Contrasting the efficacy of selection on the X and autosomes in drosophila

Molecular Biology and Evolution

Volumn 25, Issue 2, 2008, Pages 454-467

  Singh, Nadia D ^a   Larracuente, Amanda M ^a   Clark, Andrew G ^a  

^a Cornell University ^*

Author keywords

Drosophila; Faster X; Positive selection; Purifying selection

Indexed keywords

AMINO ACID;

ALLELE; ARTICLE; AUTOSOME; DROSOPHILA; EVOLUTION; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC PARAMETERS; GENOME; GERM LINE; HEMIZYGOSITY; MUTATION; NONHUMAN; PHYLOGENY; POPULATION GENETICS; SEQUENCE ALIGNMENT; X CHROMOSOME;

ANIMALS; DROSOPHILA; EVOLUTION; FEMALE; GENOME, INSECT; MALE; PHYLOGENY; SELECTION (GENETICS); X CHROMOSOME;

EID: 38949208249     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msm275     Document Type: Article

References (66)

1. Akashi H. 1994. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 136:927-935.
2. Akashi H. 1995. Inferring weak selection from patterns of polymorphism and sivergence at "silent" sites in Drosophila DNA. Genetics. 139:1067-1076.
3. Akashi H. 1997. Codon bias evolution in Drosophila. Population genetics of mutation-selection drift. Gene (Amsterdam). 205:269-278.
4. Avery PJ. 1984. The population genetics of haplo-diploids and X-linked genes. Genet Res. 44:321-341.
5. Bauer DuMont V, Aquadro CF. 1997. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol. 14:1252-1257.
6. Begun DJ, Whitley P. 2000. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci USA. 97:5960-5965.
7. Betancourt AJ, Kim Y, Orr HA. 2004. A pseudohitchhiking model of x vs. autosomal diversity. Genetics. 168:2261-2269.
8. Betancourt AJ, Presgraves DC, Swanson WJ. 2002. A test for faster X evolution in Drosophila. Mol Biol Evol. 19:1816-1819.
9. Bhutkar A, Russo S, Smith TF, Gelbart WM. 2006. Techniques for multi-genome synteny analysis to overcome assembly limitations. Genome Inform. 17:152-161.
10. Bhutkar AV, Russo S, Smith TF, Gelbart WM. 2007. Genomescale analysis of positionally relocated genes. Genome Res. 17:1880-1889.
11. Bierne N, Eyre Walker AC. 2004. The genomic rate of adaptive amino acid substitution in Drosophila. Mol Biol Evol. 21:1350-1360.
12. Bulmer M. 1991. The selection-mutation-drift theory of synonymous codon usage. Genetics. 129:897-908.
13. Charlesworth B, Coyne JA, Barton NH. 1987. The relative rates of evolution of sex chromosomes and autosomes. Am Nat. 130:113-146.
14. Chintapalli VR, Wang J, Dow JAT. 2007. Using fly atlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 39:715-750.
15. 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.
16. Counterman BA, Ortiz-Barrientos C, Noor MAF. 2004. Using comparative genomic data to test for fast-X evolution. Evolution. 58:656-660.
17. Drosophila 12 Genomes Consortium et al. 128 co-authors. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 450:203-218.
18. Drost JB, Lee WR. 1995. Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among Drosophila, mouse and human. Environ Mol Mutag. 25:48-64.
19. Garcia-Dorado A, Lopez-Fanjul C, Caballero A. 2004. Rates and effects of deleterious mutations and their evolutionary consequences. In: Moya A, Font E, editors. Evolution of molecules and ecosystems. Oxford: Oxford University Press. p. 20-32.
20. Haerty W, Jagadeeshan WS, Kulathinal RJ, et al. 2007. Evolution in the fast lane: rapidly evolving sex-and reproduction-related genes in Drosophila species. Genetics. 177:1321-1335.
21. Hamblin MT, Aquadro CF. 1996. High nucleotide sequence variation in a region of low recombination in Drosophila simulans is consistent with the background selection model. Mol Biol Evol. 13:1133-1140.
22. Hamblin MT, Aquadro CF. 1999. DNA sequence variation and the recombinational landscape in Drosophila pseudoobscura: a study of the second chromosome. Genetics. 153:859-869.
23. Hambuch TM, Parsch J. 2005. Patterns of synonymous codon usage in Drosophila melanogaster genes with sex-biased expression. Genetics. 170:1691-1700.
24. Hartl DL, Clark AG. 2007. Principles of population genetics, 4th ed. Sunderland (MA): Sinauer Associates, Inc.
25. Holm S. 1979. A simple sequentially rejective bonferroni test procedure. Scandinavian J Stat. 6:65-70.
26. Hutter S, Li H, Beisswanger S, De Lorenzo D, Stephan W. 2007. Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data. Genetics. 177:469-480.
27. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
28. Larracuente AM, Sackton TB, Greenberg A, Wong A, Singh ND, Sturgill D, Zhang Y, Oliver B, Clark AG. Protein-coding gene evolution in Drosophila. Trends Genet. Forthcoming.
29. Lu J, Wu C-I. 2005. Weak selection revealed by the wholegenome comparison of the X chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci USA. 102:4063-4067.
