Genome-wide patterns of selection in 230 ancient Eurasians

Nature

Volumn 528, Issue 7583, 2015, Pages 499-503

  Mathieson, Iain ^a   Lazaridis, Iosif ^a,b   Rohland, Nadin ^a,b   Mallick, Swapan ^a,b,c   Patterson, Nick ^b   Roodenberg, Songül Alpaslan ^d   Harney, Eadaoin ^a,c   Stewardson, Kristin ^a,c   Fernandes, Daniel ^e   Novak, Mario ^e,f   Sirak, Kendra ^e,g   Gamba, Cristina ^e,h,ac   Jones, Eppie R ^h   Llamas, Bastien ⁱ   Dryomov, Stanislav ^j,k   Pickrell, Joseph ^a,ac,ad   Arsuaga, Juan Luís ^l,m   De Castro, José María Bermúdez ⁿ   Carbonell, Eudald ^o,p   Gerritsen, Fokke ^q   Khokhlov, Aleksandr ^r   Kuznetsov, Pavel ^r   Lozano, Marina ^o,p   Meller, Harald ^s   Mochalov, Oleg ^r   Moiseyev, Vyacheslav ^t   Guerra, Manuel A Rojo ^u   Roodenberg, Jacob ^v   Vergès, Josep Maria ^o,p   Krause, Johannes ^w,x   Cooper, Alan ⁱ   Alt, Kurt W ^s,y,z   Brown, Dorcas ^aa   Anthony, David ^aa   Lalueza Fox, Carles ^ab   Haak, Wolfgang ^i,w   Pinhasi, Ron ^e   Reich, David ^a,b,c   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Institute for Anthropological Research ^*  (Netherlands)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

^f INSTITUTE FOR ANTHROPOLOGICAL RESEARCH   (Croatia)

^g EMORY UNIVERSITY   (United States)

^h TRINITY COLLEGE DUBLIN   (Ireland)

ⁱ UNIVERSITY OF ADELAIDE   (Australia)

^j INSTITUTE OF MOLECULAR AND CELLULAR BIOLOGY   (Russian Federation)

^k INSTITUTE OF ARCHAEOLOGY AND ETHNOGRAPHY   (Russian Federation)

^l INSTITUTO DE SALUD CARLOS III   (Spain)

^m UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

ⁿ CENTRO NACIONAL DE INVESTIGACIÓN SOBRE LA EVOLUCIÓN HUMANA CENIEH   (Spain)

^o INSTITUT CATALÀ DE PALEOECOLOGIA HUMANA I EVOLUCIÓ SOCIAL   (Spain)

^p UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^q Vocational School of Technical Sciences   (Turkey)

^r SAMARA STATE UNIVERSITY OF SOCIAL SCIENCES AND EDUCATION   (Russian Federation)

^s State Office for Heritage Management and Archaeology   (Germany)

^t RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^u UNIVERSITY OF VALLADOLID   (Spain)

^v Netherlands Institute for the Near East (NINO)   (Netherlands)

^w MAX PLANCK INSTITUTE FOR THE SCIENCE OF HUMAN HISTORY   (Germany)

^x UNIVERSITY OF TÜBINGEN   (Germany)

^y Austria   (Austria)

^z UNIVERSITY OF BASEL   (Switzerland)

^aa HARTWICK COLLEGE   (United States)

^ab UNIVERSITAT POMPEU FABRA   (Spain)

^ac UNIVERSITY OF COPENHAGEN   (Denmark)

^ad NEW YORK GENOME CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ADAPTATION; BONE; DATA SET; GENOME; HUMAN EVOLUTION; IMMUNE RESPONSE; MITOCHONDRIAL DNA; NATURAL SELECTION; NEOLITHIC; PIGMENT; STEPPE;

AGRICULTURAL WORKER; ALLELE; ARTICLE; EURASIAN; EUROPEAN; GENE LOCUS; HUMAN; NEOLITHIC; PETROUS BONE; PIGMENTATION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; AGRICULTURE; ASIA; BODY HEIGHT; BONE; DIET; DNA SEQUENCE; ETHNOLOGY; EUROPE; GENETIC SELECTION; GENETICS; HAPLOTYPE; HISTORY; HUMAN GENOME; IMMUNITY; ISOLATION AND PURIFICATION; MALE; MULTIFACTORIAL INHERITANCE; POPULATION GENETICS;

ANATOLIA; RUSSIAN FEDERATION; SAMARA; TURKEY;

AGRICULTURE; ASIA; BODY HEIGHT; BONE AND BONES; DIET; DNA; EUROPE; GENETICS, POPULATION; GENOME, HUMAN; HAPLOTYPES; HISTORY, ANCIENT; HUMANS; IMMUNITY; MALE; MULTIFACTORIAL INHERITANCE; PIGMENTATION; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84951286136     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16152     Document Type: Article

References (60)

