Journal of Molecular Evolution

, Volume 57, Supplement 1, pp S214–S225

Analysis of a Shift in Codon Usage in Drosophila

  • Jeffrey R. Powell
  • Erminia Sezzi
  • Etsuko N. Moriyama
  • Jennifer M. Gleason
  • Adalgisa Caccone
Article

Abstract

In order to gain further insight into a shift in codon usage first observed in Drosophila willistoni we have analyzed seven genes in six species in the lineage leading to D. willistoni. This lineage contains the willistoni and saltans species groups. Sequences were obtained from GenBank or newly sequenced for this study. All species studied showed significant difference in codon usage compared to D. melanogaster for about one third of all amino acids. Within the willistoni/saltans lineage, codon usage is homogeneous, indicating that the shift in codon usage occurred prior to the diversification of extant species in this lineage which we estimate to date to about 20 million years ago. Thus the shift is old and has been stable. We also examined introns from these genes and the G/C composition at four-fold degenerate sites in an effort to detect a change in mutation bias. There is little or no evidence for a difference in mutation bias compared to D. melanogaster. We also considered whether relaxed selection (possibly due to reduced population sizes) or reduced recombination (due to numerous naturally occurring inversions) could account for the shift and concluded these factors alone are insufficient to explain the patterns observed. A change in the relative abundance of isoaccepting tRNAs is one of the few explanations that can account for the observations. Particularly intriguing is the fact that the greatest changes in codon usage have occurred for amino acids with two-fold C/T ending codons for which it is known that posttranscriptional modification occurs in tRNAs from a G in the wobble position to Queuosine that changes optimal binding from C to a slight preference for U. However, we do not argue that this shift was adaptive in nature, rather it may be an example of a “frozen accident.”

Keywords

Codon usage bias Drosophila willistoni Drosophila saltans tRNA 

References

  1. 1.
    Anderson, CL, Carew, EA, Powell, JR 1993Evolution of the Adh locus in the Drosophila willistoni group: The loss of an intron, and shift in codon usage.Mol Biol Evol10605618PubMedGoogle Scholar
  2. 2.
    Dobzhansky, TH, Powell, JR 1975

    The willistoni group of sibling species.

    King, R eds. Handbook of genetics, volume 3.Plenum PressNew York589622
    Google Scholar
  3. 3.
    Dunn, KA, Bielawski, JP, Yang, Z 2001Substitution rates in Drosophila nuclear genes: Implications for translational selection.Genetics157295305PubMedGoogle Scholar
  4. 4.
    Farris, JS 1970Methods for computing Wagner trees.Syst Zool18374402Google Scholar
  5. 5.
    Farris, JS, Kallersjo, M, Kluge, AG, Bult, C 1995Testing significance of incongruence.Cladistics10315319CrossRefGoogle Scholar
  6. 6.
    Felsestein, J 1981Evolutionary trees from DNA sequences: A maximum likelihood approach.J Mol Evol17368376PubMedGoogle Scholar
  7. 7.
    Gleason, JM, Powell, JR 1997Interspecific and intraspecific comparisons of the period locus in the Drosophila willistoni sibling species.Mol Biol Evol14741753PubMedGoogle Scholar
  8. 8.
    Griffith, EC, Powell, JR 1997Adh nucleotide variation in Drosophila willistoni: High replacement polymorphism in an electrophoretically monomorphic protein.J Mol Evol45232237PubMedGoogle Scholar
  9. 9.
    Hosbach, HA, Kubli, E 1979Transfer RNA in aging Drosophila: II. Isoacceptor patterns.Mech Ageing Dev10141149CrossRefPubMedGoogle Scholar
  10. 10.
    Ikemura, T 1992

    Correlation between codon usage and tRNA content in microorganisms.

    Hatfield, DLLee, BJPirtle, RM eds. Transfer RNA in protein synthesis.CRC PressBoca Raton87111
    Google Scholar
  11. 11.
    Kliman, RM, Hey, J 1993Reduced natural selection associated with low recombination in Drosophila melanogaster.Mol Biol Evol1012391258PubMedGoogle Scholar
  12. 12.
    Larson, A 1994

    The comparison of morphological and molecular data in phylogenetic systematics.

