Major role of positive selection in the evolution of conservative segments of Drosophila proteins

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1742, 2012, Pages 3409-3417

  Bazykin, Georgii A ^a,b   Kondrashov, Alexey S ^a,c  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Double substitutions; McDonald Kreitman test; Negative selection; Positive selection

Indexed keywords

ALLELE; CONSERVATION GENETICS; DATA SET; FLY; GENETIC ANALYSIS; PROTEIN; SEGMENTATION; SELECTION;

DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS;

EID: 84864398902     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0776     Document Type: Article

References (55)

1. Kimura, M. 1985 The neutral theory of molecular evolution. Cambridge, UK: Cambridge University Press.
2. Yang, Z. & Nielsen, R. 2002 Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19, 908-917. (doi:10.1093/oxfordjournals.molbev.a004148)
3. Zhang, J., Nielsen, R. & Yang, Z. 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479. (doi:10.1093/molbev/msi237)
4. Studer, R. A., Penel, S., Duret, L. & Robinson-Rechavi, M. 2008 Pervasive positive selection on duplicated and nonduplicated vertebrate protein coding genes. Genome Res. 18, 1393-1402. (doi:10.1101/gr.076992.108)
5. Wang, H.-Y., Tang, H., Shen, C.-K. J. & Wu, C.-I. 2003 Rapidly evolving genes in human. I. The glycophorins and their possible role in evading malaria parasites. Mol. Biol. Evol. 20, 1795-1804. (doi:10.1093/molbev/msg185)
6. Barrier, M., Bustamante, C. D., Yu, J. & Purugganan, M. D. 2003 Selection on rapidly evolving proteins in the Arabidopsis genome. Genetics 163, 723-733.
7. Jiggins, F. M. & Kim, K. W. 2007 A screen for immunity genes evolving under positive selection in Drosophila. J. Evol. Biol. 20, 965-970. (doi:10.1111/j.1420-9101.2007.01305.x)
8. Kosiol, C., Vinar, T., da Fonseca, R. R., Hubisz, M. J., Bustamante, C. D., Nielsen, R. & Siepel, A. 2008 Patterns of positive selection in six Mammalian genomes. PLoS Genet. 4, e1000144. (doi:10.1371/journal.pgen.1000144)
9. Aguileta, G., Refregiér, G., Yockteng, R., Fournier, E. & Giraud, T. 2009 Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect. Genet. Evol. 9, 656-670. (doi:10.1016/j.meegid.2009.03.010)
10. Fay, J. C., Wyckoff, G. J. & Wu, C.-I. 2002 Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024-1026. (doi:10.1038/4151024a)
11. Clark, A. G. et al. 2007 Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203-218. (doi:10.1038/nature06341)
12. Bierne, N. & Eyre-Walker, A. 2004 The genomic rate of adaptive amino acid substitution in Drosophila. Mol. Biol. Evol. 21, 1350-1360. (doi:10.1093/molbev/msh134)
13. Welch, J. J. 2006 Estimating the genomewide rate of adaptive protein evolution in Drosophila. Genetics 173, 821-837. (doi:10.1534/genetics.106.056911)
14. Charlesworth, J. & Eyre-Walker, A. 2006 The rate of adaptive evolution in enteric bacteria. Mol. Biol. Evol. 23, 1348-1356. (doi:10.1093/molbev/msk025)
15. Haddrill, P. R., Loewe, L. & Charlesworth, B. 2010 Estimating the parameters of selection on nonsynonymous mutations in Drosophila pseudoobscura and D. miranda. Genetics 185, 1381-1396. (doi:10.1534/genetics.110.117614)
16. Andolfatto, P. 2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437, 1149-1152. (doi:10.1038/nature04107)
