Recent human adaptation: Genomic approaches, interpretation and insights

Nature Reviews Genetics

Volumn 14, Issue 10, 2013, Pages 692-702

  Scheinfeldt, Laura B ^a,b   Tishkoff, Sarah A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Laboratory of Molecular and Cellular Biology of Hematopoiesis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1;

ADAPTATION; DEMOGRAPHY; FUNCTIONAL GENOMICS; GENE FREQUENCY; GENETIC ASSOCIATION; GENOME; GENOMICS; HAPLOTYPE; HUMAN; MUTATION RATE; PHENOTYPE; POPULATION STRUCTURE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TECHNOLOGY; ULTRAVIOLET RADIATION;

EID: 84884467851     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3604     Document Type: Review

References (110)

1. Scheinfeldt, L. B., Soi, S. & Tishkoff, S. A. Colloquium paper: working toward a synthesis of archaeological, linguistic, and genetic data for inferring African population history. Proc. Natl Acad. Sci. USA 107 (Suppl. 2), 8931-8938 (2010).
2. Henn, B. M., Cavalli-Sforza, L. L. & Feldman, M. W. The great human expansion. Proc. Natl Acad. Sci. USA 109, 17758-17764 (2012).
3. Jobling, M. A., Hurles, M. & Tyler-Smith, C. Human Evolutionary Genetics: Origins, Peoples and Disease (Garland Publishing, 2004).
4. Fraser, H. B. Gene expression drives local adaptation in humans. Genome Res. 23, 1089-1096 (2013).
5. Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832-837 (2002). (Pubitemid 35238568)
6. Scheinfeldt, L. B. et al. Population genomic analysis of ALMS1 in humans reveals a surprisingly complex evolutionary history. Mol. Biol. Evol. 26, 1357-1367 (2009).
7. Kleinjan, D. A. & van Heyningen, V. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76, 8-32 (2005). (Pubitemid 40023762)
8. Thorisson, G. A. & Stein, L. D. The SNP Consortium website: past, present and future. Nucleic Acids Res. 31, 124-127 (2003). (Pubitemid 36150350)
9. International HapMap Consortium. A haplotype map of the human genome. Nature 437, 1299-1320 (2005).
10. Hinds, D. A. et al. Whole-genome patterns of common DNA variation in three human populations. Science 307, 1072-1079 (2005). (Pubitemid 40262106)
11. Li, J. Z. et al. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319, 1100-1104 (2008). (Pubitemid 351300793)
12. Jakobsson, M. et al. Genotype, haplotype and copy-number variation in worldwide human populations. Nature 451, 998-1003 (2008). (Pubitemid 351301742)
13. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-918 (2007). (Pubitemid 47598625)
14. Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).
15. Wang, E. T., Kodama, G., Baldi, P. & Moyzis, R. K. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc. Natl Acad. Sci. USA 103, 135-140 (2006). (Pubitemid 43076117)
16. Williamson, S. H. et al. Localizing recent adaptive evolution in the human genome. PLoS Genet. 3, e90 (2007).
17. Zhang, C. et al. A whole genome long-range haplotype (WGLRH) test for detecting imprints of positive selection in human populations. Bioinformatics 22, 2122-2128 (2006). (Pubitemid 44390903)
18. Kelley, J. L., Madeoy, J., Calhoun, J. C., Swanson, W. & Akey, J. M. Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Res. 16, 980-989 (2006). (Pubitemid 44162257)
19. Kimura, R., Fujimoto, A., Tokunaga, K. & Ohashi, J. A practical genome scan for population-specific strong selective sweeps that have reached fixation. PLoS ONE 2, e286 (2007).
20. Pickrell, J. K. et al. Signals of recent positive selection in a worldwide sample of human populations. Genome Res. 19, 826-837 (2009).
21. Fumagalli, M. et al. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7, e1002355 (2011).
22. Brodwin, P. "Bioethics in action" and human population genetics research. Cult. Med. Psychiatry 29, 145-178 (2005). (Pubitemid 41545603)
23. Clark, A. G., Hubisz, M. J., Bustamante, C. D., Williamson, S. H. & Nielsen, R. Ascertainment bias in studies of human genome-wide polymorphism. Genome Res. 15, 1496-1502 (2005). (Pubitemid 41545003)
