Mutation pressure, natural selection, and the evolution of base composition in Drosophila

Genome sequencing in a number of taxa has revealed variation in nucleotide composition both among regions of the genome and among functional classes of sites in DNA. Mutational biases, biased gene conversion, and natural selection have been proposed as causes of this variation. Here, we review patterns of base composition in Drosophila DNA. Nucleotide composition in Drosophila melanogaster varys regionally, and base composition is correlated between introns and exons. Drosophila species also show striking patterns of non-random codon usage. Patterns of synonymous codon usage and the biochemistry of translation suggest that natural selection may act at ‘silent’ sites. A relationship between recombination rates and codon usage and comparisons of the evolutionary dynamics of silent mutations within and between species support natural selection discriminating among synonymous codons. The causes of regional base composition variation are less clear. Progress in functional studies of non-coding DNA, further investigations of genome patterns, and statistical tests based on evolutionary theory will lead to a greater understanding of the contributions of mutational processes and natural selection in patterning genome-wide nucleotide composition.

[1]  J. Powell,et al.  Rates of DNA evolution in Drosophila depend on function and developmental stage of expression. , 1993, Genetics.

[2]  N. Barton.  Linkage and the limits to natural selection. , 1995, Genetics.

[3]  J. Jiricny,et al.  Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells , 1988, Cell.

[4]  P. Sharp,et al.  Codon usage: mutational bias, translational selection, or both? , 1993, Biochemical Society transactions.

[5]  D. Hartl,et al.  Population genetics of polymorphism and divergence. , 1992, Genetics.

[6]  H. Shibata,et al.  Molecular evolution of the duplicated Amy locus in the Drosophila melanogaster species subgroup: concerted evolution only in the coding region and an excess of nonsynonymous substitutions in speciation. , 1995, Genetics.

[7]  J. Filipski,et al.  Correlation between molecular clock ticking, codon usage, fidelity of DNA repair, chromosome banding and chromatin compactness in germline cells , 1987, FEBS letters.

[8]  N. Sueoka.  On the genetic basis of variation and heterogeneity of DNA base composition. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. True,et al.  Differences in crossover frequency and distribution among three sibling species of Drosophila. , 1996, Genetics.

[10]  D. Hartl,et al.  Codon usage bias and base composition of nuclear genes in Drosophila. , 1993, Genetics.

[11]  Adam Eyre-Walker,et al.  Recombination and mammalian genome evolution , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Wen-Hsiung Li.  Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons , 2005, Journal of Molecular Evolution.

[13]  D. Hickey,et al.  Gene Duplication, Gene Conversion and Codon Bias , 1994 .

[14]  M Yarus,et al.  Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. , 1989, Journal of molecular biology.

[15]  M. Bulmer,et al.  Are codon usage patterns in unicellular organisms determined by selection‐mutation balance? , 1988 .

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

[17]  F. Wright.  The 'effective number of codons' used in a gene. , 1990, Gene.

[18]  M. Schuler,et al.  AU-rich intronic elements affect pre-mRNA 5' splice site selection in Drosophila melanogaster , 1993, Molecular and cellular biology.

[19]  S. Schaeffer,et al.  Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. , 1993, Genetics.

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

[21]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[22]  F. Crick.  Origin of the Genetic Code , 1967, Nature.

[23]  A. Nicolas,et al.  Polarity of meiotic gene conversion in fungi: Contrasting views , 1994, Experientia.

[24]  R. H.J.MULLE.  THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE , 2002 .

[25]  B. Golding.  Non-Neutral Evolution: Theories And Molecular Data , 1994 .

[26]  T. Kaufman,et al.  A functional analysis of 5', intronic and promoter regions of the homeotic gene proboscipedia in Drosophila melanogaster. , 1995, Development.

[27]  L. Kann,et al.  Neutral and non-neutral evolution of Drosophila mitochondrial DNA. , 1994, Genetics.

