drosophila
Genome Res., February 1, 2004; 14(2): 273 - 279.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
Z. Zhang and H. Kishino
Genomic Background Drives the Divergence of Duplicated Amylase Genes at Synonymous Sites in Drosophila
Mol. Biol. Evol., February 1, 2004; 21(2): 222 - 227.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
N. Cobbe and M. M. S. Heck
The Evolution of SMC Proteins: Phylogenetic Analysis and Structural Implications
Mol. Biol. Evol., February 1, 2004; 21(2): 332 - 347.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
Y. Kim
Effect of Strong Directional Selection on Weakly Selected Mutations at Linked Sites: Implication for Synonymous Codon Usage
Mol. Biol. Evol., February 1, 2004; 21(2): 286 - 294.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
K. Tamura, S. Subramanian, and S. Kumar
Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks
Mol. Biol. Evol., January 1, 2004; 21(1): 36 - 44.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
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]


Home page
Mol Biol EvolHome page
A. Eyre-Walker, P. D. Keightley, N. G. C. Smith, and D. Gaffney
Quantifying the Slightly Deleterious Mutation Model of Molecular Evolution
Mol. Biol. Evol., December 1, 2002; 19(12): 2142 - 2149.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
D. J. Lynn, G. A. C. Singer, and D. A. Hickey
Synonymous codon usage is subject to selection in thermophilic bacteria
Nucleic Acids Res., October 1, 2002; 30(19): 4272 - 4277.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
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]


Home page
Mol Biol EvolHome page
A. Mira and H. Ochman
Gene Location and Bacterial Sequence Divergence
Mol. Biol. Evol., August 1, 2002; 19(8): 1350 - 1358.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
Z. Zhang, N. Inomata, T. Ohba, M.-L. Cariou, and T. Yamazaki
Codon Bias Differentiates Between the Duplicated Amylase Loci Following Gene Duplication in Drosophila
Genetics, July 1, 2002; 161(3): 1187 - 1196.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
J. E. Oppentocht, W. van Delden, and L. van de Zande
Isolation and Characterization of the Genomic Region from Drosophila kuntzei Containing the Adh and Adhr Genes
Mol. Biol. Evol., July 1, 2002; 19(7): 1026 - 1040.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
D. A. Filatov and D. Charlesworth
Substitution Rates in the X- and Y-Linked Genes of the Plants, Silene latifolia and S. dioica
Mol. Biol. Evol., June 1, 2002; 19(6): 898 - 907.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. M. Comeron and M. Kreitman
Population, Evolutionary and Genomic Consequences of Interference Selection
Genetics, May 1, 2002; 161(1): 389 - 410.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. Hey and R. M. Kliman
Interactions Between Natural Selection, Recombination and Gene Density in the Genes of Drosophila
Genetics, February 1, 2002; 160(2): 595 - 608.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
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]


Home page
GeneticsHome page
K. J. Schmid and C. F. Aquadro
The Evolutionary Analysis of ""Orphans"" From the Drosophila Genome Identifies Rapidly Diverging and Incorrectly Annotated Genes
Genetics, October 1, 2001; 159(2): 589 - 598.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
S. W. Schaeffer, C. S. Walthour, D. M. Toleno, A. T. Olek, and E. L. Miller
Protein Variation in ADH and ADH-RELATED in Drosophila pseudoobscura: Linkage Disequilibrium Between Single Nucleotide Polymorphisms and Protein Alleles
Genetics, October 1, 2001; 159(2): 673 - 687.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
H. Musto, S. Cruveiller, G. D'Onofrio, H. Romero, and G. Bernardi
Translational Selection on Codon Usage in Xenopus laevis
Mol. Biol. Evol., September 1, 2001; 18(9): 1703 - 1707.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. Munte, M. Aguade, and C. Segarra
Changes in the Recombinational Environment Affect Divergence in the yellow Gene of Drosophila
Mol. Biol. Evol., June 1, 2001; 18(6): 1045 - 1056.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
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]


Home page
Mol Biol EvolHome page
T. Takano-Shimizu
Local Changes in GC/AT Substitution Biases and in Crossover Frequencies on Drosophila Chromosomes
Mol. Biol. Evol., April 1, 2001; 18(4): 606 - 619.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
L. Brocchieri
Low-Complexity Regions in Plasmodium Proteins: In Search of a Function
Genome Res., February 1, 2001; 11(2): 195 - 197.
[Full Text]


Home page
GeneticsHome page
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]


Home page
GeneticsHome page
K. A. Dunn, J. P. Bielawski, and Z. Yang
Substitution Rates in Drosophila Nuclear Genes: Implications for Translational Selection
Genetics, January 1, 2001; 157(1): 295 - 305.
[Abstract] [Full Text]


Home page
GeneticsHome page
J. M. Comeron and M. Kreitman
The Correlation Between Intron Length and Recombination in Drosophila: Dynamic Equilibrium Between Mutational and Selective Forces
Genetics, November 1, 2000; 156(3): 1175 - 1190.
[Abstract] [Full Text]


Home page
GeneticsHome page
J. P. Bielawski, K. A. Dunn, and Z. Yang
Rates of Nucleotide Substitution and Mammalian Nuclear Gene Evolution: Approximate and Maximum-Likelihood Methods Lead to Different Conclusions
Genetics, November 1, 2000; 156(3): 1299 - 1308.
[Abstract] [Full Text]


Home page
ScienceHome page
P. D. Keightley and A. Eyre-Walker
Deleterious Mutations and the Evolution of Sex
Science, October 13, 2000; 290(5490): 331 - 333.
[Abstract] [Full Text]


Home page
Mol Biol EvolHome page
J. C. Silva and M. G. Kidwell
Horizontal Transfer and Selection in the Evolution of P Elements
Mol. Biol. Evol., October 1, 2000; 17(10): 1542 - 1557.
[Abstract] [Full Text] [PDF]


Home page
J. Gen. Virol.Home page
D. B. Levin and B. Whittome
Codon usage in nucleopolyhedroviruses
J. Gen. Virol., September 1, 2000; 81(9): 2313 - 2325.
[Abstract] [Full Text]


Home page
Mol Biol EvolHome page
B. S. W. Chang and D. L. Campbell
Bias in Phylogenetic Reconstruction of Vertebrate Rhodopsin Sequences
Mol. Biol. Evol., August 1, 2000; 17(8): 1220 - 1231.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
GeneticsHome page
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]


Home page
Mol Biol EvolHome page
D. L. Campbell, A. V. Z. Brower, and N. E. Pierce
Molecular Evolution of the Wingless Gene and Its Implications for the Phylogenetic Placement of the Butterfly Family Riodinidae (Lepidoptera: Papilionoidea)
Mol. Biol. Evol., May 1, 2000; 17(5): 684 - 696.
[Abstract] [Full Text] [PDF]


Home page
MicrobiologyHome page
B. Lafay, J. C. Atherton, and P. M. Sharp
Absence of translationally selected synonymous codon usage bias in Helicobacter pylori
Microbiology, April 1, 2000; 146(4): 851 - 860.