24. Biswas, S., Scheinfeldt, L. B. & Akey, J. M. Genome-wide insights into the patterns and determinants of fine-scale population structure in humans. Am. J. Hum. Genet. 84, 641-650 (2009).
25. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065-1093 (2012).
26. Pickrell, J. K. et al. The genetic prehistory of southern Africa. Nature Commun. 3, 1143 (2012).
27. Teshima, K. M., Coop, G. & Przeworski, M. How reliable are empirical genomic scans for selective sweeps? Genome Res. 16, 702-712 (2006). (Pubitemid 43830690)
28. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 (1989). (Pubitemid 19274682)
29. Fay, J. C. & Wu, C. I. Hitchhiking under positive Darwinian selection. Genetics 155, 1405-1413 (2000). (Pubitemid 30463447)
30. Fu, Y. X. & Li, W. H. Statistical tests of neutrality of mutations. Genetics 133, 693-709 (1993).
31. ST. Nature Rev. Genet. 10, 639-650 (2009).
32. Shriver, M. D. et al. The genomic distribution of population substructure in four populations using 8, 525 autosomal SNPs. Hum. Genom. 1, 274-286 (2004).
33. Yi, X. et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75-78 (2010).
34. Chen, H., Patterson, N. & Reich, D. Population differentiation as a test for selective sweeps. Genome Res. 20, 393-402 (2010).
35. Grossman, S. R. et al. A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327, 883-886 (2010).
36. Liu, X. et al. Detecting and characterizing genomic signatures of positive selection in global populations. Am. J. Hum. Genet. 92, 866-881 (2013).
37. Sabeti, P. C. et al. Positive natural selection in the human lineage. Science 312, 1614-1620 (2006). (Pubitemid 43902654)
38. Oleksyk, T. K., Smith, M. W. & O'Brien, S. J. Genome-wide scans for footprints of natural selection. Phil. Trans. R. Soc. B 365, 185-205 (2010).
39. Lohmueller, K. E. et al. Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet. 7, e1002326 (2011).
40. Price, A. L. et al. Long-range LD can confound genome scans in admixed populations. Am. J. Hum. Genet. 83, 132-135 (2008). (Pubitemid 351905729)
41. Tang, H. et al. Response to Price et al. Am. J. Hum. Genet. 83, 135-139 (2008).
42. Przeworski, M., Coop, G. & Wall, J. D. The signature of positive selection on standing genetic variation. Evolution 59, 2312-2323 (2005). (Pubitemid 41752645)
43. Innan, H. & Kim, Y. Detecting local adaptation using the joint sampling of polymorphism data in the parental and derived populations. Genetics 179, 1713-1720 (2008).
44. Pritchard, J. K., Pickrell, J. K. & Coop, G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20, R208-R215 (2010).
45. Cutter, A. D. & Payseur, B. A. Genomic signatures of selection at linked sites: unifying the disparity among species. Nature Rev. Genet. 14, 262-274 (2013).
46. Coop, G. et al. The role of geography in human adaptation. PLoS Genet. 5, e1000500 (2009).
47. Daub, J. T. et al. Evidence for polygenic adaptation to pathogens in the human genome. Mol. Biol. Evol. 30, 1544-1558 (2013).
48. Hernandez, R. D. et al. Classic selective sweeps were rare in recent human evolution. Science 331, 920-924 (2011).
49. Simonson, T. S. et al. Genetic evidence for high-altitude adaptation in Tibet. Science 329, 72-75 (2010).
50. Hancock, A. M. et al. Adaptations to climate-mediated selective pressures in humans. PLoS Genet. 7, e1001375 (2010).
51. Moore, L. G. et al. Maternal adaptation to high-altitude pregnancy: an experiment of nature-a review. Placenta 25 (Suppl. A), S60-S71 (2004). (Pubitemid 38514959)
52. Buzbas, E. O., Joyce, P. & Rosenberg, N. A. Inference on the strength of balancing selection for epistatically interacting loci. Theor. Popul. Biol. 79, 102-113 (2011).
53. Scheinfeldt, L. B., Biswas, S., Madeoy, J., Connelly, C. F. & Akey, J. M. Clusters of adaptive evolution in the human genome. Frontiers Genet. 2, 50 (2011).
54. Akey, J. M. Constructing genomic maps of positive selection in humans: where do we go from here? Genome Res. 19, 711-722 (2009).
