Scanning the human genome for signals of selection

Current Opinion in Genetics and Development

Volumn 16, Issue 6, 2006, Pages 624-629

  McVean, Gil ^a   Spencer, Chris CA ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EVOLUTION; GENE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; HUMAN GENOME; PRIORITY JOURNAL; REVIEW;

ADAPTATION, BIOLOGICAL; EVOLUTION, MOLECULAR; GENETIC SCREENING; GENOME, HUMAN; HUMANS; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 33750964658     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.09.004     Document Type: Review

References (55)

1. Sachidanandam R., Weissman D., Schmidt S.C., Kakol J.M., Stein L.D., Marth G., Sherry S., Mullikin J.C., Mortimore B.J., Willey D.L., et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409 (2001) 928-933
2. The International HapMap Consortium. A haplotype map of the human genome. Nature 437 (2005) 1299-1320. Description and analysis of approximately one million single nucleotide polymorphisms typed in 270 individuals from four different populations. The consortium also used various approaches to detect candidate regions for adaptive evolution.
3. Hinds D.A., Stuve L.L., Nilsen G.B., Halperin E., Eskin E., Ballinger D.G., Frazer K.A., and Cox D.R. Whole-genome patterns of common DNA variation in three human populations. Science 307 (2005) 1072-1079. Along with the International HapMap Project, this is the main source of data currently used in genome scans for selective sweeps. The authors show that between-population differentiation is higher in genic than non-genic regions.
4. Bustamante C.D., Fledel-Alon A., Williamson S., Nielsen R., Hubisz M.T., Glanowski S., Tanenbaum D.M., White T.J., Sninsky J.J., Hernandez R.D., et al. Natural selection on protein-coding genes in the human genome. Nature 437 (2005) 1153-1157. Genome-wide comparison of patterns of diversity in divergence, focusing entirely on coding genes. The authors find that nearly 10% of all genes show evidence of rapid amino acid evolution.
5. Akey J.M., Eberle M.A., Rieder M.J., Carlson C.S., Shriver M.D., Nickerson D.A., and Kruglyak L. Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2 (2004) e286
6. Clark A.G., Glanowski S., Nielsen R., Thomas P.D., Kejariwal A., Todd M.A., Tanenbaum D.M., Civello D., Lu F., Murphy B., et al. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302 (2003) 1960-1963
7. Nielsen R., Bustamante C., Clark A.G., Glanowski S., Sackton T.B., Hubisz M.J., Fledel-Alon A., Tanenbaum D.M., Civello D., White T.J., et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3 (2005) e170
8. Voight B.F., Kudaravalli S., Wen X., and Pritchard J.K. A map of recent positive selection in the human genome. PLoS Biol 4 (2006) e72. A well-constructed search for genomic regions where there is evidence for ongoing selective sweeps. In addition to developing a new test for selection, the authors present multiple lines of evidence indicating that the method really does detect adaptive evolution.
9. Wang E.T., Kodama G., Baldi P., and Moyzis R.K. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci USA 103 (2006) 135-140
10. Enard W., Przeworski M., Fisher S.E., Lai C.S., Wiebe V., Kitano T., Monaco A.P., and Paabo S. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418 (2002) 869-872
11. Arbiza L., Dopazo J., and Dopazo H. Positive selection, relaxation, and acceleration in the evolution of the human and chimp genome. PLoS Comput Biol 2 (2006) e38
12. Walsh E.C., Sabeti P., Hutcheson H.B., Fry B., Schaffner S.F., de Bakker P.I., Varilly P., Palma A.A., Roy J., Cooper R., et al. Searching for signals of evolutionary selection in 168 genes related to immune function. Hum Genet 119 (2006) 92-102
13. Izagirre N., Garcia I., Junquera C., de la R.C., and Alonso S. A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol Biol Evol 23 (2006) 1697-1706
14. Varki A., and Altheide T.K. Comparing the human and chimpanzee genomes: searching for needles in a haystack. Genome Res 15 (2005) 1746-1758
15. The Chimpanzee Sequencing Analysis Consortium. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437 (2005) 69-87
