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PMID: 17194784 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Background selection in single genes may explain patterns of codon bias.

Genetics ·Vol. 175 ·No. 3 ·2007-03-00 ·Pages 1381-93

Loewe L, Charlesworth B

Abstract

Background selection involves the reduction in effective population size caused by the removal of recurrent deleterious mutations from a population. Previous work has examined this process for large genomic regions. Here we focus on the level of a single gene or small group of genes and investigate how the effects of background selection caused by nonsynonymous mutations are influenced by the lengths of coding sequences, the number and length of introns, intergenic distances, neighboring genes, mutation rate, and recombination rate. We generate our predictions from estimates of the distribution of the fitness effects of nonsynonymous mutations, obtained from DNA sequence diversity data in Drosophila. Results for genes in regions with typical frequencies of crossing over in Drosophila melanogaster suggest that background selection may influence the effective population sizes of different regions of the same gene, consistent with observed differences in codon usage bias along genes. It may also help to cause the observed effects of gene length and introns on codon usage. Gene conversion plays a crucial role in determining the sizes of these effects. The model overpredicts the effects of background selection with large groups of nonrecombining genes, because it ignores Hill-Robertson interference among the mutations involved.

MeSH Terms
Animals Codon/genetics Computer Simulation Drosophila/genetics Gene Components Gene Conversion/genetics Genes/genetics Models, Genetic Mutation/genetics Selection, Genetic
Chemicals
Codon
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Loewe Laurence
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom. [email protected]
Charlesworth Brian
References (54)
54 references, click to expand
  1. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  2. Intragenic spatial patterns of codon usage bias in prokaryotic and eukaryotic genomes.
    Genetics. 2004 Dec;168(4):2245-60 PMID: 15611189
  3. The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation.
    Genetics. 2000 Jun;155(2):929-44 PMID: 10835411
  4. The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces.
    Genetics. 2000 Nov;156(3):1175-90 PMID: 11063693
  5. Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome.
    Genetics. 2000 Dec;156(4):1837-52 PMID: 11102378
  6. Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila.
    Genetics. 2001 Jan;157(1):245-57 PMID: 11139506
  7. DNA evolution under weak selection.
    Gene. 2000 Dec 30;261(1):3-9 PMID: 11164031
  8. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels.
    Am J Hum Genet. 2001 Oct;69(4):831-43 PMID: 11533915
  9. Genetic linkage and molecular evolution.
    Curr Biol. 2001 Sep 4;11(17):R684-6 PMID: 11553339
  10. Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans.
    Genetics. 2002 Feb;160(2):493-507 PMID: 11861556
  11. Interactions between natural selection, recombination and gene density in the genes of Drosophila.
    Genetics. 2002 Feb;160(2):595-608 PMID: 11861564
  12. Gene density and human nucleotide polymorphism.
    Mol Biol Evol. 2002 Mar;19(3):336-40 PMID: 11861892
  13. Population, evolutionary and genomic consequences of interference selection.
    Genetics. 2002 May;161(1):389-410 PMID: 12019253
  14. Linkage limits the power of natural selection in Drosophila.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13616-20 PMID: 12370444
  15. Natural selection at linked sites in humans.
    Gene. 2002 Oct 30;300(1-2):31-42 PMID: 12468083
  16. Annotation of the Drosophila melanogaster euchromatic genome: a systematic review.
    Genome Biol. 2002;3(12):RESEARCH0083 PMID: 12537572
  17. Recombination, dominance and selection on amino acid polymorphism in the Drosophila genome: contrasting patterns on the X and fourth chromosomes.
    Genetics. 2003 Nov;165(3):1195-208 PMID: 14668375
  18. Selection on codon usage in Drosophila americana.
    Curr Biol. 2004 Jan 20;14(2):150-4 PMID: 14738738
  19. Effect of strong directional selection on weakly selected mutations at linked sites: implication for synonymous codon usage.
    Mol Biol Evol. 2004 Feb;21(2):286-94 PMID: 14660698
  20. The effect of linkage on limits to artificial selection.