17. Halligan, D. L., Oliver, F., Guthrie, J., Stemshorn, K. C., Harr, B. & Keightley, P. D. 2011 Positive and negative selection in murine ultra-conserved noncoding elements. Mol. Biol. Evol. 28, 2651-2660. (doi:10.1093/molbev/msr093)
18. Cai, J. J., Macpherson, J. M., Sella, G. & Petrov, D. A. 2009 Pervasive hitchhiking at coding and regulatory sites in humans. PLoS Genet. 5, e1000336. (doi:10.1371/journal.pgen.1000336)
19. Callahan, B., Neher, R. A., Bachtrog, D., Andolfatto, P., Shraiman, B. I. & McVean, G. 2011 Correlated evolution of nearby residues in Drosophilid proteins. PLoS Genet. 7, e1001315. (doi:10.1371/journal.pgen.1001315)
20. McDonald, J. H. & Kreitman, M. 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652-654. (doi:10.1038/351652a0)
21. Smith, N. G. C. & Eyre-Walker, A. 2002 Adaptive protein evolution in Drosophila. Nature 415, 1022-1024. (doi:10.1038/4151022a)
22. Nielsen, R., Hellmann, I., Hubisz, M., Bustamante, C. & Clark, A. G. 2007 Recent and ongoing selection in the human genome. Nat. Rev. Genet. 8, 857-868. (doi:10.1038/nrg2187)
23. Charlesworth, J. & Eyre-Walker, A. 2008 The McDonald-Kreitman test and slightly deleterious mutations. Mol. Biol. Evol. 25, 1007-1015. (doi:10.1093/molbev/msn005)
24. Eyre-Walker, A. 2006 The genomic rate of adaptive evolution. Trends Ecol. Evol. (Amst.) 21, 569-575. (doi:10.1016/j.tree.2006.06.015)
25. Shapiro, J. A. et al. 2007 Adaptive genic evolution in theDrosophila genomes. Proc. Natl Acad. Sci. USA 104, 2271-2276. (doi:10.1073/pnas.0610385104)
26. Eyre-Walker, A. & Keightley, P. D. 2009 Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol. Biol. Evol. 26, 2097-2108. (doi:10.1093/molbev/msp119)
27. Sella, G., Petrov, D. A., Przeworski, M., Andolfatto, P. & Nachman, M. W. 2009 Pervasive natural selection in the Drosophila genome? PLoS Genet. 5, e1000495. (doi:10.1371/journal.pgen.1000495)
28. Andolfatto, P., Wong, K. M. & Bachtrog, D. 2011 Effective population size and the efficacy of selection on the X chromosomes of two closely related Drosophila species. Genome. Biol. Evol. 3, 114-128. (doi:10.1093/gbe/evq086)
29. Begun, D. J. et al. 2007 Population genomics: wholegenome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5, e310. (doi:10.1371/journal.pbio.0050310)
30. Aquadro, C. F., Lado, K. M. & Noon, W. A. 1988 The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics 119, 875-888.
31. Nolte, V. & Schlötterer, C. 2008 African Drosophila melanogaster and D. simulans populations have similar levels of sequence variability, suggesting comparable effective population sizes. Genetics 178, 405-412. (doi:10.1534/genetics.107.080200)
32. Akashi, H. 1995 Inferring weak selection from patterns of polymorphism and divergence at 'silent' sites in Drosophila DNA. Genetics 139, 1067-1076.
33. Akashi, H. 1999 Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151, 221-238.
34. Akashi, H. 1994 Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136, 927-935.
35. Gossmann, T. I., Song, B.-H., Windsor, A. J., Mitchell-Olds, T., Dixon, C. J., Kapralov, M. V., Filatov, D. A. & Eyre-Walker, A. 2010 Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol. Biol. Evol. 27, 1822-1832. (doi:10.1093/molbev/msq079)
36. Kousathanas, A., Oliver, F., Halligan, D. L. & Keightley, P. D. 2011 Positive and negative selection on noncoding DNA close to protein-coding genes in wild house mice. Mol. Biol. Evol. 28, 1183-1191. (doi:10.1093/molbev/msq299)
