Journal of Molecular Evolution

, Volume 64, Issue 5, pp 586–590 | Cite as

Reduced Selection for Codon Usage Bias in Drosophila miranda



Biased codon usage in many species results from a balance among mutation, weak selection, and genetic drift. Here I show that selection to maintain biased codon usage is reduced in Drosophila miranda relative to its ancestor. Analyses of mutation patterns in noncoding DNA suggest that the extent of this reduction cannot be explained by changes in mutation bias or by biased gene conversion. Low levels of variability in D. miranda relative to its sibling species, D. pseudoobscura, suggest that it has a much smaller effective population size. Reduced codon usage bias in D. miranda may thus result from the reduced efficacy of selection against newly arising mutations to unpreferred codons.


Codon bias Drosophila miranda Reduced selection 



I am grateful to Peter Andolfatto and Brian Charlesworth for comments on the manuscript. This work was funded by National Institutes of Health Grant GM076007 to D.B.


  1. Akashi H (1995) Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA. Genetics 139:1067–1076PubMedGoogle Scholar
  2. 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 144:1297–1307PubMedGoogle Scholar
  3. Akashi H, Schaeffer SW (1997) Natural selection and the frequency distributions of “silent” DNA polymorphism in Drosophila. Genetics 146:295–307PubMedGoogle Scholar
  4. Akashi H, Kliman RM, Eyre-Walker A (1998) Mutation pressure, natural selection, and the evolution of base composition in Drosophila. Genetica 102–103:49–60PubMedCrossRefGoogle Scholar
  5. Akashi H, Ko W, Piao S, et al. (2006) Molecular evolution in the Drosophila melanogaster species subgroup: frequent parameter fluctuations on the timescale of molecular divergence. Genetics 172:1711–1726PubMedCrossRefGoogle Scholar
  6. Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437:1149–1152PubMedCrossRefGoogle Scholar
  7. Bachtrog D (2003) Protein evolution and codon usage bias on the neo-sex chromosomes of Drosophila miranda. Genetics 165:1221–1232PubMedGoogle Scholar
  8. Bachtrog D, Andolfatto P (2006) Selection, recombination and demographic history in Drosophila miranda. Genetics 174:2045–2059PubMedCrossRefGoogle Scholar
  9. Bartolome C, Maside X, Yi S, Grant A, Charlesworth B (2005) Patterns of selection on synonymous and nonsynonymous variants in Drosophila miranda. Genetics 169:1495–1507PubMedCrossRefGoogle Scholar
  10. Begun DJ, Whitley P (2002) Molecular population genetics of Xdh and the evolution of base composition in Drosophila. Genetics 162:1725–1735PubMedGoogle Scholar
  11. Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907PubMedGoogle Scholar
  12. Galtier N, Piganeau G, Mouchiroud D, Duret L (2001) GC-content evolution in mammalian genomes:the biased gene conversion hypothesis. Genetics 159:907–911PubMedGoogle Scholar
  13. Galtier N, Bazin E, Bierne N (2006) GC-biased segregation of noncoding polymorphisms in Drosophila. Genetics 172:221–228PubMedCrossRefGoogle Scholar
  14. Haddrill P, Charlesworth B, Halligan D, Andolfatto P (2005) Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol 6:R67PubMedCrossRefGoogle Scholar
  15. Halligan D, Keightley P (2006) Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res 16:875–884PubMedCrossRefGoogle Scholar
  16. Halligan D, Eyre-Walker A, Andolfatto P, Keightley P (2004) Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res 14:273–279PubMedCrossRefGoogle Scholar
  17. Kawahara Y, Matsuo T, Nozawa M, et al. (2004) Comparative sequence analysis of a gene-dense region among closely related species of Drosophila melanogaster. Genes Genet Syst 79:351–359PubMedCrossRefGoogle Scholar
  18. Kern A, Begun D (2005) Patterns of polymorphism and divergence from noncoding sequences of Drosophila melanogaster and D. simulans: evidence for nonequilibrium processes. Mol Biol Evol 22:51–62PubMedCrossRefGoogle Scholar
  19. McVean GA, Vieira J (1999) The evolution of codon preferences in Drosophila: a maximum-likelihood approach to parameter estimation and hypothesis testing. J Mol Evol 49:63–75PubMedCrossRefGoogle Scholar
  20. Nagylaki T (1983) Evolution of a finite population under gene conversion. Proc Natl Acad Sci USA 80:6278–6281PubMedCrossRefGoogle Scholar
  21. Pérez J, Munté A, Rozas J, Segarra C, Aguadé M (2003) Nucleotide polymorphism in the RpII215 gene region of the insular species Drosophila guanche: reduced efficacy of weak selection on synonymous variation. Mol Biol Evol 20:1867–1875PubMedCrossRefGoogle Scholar
  22. Richards S, Liu Y, Bettencourt B, et al. (2005) Comparative genome sequencing of Drosophila pseudoobscura:chromosomal, gene, and cis-element evolution. Genome Res 15:1–18PubMedCrossRefGoogle Scholar
  23. 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 5:704–716PubMedGoogle Scholar
  24. Yi S, Bachtrog D, Charlesworth B (2003) A survey of chromosomal and nucleotide sequence variation in Drosophila miranda. Genetics 164:1369–1381PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Division of Biological SciencesUniversity of CaliforniaLa JollaUSA

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