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Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

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Abstract

The patterns and processes of molecular evolution may differ between the X chromosome and the autosomes in Drosophila melanogaster. This may in part be due to differences in the effective population size between the two chromosome sets and in part to the hemizygosity of the X chromosome in Drosophila males. These and other factors may lead to differences both in the gene complements of the X and the autosomes and in the properties of the genes residing on those chromosomes. Here we show that codon bias and recombination rate are correlated strongly and negatively on the X chromosome, and that this correlation cannot be explained by indirect relationships with other known determinants of codon bias. This is in dramatic contrast to the weak positive correlation found on the autosomes. We explored possible explanations for these patterns, which required a comprehensive analysis of the relationships among multiple genetic properties such as protein length and expression level. This analysis highlights conserved features of coding sequence evolution on the X and the autosomes and illuminates interesting differences between these two chromosome sets.

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References

  • Akashi H (1994) Synonymous codon usage in Drosophila melanogaster: Natural selection and translational accuracy. Genetics 136:927–935

    PubMed  Google Scholar 

  • Akashi H (1995) Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA. Genetics 139:1067–1076

    PubMed  Google Scholar 

  • Akashi H (1996) Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias. Faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144:1297–1307

    PubMed  Google Scholar 

  • Akashi H, Eyre-Walker A (1998) Translational selection and molecular evolution. Curr Opin Genet Dev 8:688–693

    Article  PubMed  Google Scholar 

  • Akashi H, Kliman RM, Eyre-Walker A (1998) Mutation pressure, natural selection, and the evolution of base composition in Drosophila. Genetica (Dordrecht) 102-103:49–60

    Google Scholar 

  • Aquadro CF (1997) Insights into the evolutionary process from patterns of DNA sequence variability. Curr Opin Genet Dev 7:835–840

    Article  PubMed  Google Scholar 

  • Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in Drosophila melanogaster. Nature (London) 356:519–520

    Article  Google Scholar 

  • Betancourt AJ, Presgraves DC (2002) Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci USA 99:13616–13620

    Article  PubMed  Google Scholar 

  • Betran E, Thornton K, Long M (2002) Retroposed new genes out of the X in Drosophila. Genome Res 12:1854–1859

    Article  PubMed  Google Scholar 

  • Birdsell JA (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19:1181–1197

    PubMed  Google Scholar 

  • Bridges CB (1935) Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J Hered 26:60–64

    Google Scholar 

  • Bulmer M (1988) Are codon usage patterns in unicellular organisms determined by selection mutation balance? J Evol Biol 1:15–26

    Article  Google Scholar 

  • Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–908

    PubMed  Google Scholar 

  • Caballero A (1995) On the effective size of populations with separate sexes, with particular reference to sex-linked genes. Genetics 139:1007–1011

    PubMed  Google Scholar 

  • Carvalho AB, Clark AG (1999) Intron size and natural selection. Nature (London) 401:344

    Article  Google Scholar 

  • Charlesworth B (1991) The evolution of sex chromosomes. Science (Washington DC) 251:1030–1033

    Google Scholar 

  • Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Natural 130:113–146

    Article  Google Scholar 

  • Comeron JM, Kreitman M (1998) The correlation between synonymous and nonsynonymous substitutions in Drosophila: Mutation, selection or relaxed constraints? Genetics 150:767–775

    PubMed  Google Scholar 

  • Comeron JM, Kreitman M (2000) The correlation between intron length and recombination in Drosophila: Dynamic equilibrium between mutational and selective forces. Genetics 156:1175–1190

    PubMed  Google Scholar 

  • Comeron JM, Kreitman M (2002) Population, evolutionary and genomic consequences of interference selection. Genetics 161:389–410

    PubMed  Google Scholar 

  • Comeron JM, Kreitman M, Aguade M (1999) Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151:239–249

    PubMed  Google Scholar 

  • Conery JS, Lynch M (2001) Nucleotide substitutions and the evolution of duplicate genes. Pacific Symposium on Biocomputing, pp 167–178

  • Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487

    Article  PubMed  Google Scholar 

  • Duret L, Mouchiroud D (2000) Determinants of substitution rates in mammalian genes: Expression pattern affects selection intensity but not mutation rate. Mol Biol Evol 17:68–74

    PubMed  Google Scholar 

  • Emerson JJ, Kaessmann H, Betran E, Long M (2004) Extensive gene traffic on the mammalian X chromosome. Science (Washington DC) 303:537–540