16. Bubb K.L., Bovee D., Buckley D., Haugen E., Kibukawa M., Paddock M., Palmier A., Subramanian S., Zhou Y., Kaul R., et al. Scan of human genome reveals no new loci under ancient balancing selection. Genetics 173 (2006) 2165-2177. A great idea - to look for additional regions of the genome where there might be ancient polymorphism - and a well constructed analysis. Unfortunately, the authors do not find any outstanding new candidates.
17. Zhang L., and Li W.H. Human SNPs reveal no evidence of frequent positive selection. Mol Biol Evol 22 (2005) 2504-2507
18. Fay J.C., Wyckoff G.J., and Wu C.I. Positive and negative selection on the human genome. Genetics 158 (2001) 1227-1234
19. Przeworski M., Coop G., and Wall J.D. The signature of positive selection on standing genetic variation. Evolution Int J Org Evolution 59 (2005) 2312-2323. A provocative study that raises the question of whether much of the adaptive evolution in humans might result from selection on existing variation. Not surprisingly, it is much harder to detect such selection.
20. Przeworski M. The signature of positive selection at randomly chosen loci. Genetics 160 (2002) 1179-1189
21. Clark A.G., Hubisz M.J., Bustamante C.D., Williamson S.H., and Nielsen R. Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15 (2005) 1496-1502
22. Stajich J.E., and Hahn M.W. Disentangling the effects of demography and selection in human history. Mol Biol Evol 22 (2005) 63-73
23. Sabeti P.C., Schaffner S.F., Fry B., Lohmueller J., Varilly P., Shamovsky O., Palma A., Mikkelsen T.S., Altshuler D., and Lander E.S. Positive natural selection in the human lineage. Science 312 (2006) 1614-1620. A good review (with excellent supplementary material) of recent efforts to map selective loci. The authors strongly advocate an empirical approach, although they present rather familiar examples to back up their claims.
24. Wall J. Recombination and the power of statistical tests of neutrality. Genet Res 74 (1999) 65-79
25. Wall J.D., and Hudson R.R. Coalescent simulations and statistical tests of neutrality. Mol Biol Evol 18 (2001) 1134-1135
26. Myers S., Bottolo L., Freeman C., McVean G., and Donnelly P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310 (2005) 321-324
27. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 (1989) 585-595
28. Fay J.C., and Wu C.I. Hitchhiking under positive Darwinian selection. Genetics 155 (2000) 1405-1413
29. Carlson C.S., Thomas D.J., Eberle M.A., Swanson J.E., Livingston R.J., Rieder M.J., and Nickerson D.A. Genomic regions exhibiting positive selection identified from dense genotype data. Genome Res 15 (2005) 1553-1565
30. Mekel-Bobrov N., Gilbert S.L., Evans P.D., Vallender E.J., Anderson J.R., Hudson R.R., Tishkoff S.A., and Lahn B.T. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 309 (2005) 1720-1722
31. Evans P.D., Gilbert S.L., Mekel-Bobrov N., Vallender E.J., Anderson J.R., Vaez-Azizi L.M., Tishkoff S.A., Hudson R.R., and Lahn B.T. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309 (2005) 1717-1720
32. Khaitovich P., Tang K., Franz H., Kelso J., Hellmann I., Enard W., Lachmann M., and Paabo S. Positive selection on gene expression in the human brain. Curr Biol 16 (2006) R356-R358
33. McDonald J.H., and Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 (1991) 652-654
34. Hudson R.R., Kreitman M., and Aguade M. A test of neutral molecular evolution based on nucleotide data. Genetics 116 (1987) 153-159
35. Gilad Y., Man O., and Glusman G. A comparison of the human and chimpanzee olfactory receptor gene repertoires. Genome Res 15 (2005) 224-230
36. Spencer CC, Myers S, Deloukas P, Hunt S, Mullikin JC, Bentley D, Donnelly P, McVean G: Scale-specific influences on human genetic diversity. PLoS Genet 2006, in press.
37. Smith A.V., Thomas D.J., Munro H.M., and Abecasis G.R. Sequence features in regions of weak and strong linkage disequilibrium. Genome Res 15 (2005) 1519-1534