[28]  O. Berg,et al.  Synonymous substitution-rate constants in Escherichia coli and Salmonella typhimurium and their relationship to gene expression and selection pressure , 1995, Journal of Molecular Evolution.

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

[30]  J. Felsenstein.  The evolutionary advantage of recombination. , 1974, Genetics.

[31]  K. Low.  The Recombination of genetic material , 1988 .

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

[33]  W. Marzluff,et al.  Selection on silent sites in the rodent H3 histone gene family. , 1994, Genetics.

[34]  M. Gouy,et al.  Codon usage in bacteria: correlation with gene expressivity. , 1982, Nucleic acids research.

[35]  B. Dastugue,et al.  Intronic and 5′ flanking sequences of the Drosophila β3 tubulin gene are essential to confer ecdysone responsiveness , 1993, Molecular and Cellular Endocrinology.

[36]  F J Ayala,et al.  Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. , 1994, Genetics.

[37]  D. A. Kirby,et al.  RNA folding in Drosophila shows a distance effect for compensatory fitness interactions. , 1993, Genetics.

[38]  M. Bulmer,et al.  A statistical analysis of nucleotide sequences of introns and exons in human genes. , 1987, Molecular biology and evolution.

[39]  G. Bernardi,et al.  Compositional constraints and genome evolution , 2005, Journal of Molecular Evolution.

[40]  T. Ohta,et al.  Protein Polymorphism as a Phase of Molecular Evolution , 1971, Nature.

[41]  G. Bernardi,et al.  The isochore organization of the human genome. , 1989, Annual review of genetics.

[42]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[43]  A. Eyre-Walker.  The close proximity ofEscherichia coli genes: Consequences for stop codon and synonymous codon use , 1996, Journal of Molecular Evolution.

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

[45]  B. Charlesworth,et al.  The pattern of neutral molecular variation under the background selection model. , 1995, Genetics.

[46]  Wen-Hsiung Li,et al.  Mutation rates differ among regions of the mammalian genome , 1989, Nature.

[47]  Stephen M. Mount,et al.  Splicing signals in Drosophila: intron size, information content, and consensus sequences. , 1992, Nucleic acids research.

[48]  R. Lloubès,et al.  Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. , 1984, Journal of molecular biology.

[49]  M. D. Brennan,et al.  The two small introns of the Drosophila affinidisjuncta Adh gene are required for normal transcription. , 1996, Nucleic acids research.

[50]  J. Powell,et al.  Evolution of the Adh locus in the Drosophila willistoni group: the loss of an intron, and shift in codon usage. , 1993, Molecular biology and evolution.

[51]  B. Dastugue,et al.  Enhancer and silencer elements within the first intron mediate the transcriptional regulation of the beta 3 tubulin gene by 20-hydroxyecdysone in Drosophila Kc cells. , 1993, Insect biochemistry and molecular biology.

[52]  G. M. Tener,et al.  Analysis of tRNAs during the development of Drosophila. , 1973, Developmental biology.

[53]  Douglas O. Clary,et al.  The mitochondrial DNA molecule ofDrosophila yakuba: Nucleotide sequence, gene organization, and genetic code , 2005, Journal of Molecular Evolution.

[54]  B. Charlesworth.  Background selection and patterns of genetic diversity in Drosophila melanogaster. , 1996, Genetical research.

[55]  W. Fiers,et al.  Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. , 1982, Gene.

[56]  C. Kurland,et al.  Codon preferences in free-living microorganisms. , 1990, Microbiological reviews.

[57]  J. Hey,et al.  Reduced natural selection associated with low recombination in Drosophila melanogaster. , 1993, Molecular biology and evolution.

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

[59]  P. Sharp,et al.  Regional base composition variation along yeast chromosome III: evolution of chromosome primary structure. , 1993, Nucleic acids research.

[60]  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.

[61]  A. Hilliker,et al.  3 – Genetic Analysis of Intragenic Recombination in Drosophila , 1988 .