    Genet Res. 1966 Dec;8(3):269-94 PMID: 5980116
  21. The hitch-hiking effect of a favourable gene.
    Genet Res. 1974 Feb;23(1):23-35 PMID: 4407212
  22. The evolutionary advantage of recombination.
    Genetics. 1974 Oct;78(2):737-56 PMID: 4448362
  23. Further observations on intragenic recombination in Drosophila melanogaster.
    Genet Res. 1981 Dec;38(3):281-96 PMID: 6800885
  24. Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons.
    J Mol Evol. 1987;24(4):337-45 PMID: 3110426
  25. Effects of linkage on rates of molecular evolution.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6414-8 PMID: 3413105
  26. The selection-mutation-drift theory of synonymous codon usage.
    Genetics. 1991 Nov;129(3):897-907 PMID: 1752426
  27. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster.
    Nature. 1992 Apr 9;356(6369):519-20 PMID: 1560824
  28. Splicing signals in Drosophila: intron size, information content, and consensus sequences.
    Nucleic Acids Res. 1992 Aug 25;20(16):4255-62 PMID: 1508718
  29. The effect of deleterious mutations on neutral molecular variation.
    Genetics. 1993 Aug;134(4):1289-303 PMID: 8375663
  30. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster.
    Genetics. 1994 Aug;137(4):1019-26 PMID: 7982556
  31. Intraspecific nuclear DNA variation in Drosophila.
    Mol Biol Evol. 1996 Jan;13(1):261-77 PMID: 8583899
  32. Variation in synonymous codon use and DNA polymorphism within the Drosophila genome.
    J Evol Biol. 2006 Jan;19(1):1-11 PMID: 16405571
  33. Patterns of selection on synonymous and nonsynonymous variants in Drosophila miranda.
    Genetics. 2005 Mar;169(3):1495-507 PMID: 15545653
  34. The pattern of polymorphism in Arabidopsis thaliana.
    PLoS Biol. 2005 Jul;3(7):e196 PMID: 15907155
  35. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content.
    Genome Biol. 2005;6(8):R67 PMID: 16086849
  36. Fitting background-selection predictions to levels of nucleotide variation and divergence along the human autosomes.
    Genome Res. 2005 Sep;15(9):1211-21 PMID: 16140989
  37. Recombination enhances protein adaptation in Drosophila melanogaster.
    Curr Biol. 2005 Sep 20;15(18):1651-6 PMID: 16169487
  38. Intragenic Hill-Robertson interference influences selection intensity on synonymous mutations in Drosophila.
    Mol Biol Evol. 2005 Dec;22(12):2519-30 PMID: 16120803
  39. Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans.
    Genetics. 2006 Jan;172(1):171-84 PMID: 16272415
  40. Estimating selection on nonsynonymous mutations.
    Genetics. 2006 Feb;172(2):1079-92 PMID: 16299397
  41. The hitchhiking effect on linkage disequilibrium between linked neutral loci.
    Genetics. 2006 Apr;172(4):2647-63 PMID: 16452153
  42. Inferring the distribution of mutational effects on fitness in Drosophila.
    Biol Lett. 2006 Sep 22;2(3):426-30 PMID: 17148422
  43. Evolution of amino-acid sequences and codon usage on the Drosophila miranda neo-sex chromosomes.
    Genetics. 2006 Dec;174(4):2033-44 PMID: 17028318
  44. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila.
    Nature. 2007 Jan 4;445(7123):82-5 PMID: 17203060
  45. Deleterious background selection with recombination.
    Genetics. 1995 Dec;141(4):1605-17 PMID: 8601498
  46. The pattern of neutral molecular variation under the background selection model.
    Genetics. 1995 Dec;141(4):1619-32 PMID: 8601499
  47. The effect of recombination on background selection.
    Genet Res. 1996 Apr;67(2):159-74 PMID: 8801188
  48. Background selection and patterns of genetic diversity in Drosophila melanogaster.
    Genet Res. 1996 Oct;68(2):131-49 PMID: 8940902
  49. The effect of gene conversion on intralocus associations.
    Genetics. 1998 Mar;148(3):1397-9 PMID: 9539452
  50. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila.
    Genetics. 1999 Jan;151(1):239-49 PMID: 9872963
  51. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482-7 PMID: 10200288
  52. On the probability of fixation of mutant genes in a population.
    Genetics. 1962 Jun;47:713-9 PMID: 14456043
  53. Correlated evolution of synonymous and nonsynonymous sites in Drosophila.
    J Mol Evol. 2004 Dec;59(6):771-9 PMID: 15599509
  54. The coalescent with gene conversion.
    Genetics. 2000 May;155(1):451-62 PMID: 10790416
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2007-03-00
Epub
2006-00-28
Pages
1381-93
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1840058
Subset
IM
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