37. Bazykin, G. A., Kondrashov, F. A., Ogurtsov, A. Y., Sunyaev, S. & Kondrashov, A. S. 2004 Positive selection at sites of multiple amino acid replacements since rat-mouse divergence. Nature 429, 558-562. (doi:10.1038/nature02601)
38. Bazykin, G. A., Dushoff, J., Levin, S. A. & Kondrashov, A. S. 2006 Bursts of nonsynonymous substitutions in HIV-1 evolution reveal instances of positive selection at conservative protein sites. Proc. Natl Acad. Sci. USA 103, 19 396-19 401. (doi:10.1073/pnas.0609484103)
39. Heger, A. & Ponting, C. P. 2007 Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. Genome Res. 17, 1837-1849. (doi:10.1101/gr.6249707)
40. Nielsen, R. & Yang, Z. 1998 Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929-936.
41. Kordis, D. & Gubensek, F. 2000 Adaptive evolution of animal toxin multigene families. Gene 261, 43-52. (doi:10.1016/S0378-1119(00)00490-X)
42. Juárez, P., Comas, I., Gonzalez-Candelas, F. Calvete, J. J. 2008 Evolution of snake venom disintegrins by positive Darwinian selection. Mol. Biol. Evol. 25, 2391-2407. (doi:10.1093/molbev/msn179)
43. Lee, Y. H. & Vacquier, V. D. 1992 The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol. Bull. 182, 97-104. (doi:10.2307/1542183)
44. Swanson, W. J., Clark, A. G., Waldrip-Dail, H. M., Wolfner, M. F. & Aquadro, C. F. 2001 Evolutionary ESTanalysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl Acad. Sci. USA 98, 7375-7379. (doi:10.1073/pnas.131568198)
45. Schneider, A., Souvorov, A., Sabath, N., Landan, G., Gonnet, G. H. & Graur, D. 2009 Estimates of positive Darwinian selection are inflated by errors in sequencing, annotation, and alignment. Genome Biol. Evol. 1, 114-118. (doi:10.1093/gbe/evp012)
46. Mallick, S., Gnerre, S., Muller, P. & Reich, D. 2009 The difficulty of avoiding false positives in genome scans for natural selection. Genome Res. 19, 922-933. (doi:10.1101/gr.086512.108)
47. Wong, K. M., Suchard, M. A. & Huelsenbeck, J. P. 2008 Alignment uncertainty and genomic analysis. Science 319, 473-476. (doi:10.1126/science.1151532)
48. Markova-Raina, P. & Petrov, D. 2011 High sensitivity to aligner and high rate of false positives in the estimates of positive selection in the 12 Drosophila genomes. Genome Res. 21, 863-874. (doi:10.1101/gr.115949.110)
49. Holloway, A. K., Begun, D. J. & Hahn, M. 2007 Rampant adaptive evolution in regions of proteins with unknown function in Drosophila simulans. PLoS ONE 2, e1113. (doi:10.1371/journal.pone.0001113)
50. Mackay, T. F. C. et al. 2012 The Drosophila melanogaster genetic reference panel. Nature 482, 173-178. (doi:10.1038/nature10811)
51. Smit, A., Hubley, R. & Green, P. 1996 RepeatMasker Open-3.0. See http://www.repeatmasker.org.
52. Benson, G. 1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580. (doi:10.1093/nar/27.2.573)
53. Chen, K. & Rajewsky, N. 2006 Natural selection on human microRNA binding sites inferred from SNP data. Nat. Genet. 38, 1452-1456. (doi:10.1038/ng1910)
54. Fay, J. C., Wyckoff, G. J. & Wu, C. I. 2001 Positive and negative selection on the human genome. Genetics 158, 1227-1234.
55. Clopper, C. J. & Pearson, E. S. 1934 The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26, 404-413. (doi:10.1093/biomet/26.4.404)