55. Li, J. et al. Joint analysis of demography and selection in population genetics: where do we stand and where could we go? Mol. Ecol. 21, 28-44 (2012).
56. Granka, J. M. et al. Limited evidence for classic selective sweeps in African populations. Genetics 192, 1049-1064 (2012).
57. Quach, H. et al. Signatures of purifying and local positive selection in human miRNAs. Am. J. Hum. Genet. 84, 316-327 (2009).
58. Andres, A. M. et al. Targets of balancing selection in the human genome. Mol. Biol. Evol. 26, 2755-2764 (2009).
59. Nielsen, R. et al. Darwinian and demographic forces affecting human protein coding genes. Genome Res. 19, 838-849 (2009).
60. Bazin, E., Dawson, K. J. & Beaumont, M. A. Likelihood-free inference of population structure and local adaptation in a Bayesian hierarchical model. Genetics 185, 587-602 (2010)
61. Sousa, V. M., Carneiro, M., Ferrand, N. & Hey, J. Identifying loci under selection against gene flow in isolation with migration models. Genetics 194, 211-233 (2013).
62. Bersaglieri, T. et al. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 74, 1111-1120 (2004). (Pubitemid 38669310)
63. Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nature Genet. 39, 31-40 (2007). (Pubitemid 46026499)
64. Lamason, R. L. et al. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310, 1782-1786 (2005). (Pubitemid 41814374)
65. Jablonski, N. G. & Chaplin, G. The evolution of human skin coloration. J. Hum. Evol. 39, 57-106 (2000). (Pubitemid 30480792)
66. Beleza, S. et al. Genetic architecture of skin and eye color in an African-European admixed population. PLoS Genet. 9, e1003372 (2013).
67. Lango Allen, H. et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467, 832-838 (2010).
68. Kang, S. J. et al. Genome-wide association of anthropometric traits in African-and African-derived populations. Hum. Mol. Genet. 19, 2725-2738 (2010).
69. Jarvis, J. P. et al. Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African Pygmies. PLoS Genet. 8, e1002641 (2012).
70. Migliano, A. B., Vinicius, L. & Lahr, M. M. Life history trade-offs explain the evolution of human pygmies. Proc. Natl Acad. Sci. USA 104, 20216-20219 (2007).
71. Perry, G. H. & Dominy, N. J. Evolution of the human Pygmy phenotype. Trends Ecol. Evol. 24, 218-225 (2009).
72. Mendizabal, I., Marigorta, U. M., Lao, O. & Comas, D. Adaptive evolution of loci covarying with the human African Pygmy phenotype. Hum. Genet. 131, 1305-1317 (2012).
73. Turchin, M. C. et al. Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nature Genet. 44, 1015-1019 (2012).
74. Bigham, A. W. et al. Andean and Tibetan patterns of adaptation to high altitude. Am. J. Hum. Biol. 25, 190-197 (2013).
75. Bigham, A. W. et al. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum. Genom. 4, 79-90 (2009).
76. Peng, Y. et al. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol. Biol. Evol. 28, 1075-1081 (2011).
77. Beall, C. M. et al. Natural selection on EPAS1 (HIF2α) associated with low hemoglobin concentration in Tibetan highlanders. Proc. Natl Acad. Sci. USA 107, 11459-11464 (2010).
78. Scheinfeldt, L. B. et al. Genetic adaptation to high altitude in the Ethiopian highlands. Genome Biol. 13, R1 (2012).
79. Alkorta-Aranburu, G. et al. The genetic architecture of adaptations to high altitude in Ethiopia. PLoS Genet. 8, e1003110 (2012).
80. Huerta-Sanchez, E. et al. Genetic signatures reveal high-altitude adaptation in a set of Ethiopian populations. Mol. Biol. Evol. 30, 1877-1888 (2013).
81. Scheinfeldt, L. B. & Tishkoff, S. A. Living the high life: high-altitude adaptation. Genome Biol. 11, 133 (2010).
82. Enattah, N. S. et al. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am. J. Hum. Genet. 82, 57-72 (2008). (Pubitemid 351735951)
83. Imtiaz, F. et al. The T/G 13915 variant upstream of the lactase gene (LCT) is the founder allele of lactase persistence in an urban Saudi population. J. Med. Genet. 44, e89 (2007).
84. Ingram, C. J. et al. A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Hum. Genet. 120, 779-788 (2007). (Pubitemid 46128833)
