Interrogating 11 fast-evolving genes for signatures of recent positive selection in worldwide human populations

Molecular Biology and Evolution

Volumn 26, Issue 10, 2009, Pages 2285-2297

  Moreno Estrada, Andrés ^a   Tang, Kun ^b,c   Sikora, Martin ^a   Marqus Bonet, Toms ^a,d   Casals, Ferran ^e   Navarro, Arcadi ^a   Calafell, Francesc ^a,f   Bertranpetit, Jaume ^a,f   Stoneking, Mark ^c   Bosch, Elena ^a,f  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF MONTREAL   (Canada)

^f CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

Author keywords

Accelerated evolution; Extended haplotype homozygosity; Human Genome Diversity Panel; Population differentiation; Recent positive selection; SNP data

Indexed keywords

CD5 ANTIGEN;

ARTICLE; CHIMPANZEE; CONTROLLED STUDY; GENE FREQUENCY; GENE IDENTIFICATION; GENE MAPPING; GENETIC SELECTION; GENETIC VARIABILITY; GENOME; GENOTYPE; HAPLOTYPE; HUMAN; MOLECULAR EVOLUTION; MOUSE; NATURAL SELECTION; NONHUMAN; ORTHOLOGY; PLESIOMORPHY; POPULATION DIFFERENTIATION; POPULATION GENETICS; RAT; SINGLE NUCLEOTIDE POLYMORPHISM;

ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENES; GENETICS, POPULATION; GENOME, HUMAN; HAPLOTYPES; HOMOZYGOTE; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; VESICULAR TRANSPORT PROTEINS;

CANIS FAMILIARIS; PAN; RATTUS;

EID: 70349923247     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp134     Document Type: Article

References (60)

1. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD. 2002. Interrogating a high-density SNP map for signatures of natural selection. Genome Res. 12:1805-1814.
2. Arbiza L, Dopazo J, Dopazo H. 2006. Positive selection, relaxation, and acceleration in the evolution of the human and chimp genome. PLoS Comput Biol. 2:e38.
3. Arbiza L, Duchi S, Montaner D, Burguet J, Pantoja-Uceda D, Pineda-Lucena A, Dopazo J, Dopazo H. 2006. Selective pressures at a codon-level predict deleterious mutations in human disease genes. J Mol Biol. 358:1390-1404.
4. Bakewell MA, Shi P, Zhang J. 2007. More genes underwent positive selection in chimpanzee evolution than in human evolution. Proc Natl Acad Sci USA. 104:7489-7494.
5. Barreiro LB, Laval G, Quach H, Patin E, Quintana-Murci L. 2008. Natural selection has driven population differentiation in modern humans. Nat Genet. 40:340-345.
6. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 21:263-265.
7. Berland R, Wortis HH. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol. 20:253-300.
8. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
9. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, Drake JA, Rhodes M, Reich DE, Hirschhorn JN. 2004. Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet. 74:1111-1120.
10. Bhandoola A, Bosselut R, Yu Q, Cowan ML, Feigenbaum L, Love PE, Singer A. 2002. CD5-mediated inhibition of TCR signaling during intrathymic selection and development does not require the CD5 extracellular domain. Eur J Immunol. 32:1811-1817.
11. Bustamante CD, Fledel-Alon A, Williamson S, et al. (14 coauthors). 2005. Natural selection on protein-coding genes in the human genome. Nature. 437:1153-1157.
12. Cann HM, de Toma C, Cazes L, et al. (41 co-authors). 2002. A human genome diversity cell line panel. Science. 296:261-262.
13. Clark AG, Glanowski S, Nielsen R, et al. (17 co-authors). 2003. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science. 302:1960-1963.
14. Conde L, Vaquerizas JM, Dopazo H, Arbiza L, Reumers J, Rousseau F, Schymkowitz J, Dopazo J. 2006. PupaSuite: finding functional single nucleotide polymorphisms for large-scale genotyping purposes. Nucleic Acids Res. 34:W621-W625.
15. de Bakker PI, Yelensky R, Pe?er I, Gabriel SB, Daly MJ, Altshuler D. 2005. Efficiency and power in genetic association studies. Nat Genet. 37:1217-1223.
16. Eastman SW, Martin-Serrano J, Chung W, Zang T, Bieniasz PD. 2005. Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding. J Biol Chem. 280:628-636.
17. Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online. 1:47-50.
18. Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 131:479-491.
19. Frazer KA, Ballinger DG, Cox DR, et al. (233 co-authors). 2007. A second generation human haplotype map of over 3.1 million SNPs. Nature. 449:851-861.
20. Goni JR, de la Cruz X, Orozco M. 2004. Triplex-forming oligonucleotide target sequences in the human genome. Nucleic Acids Res. 32:354-360.
21. Grantham R. 1974. Amino acid difference formula to help explain protein evolution. Science. 185:862-864.
22. Han Y, Gu S, Oota H, Osier MV, Pakstis AJ, Speed WC, Kidd JR, Kidd KK. 2007. Evidence of positive selection on a class I ADH locus. Am J Hum Genet. 80:441-456.
23. Hawks J, Wang ET, Cochran GM, Harpending HC, Moyzis RK. 2007. Recent acceleration of human adaptive evolution. Proc Natl Acad Sci USA. 104:20753-20758.
24. Hinds DA, Stuve LL, Nilsen GB, Halperin E, Eskin E, Ballinger DG, Frazer KA, Cox DR. 2005. Whole-genome patterns of common DNA variation in three human populations. Science. 307:1072-1079.
25. Hughes DA, Tang K, Strotmann R, Schoneberg T, Prenen J, Nilius B, Stoneking M. 2008. Parallel selection on TRPV6 in human populations. PLoS ONE. 3:e1686.
26. Kimura R, Fujimoto A, Tokunaga K, Ohashi J. 2007. A practical genome scan for population-specific strong selective sweeps that have reached fixation. PLoS ONE. 2:e286.
27. Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, Siepel A. 2008. Patterns of positive selection in six Mammalian genomes. PLoS Genet. 4:e1000144.
28. Li JZ, Absher DM, Tang H, et al. (11 co-authors). 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science. 319:1100-1104.
29. Morcillo-Suarez C, Alegre J, Sangros R, et al. (17 co-authors). 2008. SNP analysis to results (SNPator): a web-based environment oriented to statistical genomics analyses upon SNP data. Bioinformatics. 24:1643-1644.
30. Moreno-Estrada A, Casals F, Ramirez-Soriano A, Oliva B, Calafell F, Bertranpetit J, Bosch E. 2008. Signatures of selection in the human olfactory receptor OR5I1 gene. Mol Biol Evol. 25:144-154.
31. Myles S, Tang K, Somel M, Green RE, Kelso J, Stoneking M. 2008. Identification and analysis of genomic regions with large between-population differentiation in humans. Ann Hum Genet. 72:99-110.
32. Nickel GC, Tefft D, Adams MD. 2008. Human PAML browser: a database of positive selection on human genes using phylogenetic methods. Nucleic Acids Res. 36:D800-D808.
33. Nielsen R, Bustamante C, Clark AG, et al. (12 co-authors). 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3:e170.
34. 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.
35. Nozawa M, Suzuki Y, Nei M. 2009. Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci USA. 106:6700-6705.
36. Pena-Rossi C, Zuckerman LA, Strong J, Kwan J, Ferris W, Chan S, Tarakhovsky A, Beyers AD, Killeen N. 1999. Negative regulation of CD4 lineage development and responses by CD5. J Immunol. 163:6494-6501.
37. Pickrell JK, Coop G, Novembre J, et al. (11 co-authors). 2009. Signals of recent positive selection in a worldwide sample of human populations. Genome Res. 19:826-837.
38. Pieper U, Eswar N, Braberg H, et al. (15 co-authors). 2004. MODBASE, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 32:D217-D222.
39. Ramensky V, Bork P, Sunyaev S. 2002. Human non-synonymous SNPs: server and survey. Nucleic Acids Res. 30:3894-3900.
40. Ravetch JV, Lanier LL. 2000. Immune inhibitory receptors. Science. 290:84-89.
41. Rosenberg NA. 2006. Standardized subsets of the HGDP-CEPH Human Genome Diversity Cell Line Panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann Hum Genet. 70:841-847.
42. Sabeti PC, Reich DE, Higgins JM, et al. (17 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature. 419:832-837.
43. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES. 2006. Positive natural selection in the human lineage. Science. 312:1614-1620.
44. Sabeti PC, Varilly P, Fry B, et al. (244 co-authors). 2007. Genome-wide detection and characterization of positive selection in human populations. Nature. 449:913-918.
45. Scheet P, Stephens M. 2006. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet. 78:629-644.
46. Sellick GS, Wade R, Richards S, Oscier DG, Catovsky D, Houlston RS. 2008. Scan of 977 nonsynonymous SNPs in CLL4 trial patients for the identification of genetic variants influencing prognosis. Blood. 111:1625-1633.
47. Sikora M, Ferrer-Admetlla A, Mayor A, Bertranpetit J, Casals F. 2008. Evolutionary analysis of genes of two pathways involved in placental malaria infection. Hum Genet. 123:343-357.
48. Storey JD, Tibshirani R. 2003. Statistical significance for genome-wide studies. Proc Natl Acad Sci USA. 100:9440-9445.
49. Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, McKinnon R, Krausslich HG, Morham SG, Sundquist WI. 2004. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J Biol Chem. 279:36059-36071.
50. Tang K, Thornton KR, Stoneking M. 2007. A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol. 5:e171.
51. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
52. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
53. Walsh EC, Sabeti P, Hutcheson HB, et al. (16 co-authors). 2006. Searching for signals of evolutionary selection in 168 genes related to immune function. Hum Genet. 119:92-102.
54. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R. 2007. Localizing recent adaptive evolution in the human genome. PLoS Genet. 3:e90.
55. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13: 555-556.
56. Yang Z, Bielawski JP. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol Evol. 15:496-503.
57. Yang Z, Nielsen R, Goldman N, Pedersen AM. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155:431-449.
58. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
59. Zhang J, Kumar S, Nei M. 1997. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol. 14:1335-1338.
60. 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.