1. Grossman, S. R. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703-713 (2013).
2. Wilde, S. et al. Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl Acad. Sci. USA 111, 4832-4837 (2014).
3. Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nature Commun. 5, 5257 (2014).
4. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409-413 (2014).
5. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172 (2015).
6. Keller, A. et al. New insights into the Tyrolean Iceman's origin and phenotype as inferred by whole-genome sequencing. Nature Commun. 3, 698 (2012).
7. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211 (2015).
8. Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225-228 (2014).
9. Pinhasi, R. et al. Optimal ancient DNA yields from the inner ear part of the human petrous bone. PLoS ONE 10, e0129102 (2015).
10. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
11. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065-1093 (2012).
12. Underhill, P. A. et al. The phylogenetic and geographic structure of Y-chromosome haplogroup R1a. Eur. J. Hum. Genet. 23, 124-131 (2015).
13. The 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526, 68-74 (2015).
14. Devlin, B. & Roeder, K. Genomic control for association studies. Biometrics 55, 997-1004 (1999).
15. Enattah, N. S. et al. Identification of a variant associated with adult-type hypolactasia. Nature Genet. 30, 233-237 (2002).
16. Bersaglieri, T. et al. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 74, 1111-1120 (2004).
17. Burger, J., Kirchner, M., Bramanti, B., Haak, W. & Thomas, M. G. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc. Natl Acad. Sci. USA 104, 3736-3741 (2007).
18. Teslovich, T. M. et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466, 707-713 (2010).
19. Fumagalli, M. et al. Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349, 1343-1347 (2015).
20. Mathias, R. A. et al. Adaptive evolution of the FADS gene cluster within Africa. PLoS ONE 7, e44926 (2012).
21. Wang, T. J. et al. Common genetic determinants of vitamin D insufficiency: a genome-wide association study. Lancet 376, 180-188 (2010).
22. Price, A. L. et al. The impact of divergence time on the nature of population structure: an example from Iceland. PLoS Genet. 5, e1000505 (2009).
23. Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447, 661-678(2007).
24. Huff, C. D. et al. Crohn's disease and genetic hitchhiking at IBD5. Mol. Biol. Evol. 29, 101-111 (2012).
25. Hunt, K. A. et al. Newly identified genetic risk variants for celiac disease related to the immune response. Nature Genet. 40, 395-402 (2008).
26. Jostins, L. et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124 (2012).
27. Beleza, S. et al. Genetic architecture of skin and eye color in an African-European admixed population. PLoS Genet. 9, e1003372 (2013).
28. Sturm, R. A. et al. A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue-brown eye color. Am. J. Hum. Genet. 82, 424-431 (2008).
29. Eiberg, H. et al. Blue eye color in humans may be caused by a perfectly associated founder mutation in a regulatory element located within the HERC2 gene inhibiting OCA2 expression. Hum. Genet. 123, 177-187 (2008).
30. Barreiro, L. B. et al. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet. 5, e1000562 (2009).
31. Uciechowski, P. et al. Susceptibility to tuberculosis is associated with TLR1 polymorphisms resulting in a lack of TLR1 cell surface expression. J. Leukoc. Biol. 90, 377-388 (2011).
32. Wong, S. H. et al. Leprosy and the adaptation of human toll-like receptor 1. PLoS Pathog. 6, e1000979 (2010).
33. Fujimoto, A. et al. A scan for genetic determinants of human hair morphology: EDAR is associated with Asian hair thickness. Hum. Mol. Genet. 17, 835-843 (2008).
34. Kimura, R. et al. A common variation in EDAR is a genetic determinant of shovel-shaped incisors. Am. J. Hum. Genet. 85, 528-535 (2009).
35. Kamberov, Y. G. et al. Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152, 691-702 (2013).
36. Turchin, M. C. et al. Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nature Genet. 44, 1015-1019 (2012).
37. Berg, J. J. & Coop, G. et al. A population genetic signal of polygenic adaptation. PLoS Genet. 10, e1004412 (2014).
38. Lango Allen, H. et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467, 832-838 (2010).
39. Speliotes, E. K. et al. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nature Genet. 42, 937-948 (2010).
40. Heid, I. M. et al. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nature Genet. 42, 949-960 (2010).
41. Morris, A. P. et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nature Genet. 44, 981-990 (2012).
42. Briggs, A. W. et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 38, e87 (2010).
43. Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223-2227 (2013).
44. Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature. 524, 216-219 (2015).
45. Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).
46. International HapMap Consortium. A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861 (2007).
47. Lappalainen, T. et al. Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501, 506-511 (2013).
48. Li, J. Z. et al. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319, 1100-1104 (2008).
49. Loh, P. R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233-1254 (2013).
50. Chang, C. C. et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4 (2015).
51. Skoglund, P., Storå, J., Götherström, A. & Jakobsson, M. Accurate sex identification of ancient human remains using DNA shotgun sequencing. J. Archaeol. Sci. 40, 4477-4482 (2013).
52. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
53. 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).
54. Bokor, S. et al. Single nucleotide polymorphisms in the FADS gene cluster are associated with delta-5 and delta-6 desaturase activities estimated by serum fatty acid ratios. J. Lipid Res. 51, 2325-2333 (2010).
55. Tanaka, T. et al. Genome-wide association study of plasma polyunsaturated fatty acids in the InCHIANTI Study. PLoS Genet. 5, e1000338 (2009).
56. Ahn, J. et al. Genome-wide association study of circulating vitamin D levels. Hum. Mol. Genet. 19, 2739-2745 (2010).
57. Gründemann, D. et al. Discovery of the ergothioneine transporter. Proc. Natl Acad. Sci. USA 102, 5256-5261 (2005).
58. Chauhan, S. et al. ZKSCAN3 is a master transcriptional repressor of autophagy. Mol. Cell 50, 16-28 (2013).
59. Soler Artigas, M. et al. Genome-wide association and large-scale follow up identifies 16 new loci influencing lung function. Nature Genet. 43, 1082-1090 (2011).
60. Pruim, R. J. et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26, 2336-2337 (2010).