[62]  P. Sharp,et al.  Synonymous codon usage in Saccharomyces cerevisiae , 1991, Yeast.

[63]  G. Bernardi,et al.  The human genome: organization and evolutionary history. , 1995, Annual review of genetics.

[64]  G. Holmquist,et al.  Chromosome bands, their chromatin flavors, and their functional features. , 1992, American journal of human genetics.

[65]  S. Wright,et al.  The Distribution of Gene Frequencies Under Irreversible Mutation. , 1938, Proceedings of the National Academy of Sciences of the United States of America.

[66]  D. Hartl,et al.  Compositional heterogeneity and patterns of molecular evolution in the Drosophila genome. , 1993, Genetics.

[67]  E. Freese.  On the evolution of the base composition of DNA , 1962 .

[68]  M. Kimura.  The Neutral Theory of Molecular Evolution: Introduction , 1983 .

[69]  J. D. Huang,et al.  The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression. , 1993, Genes & development.

[70]  M. Ashburner.  A Laboratory manual , 1989 .

[71]  J. Bennetzen,et al.  Codon selection in yeast. , 1982, The Journal of biological chemistry.

[72]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. , 1981, Journal of molecular biology.

[73]  A. Clark,et al.  Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. , 1995, Genetics.

[74]  N. Sueoka.  Directional mutation pressure and neutral molecular evolution. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[75]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.

[76]  Wen-Hsiung Li,et al.  The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. , 1987, Molecular biology and evolution.

[77]  R. H. Thomas,et al.  The molecular evolution of the alcohol dehydrogenase locus and the phylogeny of Hawaiian Drosophila. , 1991, Molecular biology and evolution.

[78]  J. M. Smith,et al.  Site-specific codon bias in bacteria. , 1996, Genetics.

[79]  D. Hartl,et al.  Confidence interval for the number of selectively neutral amino acid polymorphisms. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[80]  H. Akashi,et al.  Codon bias evolution in Drosophila. Population genetics of mutation-selection drift. , 1997, Gene.

[81]  H. Akashi.  Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. , 1994, Genetics.

[82]  T. Ikemura.  Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. , 1982, Journal of molecular biology.

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

[84]  U Grob,et al.  Statistical analysis of nucleotide sequences. , 1990, Nucleic acids research.

[85]  C C Laurie,et al.  The effect of an intronic polymorphism on alcohol dehydrogenase expression in Drosophila melanogaster. , 1994, Genetics.

[86]  T. Nagylaki.  Evolution of a finite population under gene conversion. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Jörg Köhler,et al.  Related enhancers in the intron of the beta1 tubulin gene of Drosophila melanogaster are essential for maternal and CNS-specific expression during embryogenesis , 1996, Nucleic Acids Res..

[88]  T. Gojobori,et al.  Rates of synonymous substitution and base composition of nuclear genes in Drosophila. , 1992, Genetics.

[89]  M. Bulmer,et al.  Synonymous substitution rates in enterobacteria. , 1995, Genetics.

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

[91]  EyreWaker.  Differentiating Between Selection and Mutation Bias , 2002 .

[92]  W. Gehring,et al.  Intron of the mouse Hoxa-7 gene contains conserved homeodomain binding sites that can function as an enhancer element in Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[93]  T. Ikemura.  Codon usage and tRNA content in unicellular and multicellular organisms. , 1985, Molecular biology and evolution.

[94]  D. Hickey,et al.  Concerted evolution of duplicated protein-coding genes in Drosophila. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[95]  P. Deschavanne,et al.  Correlation of GC content with replication timing and repair mechanisms in weakly expressed E.coli genes. , 1995, Nucleic acids research.

[96]  Wen-Hsiung Li,et al.  An evolutionary perspective on synonymous codon usage in unicellular organisms , 1986, Journal of Molecular Evolution.

[97]  D. A. Kirby,et al.  Maintenance of pre-mRNA secondary structure by epistatic selection. , 1995, Proceedings of the National Academy of Sciences of the United States of America.