    Schierwater, BStreit, BWagner, GPDeSalle, R eds. Molecular ecology and evolution: Approaches and applications.BirkhäuserBasil371390
    Google Scholar
  13. 13.
    Li, W-H 1993Unbiased estimation of the rates of synonymous and nonsynonymous substitution.J Mol Evol369699PubMedGoogle Scholar
  14. 14.
    Meier, F, Suter, B, Grosjean, H, Keith, G, Kubli, E 1985Queuosine modification of the wobble base in tRNAHis influences in vivo decoding properties.EMBO J4823836PubMedGoogle Scholar
  15. 15.
    Moriyama, EN, Hartl, DL 1993Codon usage bias and base composition of nuclear genes in Drosophila.Genetics134847858Google Scholar
  16. 16.
    Moriyama, EN, Petrov, DA, Hartl, DL 1998Genome size and intron size in Drosophila.Mol Biol Evol15770773PubMedGoogle Scholar
  17. 17.
    Moriyama, EN, Powell, JR 1996Intraspecific nuclear DNA variation in Drosophila.Mol Biol Evol13261277PubMedGoogle Scholar
  18. 18.
    Moriyama, EN, Powell, JR 1997Codon usage bias and tRNA abundance in Drosophila.J Mol Evol45514523PubMedGoogle Scholar
  19. 19.
    Moriyama, EN, Powell, JR 1997Synonymous substitution rates of Drosophila: Mitochondrial versus nuclear genes.J Mol Evol45378391PubMedGoogle Scholar
  20. 20.
    O’Grady, PM, Kidwell, MG 2002Phylogeny of the subgenus Sophophora (Diptera: Drosophilidae) based on combined analysis of nuclear and mitocondrial sequences.Mol Phylogenet Evol22442453CrossRefPubMedGoogle Scholar
  21. 21.
    O’Grady, PM, Clark, JB, Kidwell, MG 1998Phylogeny of the Drosophila saltans species group based on combined analysis of nuclear and mitochondrial DNA sequences.Mol Biol Evol15656664PubMedGoogle Scholar
  22. 22.
    Owenby, RK, Stulberg, MP, Jacobson, KB 1979Alteration of the Q family of transfer RNAs in adult Drosophila melanogaster as a function of age, nutrition, and genotype.Mech Ageing Dev1191103CrossRefPubMedGoogle Scholar
  23. 23.
    Powell, JR, DeSalle, R 1995Drosophila molecular phylogenies and their uses.Evol Biol2887138Google Scholar
  24. 24.
    Powell, JR, Moriyama, EN 1997Evolution of codon usage bias in Drosophila.Proc Natl Acad Sci USA9477847790CrossRefPubMedGoogle Scholar
  25. 25.
    Rodriguez-Trelles, F, Tarrio, R, Ayala, FJ 2000aEvidence for a high ancestral GC content in Drosophila.Mol Biol Evol1717101717Google Scholar
  26. 26.
    Rodriguez-Trelles, F, Tarrio, R, Ayala, FJ 2000bFluctuating mutation bias and the evolution of base composition in Drosophila.J Mol Evol50110Google Scholar
  27. 27.
    Saitou, N, Nei, M 1987The neighbor-joining method: A new method for reconstructing phylogenetic trees.Mol Biol Evol4406425PubMedGoogle Scholar
  28. 28.
    Sharp, PM, Li, W-H 1987The codon adaptation index— A measure of directional synonymous codon usage bias, and its potential applications.Nucleic Acids Res1512811295PubMedGoogle Scholar
  29. 29.
    Sharp, PM, Li, W-H 1987The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias.Mol Biol Evol4222230PubMedGoogle Scholar
  30. 30.
    Sharp, PM, Li, W-H 1989On the rate of DNA sequence evolution in Drosophila.J Mol Evol28398402PubMedGoogle Scholar
  31. 31.
    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 Evol5704716PubMedGoogle Scholar
  32. 32.
    Swofford, D 2001PAUP*, phylogenetic analysis using parimony (* and other methods). Version 4.0b.Sinauer AssociatesSunderland, MAGoogle Scholar
  33. 33.
    Tamura, K, Nei, M 1993Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Mol Biol Evol10512526PubMedGoogle Scholar
  34. 34.
    Tarrío, R, Rodríguez-Trelles, F, Ayala, FJ 2000Tree rooting with outgroups when they differ in their nucleotide composition from the ingroup: The Drosophila saltans and willistoni groups, a case study.Mol Phylog Evol16344349CrossRefGoogle Scholar
  35. 35.
    Templeton, A 1983Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and apes.Evolution37221244Google Scholar
  36. 36.
    Val, FC, Vilela, CR, Marques, MD 1981

    Drosophilidae of the neotropical region.

    Ashburner, MCarson, HLThompson, JN eds. The genetics and biology of Drosophila, volume 3a.Academic PressNew York124168
    Google Scholar
  37. 37.
    White, BN, Tener, GM, Holden, J, Suzuki, DT 1973Analysis of tRNAs during the development of Drosophila.Develop Biol33185195PubMedGoogle Scholar
  38. 38.
    Wright, F 1990The ‘effective number of codons’ used in a gene.Gene872329Google Scholar

Copyright information

© Springer-Verlag New York LLC 2003

Authors and Affiliations

  • Jeffrey R. Powell
    • 1
  • Erminia Sezzi
    • 1
  • Etsuko N. Moriyama
    • 2
  • Jennifer M. Gleason
    • 1
  • Adalgisa Caccone
    • 1
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyYale University, New Haven, CT 06520-8106USA
  2. 2.School of Biological SciencesUniversity of Nebraska, Lincoln, NE 68588-0660USA
  3. 3.Yale Institute for Biospherics StudiesYale University, New Haven, CT 06520-8106USA

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