85. Ingram, C. J., Mulcare, C. A., Itan, Y., Thomas, M. G. & Swallow, D. M. Lactose digestion and the evolutionary genetics of lactase persistence. Hum. Genet. 124, 579-591 (2009).
86. Ingram, C. J. et al. Multiple rare variants as a cause of a common phenotype: several different lactase persistence associated alleles in a single ethnic group. J. Mol. Evol. 69, 579-588 (2009).
87. Norton, H. L. et al. Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol. Biol. Evol. 24, 710-722 (2007). (Pubitemid 46355799)
88. Henn, B. M. et al. Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc. Natl Acad. Sci. USA 108, 5154-5162 (2011).
89. Kudaravalli, S., Veyrieras, J. B., Stranger, B. E., Dermitzakis, E. T. & Pritchard, J. K. Gene expression levels are a target of recent natural selection in the human genome. Mol. Biol. Evol. 26, 649-658 (2009).
90. Grossman, S. R. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703-713 (2013).
91. Lambert, C. A. & Tishkoff, S. A. Genetic structure in African populations: implications for human demographic history. Cold Spring Harb. Symp. Quant. Biol. 74, 395-402 (2009).
92. Luzzatto, L. Sickle cell anaemia and malaria. Mediterr. J. Hematol. Infect. Dis 4, e2012065 (2012).
93. Vernot, B. et al. Personal and population genomics of human regulatory variation. Genome Res. 22, 1689-1697 (2012).
94. Olds, L. C. & Sibley, E. Lactase persistence DNA variant enhances lactase promoter activity in vitro: functional role as a cis regulatory element. Hum. Mol. Genet. 12, 2333-2340 (2003). (Pubitemid 37160877)
95. Hughes, D. A. et al. Parallel selection on TRPV6 in human populations. PLoS ONE 3, e1686 (2008).
96. Akey, J. M., Swanson, W. J., Madeoy, J., Eberle, M. & Shriver, M. D. TRPV6 exhibits unusual patterns of polymorphism and divergence in worldwide populations. Hum. Mol. Genet. 15, 2106-2113 (2006). (Pubitemid 43923400)
97. Kamberov, Y. G. et al. Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152, 691-702 (2013).
98. Miller, C. T. et al. cis-regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131, 1179-1189 (2007). (Pubitemid 350235026)
99. Lao, O., de Gruijter, J. M., van Duijn, K., Navarro, A. & Kayser, M. Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann. Hum. Genet. 71, 354-369 (2007). (Pubitemid 46585678)
100. Varemo, L., Nielsen, J. & Nookaew, I. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res. 41, 4378-4391 (2013).
101. Grundberg, E. et al. Population genomics in a disease targeted primary cell model. Genome Res. 19, 1942-1952 (2009).
102. Xiong, Q., Ancona, N., Hauser, E. R., Mukherjee, S. & Furey, T. S. Integrating genetic and gene expression evidence into genome-wide association analysis of gene sets. Genome Res. 22, 386-397 (2012).
103. Zaykin, D. V., Zhivotovsky, L. A., Czika, W., Shao, S. & Wolfinger, R. D. Combining p-values in large-scale genomics experiments. Pharm. Statist. 6, 217-226 (2007). (Pubitemid 47455261)
104. Mo, Q. et al. Pattern discovery and cancer gene identification in integrated cancer genomic data. Proc. Natl Acad. Sci. USA 110, 4245-4250 (2013).
105. Schadt, E. E. et al. An integrative genomics approach to infer causal associations between gene expression and disease. Nature Genet. 37, 710-717 (2005). (Pubitemid 41754887)
106. Orr, H. A. Testing natural selection versus genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149, 2099-2104 (1998). (Pubitemid 28375975)
107. Fraser, H. B. et al. Systematic detection of polygenic cis-regulatory evolution. PLoS Genet. 7, e1002023 (2011).
108. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nature Rev. Genet. 14, 179-190 (2013).
109. Lachance, J. et al. Evolutionary history and adaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell 150, 457-469 (2012).
110. Lanktree, M. B. et al. Meta-analysis of dense genecentric association studies reveals common and uncommon variants associated with height. Am. J. Hum. Genet. 88, 6-18 (2011).