30. Machado CA, Haselkorn TS, Noor MAF. 2007. Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D-persimilis. Genetics. 175:1289-1306.
31. McVean GAT, Charlesworth B. 1999. A population genetic model for the evolution of synonymous codon usage: patterns and predictions. Genet Res. 74:145-158.
32. Meiklejohn CD, Parsch J, Ranz JM, Hartl DL. 2003. Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci USA. 100:9894-9899.
33. Moriyama EN, Powell JR. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 13:261-277.
34. Musters H, Huntley MA, Singh RS. 2006. A genomic comparison of faster-sex, faster-X, and faster-male evolution between Drosophila melanogaster and Drosophila pseudoobscura. J Mol Evol. 62:693-700.
35. Orr HA, Betancourt AJ. 2001. Haldane's sieve and adaptation from the standing genetic variation. Genetics. 157:875-884.
36. Panhuis TM, Clark NL, Swanson WJ. 2006. Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond Ser B Biol Sci. 361:261-268.
37. 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.
38. Petrov DA, Hartl DL. 1999. Patterns of nucleotide substitution in Drosophila and mammalian genomes. Proc Natl Acad Sci USA. 96:1475-1479.
39. Pool JE, Nielsen R. 2007. Population size changes reshape relative levels of X chromosome and autosome diversity. Int J Org Evolution. 61:3001-3006.
40. Powell JR, Moriyama EN. 1997. Evolution of codon usage bia s in Drosophila. Proc Natl Acad Sci USA. 94:7784-7790.
41. Ranz JM, Casals F, Ruiz A. 2001. How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Res. 11:230-239.
42. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL. 2003. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science. 300:1742-1745.
43. Rice WR. 1984. Sex chromosomes and the evolution of sex dimorphism. Evolution. 38:735-742.
44. Richards S, Liu Y, Bettencourt BR, et al. (52 co-authors). 2005. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res. 15:1-18.
45. Sawyer SA, Kulathinal RJ, Bustamante CD, Hartl DL. 2003. Bayesian analysis suggests that most amino acid replacements in Drosophila are driven by positive selection. J MolEvol. 57:S154-S164.
46. Sawyer SA, Parsch J, Zhang Z, Hartl DL. 2007. Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci USA. 104:6504-6510.
47. Schoefl G, Schloetterer C. 2004. Patterns of microsatellite variability among X chromosomes and autosomes indicate a high frequency of beneficial mutations in non-african D. simulans. Mol Biol Evol. 21:1384-1390.
48. Sharp PM, Li WH. 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol. 24:28-38.
49. Singh ND, Arndt PF, Petrov DA. 2006. Minor shift in background substitutional patterns in the Drosophila saltans and willistoni lineages is insufficient to explain GC content of coding sequences. BMC Biol. 4:doi:10.1186/1741-7007-1184-1137
50. Singh ND, Bauer DuMont VL, Hubisz MJ, Nielsen R, Aquadro CF. 2007. Patterns of mutation and selection at synonymous sites in Drosophila. Mol Biol Evol. 24:2687-2697.
51. Singh ND, Davis JC, Petrov DA. 2005. X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis. Genetics. 171:145-155.
52. Singh ND, Macpherson JM, Jensen JD, Petrov DA. 2007. Similar levels of X-linked and autosomal nucleotide polymorphism in African and non-African strains of Drosophila melanogaster. BMC Evol Biol. 7.
53. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci USA. 98:7375-7379.
54. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA. 98:7375-7379.
55. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-140.
56. Thornton K, Bachtrog D, Andolfatto P. 2006. X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution. Genome Res. 16:498-504.
57. Thornton K, Long M. 2002. Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol Biol Evol. 19:918-925.
58. True JR, Mercer JM, Laurie CC. 1996. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 142:507-523.
59. Vicario S, Moriyama EN, Powell JR. 2007. Codon usage in twelve species of Drosophila. BMC Evol Biol. 7:226.
60. Vicoso B, Charlesworth B. 2006. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet. 7:645-653.
61. Wall JD, Andolfatto P, Przeworski M. 2002. Testing models of selection and demography in Drosophila simulans. Genetics. 162:203-216.
62. Wang K, Kean L, Yang J, Allan AK, Davies SA, Herzyk P, Dow JAT. 2004. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 5:R69.
63. Welch JJ. 2006. Estimating the genomewide rate of adaptive protein evolution in Drosophila. Genetics. 173:821-837.
64. Wong A, Jensen JD, Pool JE, Aquadro CF. 2007. Phylogenetic incongruence in the Drosophila melanogaster species group. Mol Phylogen Evol. 43:1138-1150.
65. Yanai I, Benjamin H, Shmoish M, et al. 2005. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics. 21:650-659.
66. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15:568-573.