38. Lamason R.L., Mohideen M.A., Mest J.R., Wong A.C., Norton H.L., Aros M.C., Jurynec M.J., Mao X., Humphreville V.R., Humbert J.E., et al. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310 (2005) 1782-1786. This is perhaps the only case in which the signature of adaptive evolution has been used to motivate and identify a functional polymorphism in humans. The authors show that a nonsynonymous mutation of this gene, which is found at very different frequencies in African and non-African populations, explains a significant proportion of variation in skin pigmentation.
39. Tishkoff S.A., and Verrelli B.C. Patterns of human genetic diversity: implications for human evolutionary history and disease. Annu Rev Genomics Hum Genet 4 (2003) 293-340
40. Vallender E.J., and Lahn B.T. Positive selection on the human genome. Hum Mol Genet 13 Spec No 2 (2004) R245-R254
41. Stefansson H., Helgason A., Thorleifsson G., Steinthorsdottir V., Masson G., Barnard J., Baker A., Jonasdottir A., Ingason A., Gudnadottir V.G., et al. A common inversion under selection in Europeans. Nat Genet 37 (2005) 129-137. A fascinating piece of biology. The authors show that an inversion that is common in Europe and rare in Africa directly affects female reproductive success and is therefore selectively favourable. However, the inversion is also ancient (i.e. more than one million years old), which suggests that other selective forces must balance it in populations.
42. McVean G., Spencer C.C., and Chaix R. Perspectives on human genetic variation from the HapMap Project. PLoS Genet 1 (2005) e54
43. Bersaglieri T., Sabeti P.C., Patterson N., Vanderploeg T., Schaffner S.F., Drake J.A., Rhodes M., Reich D.E., and Hirschhorn J.N. Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74 (2004) 1111-1120
44. Hamblin M.T., and Di Rienzo A. Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet 66 (2000) 1669-1679
45. Sabeti P.C., Walsh E., Schaffner S.F., Varilly P., Fry B., Hutcheson H.B., Cullen M., Mikkelsen T.S., Roy J., Patterson N., et al. The case for selection at CCR5-Δ32. PLoS Biol 3 (2005) e378
46. Novembre J., Galvani A.P., and Slatkin M. The geographic spread of the CCR5-Δ32 HIV-resistance allele. PLoS Biol 3 (2005) e339
47. Galvani A.P., and Slatkin M. Evaluating plague and smallpox as historical selective pressures for the CCR5-Δ32 HIV-resistance allele. Proc Natl Acad Sci USA 100 (2003) 15276-15279
48. Woods R.P., Freimer N.B., De Young J.A., Fears S.C., Sicotte N.L., Service S.K., Valentino D.J., Toga A.W., and Mazziotta J.C. Normal variants of Microcephalin and ASPM do not account for brain size variability. Hum Mol Genet 15 (2006) 2025-2029
49. Teshima K.M., Coop G., and Przeworski M. How reliable are empirical genomic scans for selective sweeps?. Genome Res 16 (2006) 702-712. Another provocative study, with rather pessimistic conclusions - namely, empirical approaches to scanning for selection are likely to have high false-discovery rates, will miss a large proportion of all selected loci and will create a bias towards finding certain types of selection.
50. Schaffner S.F., Foo C., Gabriel S., Reich D., Daly M.J., and Altshuler D. Calibrating a coalescent simulation of human genome sequence variation. Genome Res 15 (2005) 1576-1583
51. Voight B.F., Adams A.M., Frisse L.A., Qian Y., Hudson R.R., and Di Rienzo A. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci USA 102 (2005) 18508-18513
52. Williamson S.H., Hernandez R., Fledel-Alon A., Zhu L., Nielsen R., and Bustamante C.D. Simultaneous inference of selection and population growth from patterns of variation in the human genome. Proc Natl Acad Sci USA 102 (2005) 7882-7887
53. Nielsen R., Williamson S., Kim Y., Hubisz M.J., Clark A.G., and Bustamante C. Genomic scans for selective sweeps using SNP data. Genome Res 15 (2005) 1566-1575. An ingenious method for detecting selective sweeps that mixes empirical and parametric approaches - essentially looking for regions where the local frequency spectrum is distorted from the genome-wide average in a manner suggestive of selective sweeps.
54. Fu Y.X., and Li W.H. Statistical tests of neutrality of mutations. Genetics 133 (1993) 693-709
55. Spencer C.C., and Coop G. SelSim: a program to simulate population genetic data with natural selection and recombination. Bioinformatics 20 (2004) 3673-3675