Nucleotide polymorphism at the RpII215 gene in Drosophila subobscura. Weak selection on synonymous mutations.

Nucleotide variation in an 8.1-kb fragment encompassing the RpII215 gene, which encodes the largest subunit of the RNA polymerase II complex, is analyzed in a sample of 11 chromosomes from a natural population of Drosophila subobscura. No amino acid polymorphism was detected among the 157 segregating sites. The observed numbers of preferred and unpreferred derived synonymous mutations can be explained by neutral mutational processes. In contrast, preferred mutations segregate at significantly higher frequency than unpreferred mutations, suggesting the action of natural selection. The polymorphism to divergence ratio is different for preferred and unpreferred changes, in agreement with their beneficial and deleterious effects on fitness, respectively. Preferred and unpreferred codons are nonrandomly distributed in the RpII215 gene, leading to a heterogeneous distribution of polymorphic to fixed synonymous differences across this coding region. This intragenic variation of the polymorphism/divergence ratio cannot be explained by different patterns of gene expression, mutation, or recombination rates, and therefore it indicates that selection coefficients for synonymous mutations can vary extensively across a coding region. The application of nucleotide composition stationarity tests in coding and flanking noncoding regions, assumed to behave neutrally, allows the detection of the action of natural selection when stationarity holds in the noncoding region.

[1]  R. Kliman Recent Selection on Synonymous Codon Usage in Drosophila , 1999, Journal of Molecular Evolution.

[2]  Josep M. Comeron,et al.  K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals , 1999, Bioinform..

[3]  A. Eyre-Walker,et al.  Evidence of selection on silent site base composition in mammals: potential implications for the evolution of isochores and junk DNA. , 1999, Genetics.

[4]  M. Aguadé,et al.  Synonymous rates at the RpII215 gene of Drosophila: variation among species and across the coding region. , 1999, Genetics.

[5]  L. Duret,et al.  Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Etsuko N. Moriyama,et al.  Codon Usage Bias and tRNA Abundance in Drosophila , 1997, Journal of Molecular Evolution.

[7]  S. Schaeffer,et al.  Natural selection and the frequency distributions of "silent" DNA polymorphism in Drosophila. , 1997, Genetics.

[8]  A. Templeton,et al.  Contingency tests of neutrality using intra/interspecific gene trees: the rejection of neutrality for the evolution of the mitochondrial cytochrome oxidase II gene in the hominoid primates. , 1996, Genetics.

[9]  M. Aguadé,et al.  Synonymous substitutions in the Xdh gene of Drosophila: heterogeneous distribution along the coding region. , 1996, Genetics.

[10]  H. Akashi,et al.  Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. , 1996, Genetics.

[11]  G. Churchill,et al.  Properties of statistical tests of neutrality for DNA polymorphism data. , 1995, Genetics.

[12]  H. Akashi,et al.  Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. , 1995, Genetics.

[13]  M. Aguadé,et al.  Gene conversion is involved in the transfer of genetic information between naturally occurring inversions of Drosophila. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[15]  M. Kreitman,et al.  Unraveling selection in the mitochondrial genome of Drosophila. , 1994, Genetics.

[16]  D. Hartl,et al.  Selection intensity for codon bias. , 1994, Genetics.

[17]  J. Hey,et al.  The effects of mutation and natural selection on codon bias in the genes of Drosophila. , 1994, Genetics.

[18]  M. Bulmer The selection-mutation-drift theory of synonymous codon usage. , 1991, Genetics.

[19]  M. Kreitman,et al.  Adaptive protein evolution at the Adh locus in Drosophila , 1991, Nature.

[20]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[21]  D C Shields,et al.  "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. , 1988, Molecular biology and evolution.

[22]  C. Aquadro,et al.  The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. , 1988, Genetics.

[23]  R. Hudson,et al.  Estimating the recombination parameter of a finite population model without selection. , 1987, Genetical research.

[24]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[25]  H. Akashi,et al.  Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. , 1999, Genetics.

[26]  M. Aguadé,et al.  Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. , 1999, Genetics.

[27]  J. McDonald,et al.  Detecting non-neutral heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. , 1996, Molecular biology and evolution.

[28]  J. Powell,et al.  Intraspecific nuclear DNA variation in Drosophila. , 1996, Molecular biology and evolution.

[29]  A. Eyre-Walker DNA mismatch repair and synonymous codon evolution in mammals. , 1994, Molecular biology and evolution.

[30]  R. Hudson,et al.  A statistical test for detecting geographic subdivision. , 1992, Molecular biology and evolution.

[31]  R. Hudson Gene genealogies and the coalescent process. , 1990 .

[32]  M. Ashburner Drosophila. A laboratory manual. , 1989 .