    Article  Google Scholar 

  • Eyre-Walker A, (1996) Synonymous codon bias is related to gene length in Escherichia coli: Selection for translational accuracy? Mol Biol Evol 13:864–872

    PubMed  Google Scholar 

  • Hey J, Kliman RM (2002) Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160:595–608

    PubMed  Google Scholar 

  • Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294

    PubMed  Google Scholar 

  • Kim Y (2004) Effect of strong directional selection on weakly selected mutations at linked sites: Implication for synonymous codon usage. Mol Biol Evol 21:286–294

    Article  PubMed  Google Scholar 

  • Kindahl EC (1994) Recombination and DNA polymorphism on the third chromosome of Drosophila melanogaster. Cornell University. Ithaca, NY

    Google Scholar 

  • Kliman RM, Hey J (1993) Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10:1239–1258

    PubMed  Google Scholar 

  • Kliman RM, Hey J (2003) Hill-Robertson interference in Drosophila melanogaster: Reply to Marais, Mouchiroud and Duret. Genet Res 81:89–90

    Article  PubMed  Google Scholar 

  • Krylov DM, Wolf YI, Rogozin IB, Koonin EV (2003) Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res 13:2229–2235

    Article  PubMed  Google Scholar 

  • Langley CH, Lazzaro BP, Phillips W, Heikkinen E, Braverman JM (2000) Linkage disequilibria and the site frequency spectra in the su(s) and su(wa) regions of the Drosophila melanogaster X chromosome. Genetics 156:1837–1852

    PubMed  Google Scholar 

  • Laporte V, Charlesworth B (2002) Effective population size and population subdivision in demographically structured populations. Genetics 162:501–519

    PubMed  Google Scholar 

  • Marais G, Duret L (2001) Synonymous codon usage, accuracy of translation, and gene length in Caenorhabditis elegans. J Mol Evol 52:275–280

    PubMed  Google Scholar 

  • Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98:5688–5692

    Article  PubMed  Google Scholar 

  • Marais G, Mouchiroud D, Duret L (2003) Neutral effect of recombination on base composition in Drosophila. Genet Res 81:79–87

    Article  PubMed  Google Scholar 

  • Marin I, Siegal ML, Baker BS (2000) The evolution of dosage-compensation mechanisms. Bioessays 22:1106–1114

    Article  PubMed  Google Scholar 

  • Pal C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158:927–931

    PubMed  Google Scholar 

  • Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J, Eastman S, Oliver B (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science (Washington DC) 299:697–700

    Article  Google Scholar 

  • Schmid KJ, Aquadro CF (2001) The evolutionary analysis of “orphans” from the Drosophila genome identifies rapidly diverging and incorrectly annotated genes. Genetics 159:589–598

    PubMed  Google Scholar 

  • Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38

    PubMed  Google Scholar 

  • Shields DC, Sharp PM, Higgins DG, Wright F (1988) ‘Silent’ sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5:704–716

    PubMed  Google Scholar 

  • Singh ND, Arndt PF, Petrov DA (2005) Genomic heterogeneity of background substitutional patterns in Drosophila melanogaster. Genetics 169:709–722

    Article  PubMed  Google Scholar 

  • Sorsa V (1988) Chromosome maps of Drosophila. CRC Press. Boca Raton, FL

    Google Scholar 

  • Subramanian S, Kumar S (2004) Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168:373–381

    Article  PubMed  Google Scholar 

  • Takano-Shimizu T (1999) Local recombination and mutation effects on molecular evolution in Drosophila. Genetics 153:1285–1296

    PubMed  Google Scholar 

  • True JR, Mercer JM, Laurie CC (1996) Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142:507–523

    PubMed  Google Scholar 

  • Wright SI, Yau CBK, Looseley M, Meyers BC (2004) Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol Biol Evol 21:1719–1726

    Article  PubMed  Google Scholar 

  • Yang Z, (1997) PAML: am program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Stanford Genome Training Program (funded by 5 T32 HG00044 from the National Human Genome Research Institute) to N.D.S. and a Sloan Fellowship to D.A.P. Comments from two anonymous reviews, an associate editor, and the editor-in-chief considerably improved this manuscript.

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Correspondence to Nadia D. Singh.

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[Reviewing editor: Dr. Richard Kliman]

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Singh, N.D., Davis, J.C. & Petrov, D.A. Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome. J Mol Evol 61, 315–324 (2005). https://doi.org/10.1007/s00239-004-0287-1

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  • DOI: https://doi.org/10.1007/s00239-004-0287-1

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