Human adaptation and population differentiation in the light of ancient genomes

Nature Communications

Volumn 7, Issue , 2016, Pages

  Key, Felix M ^a   Fu, Qiaomei ^a,b,c   Romagne, Frederic ^a   Lachmann, Michael ^a,d   Andres, Aida M ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; COLONIZATION; GENOME; HUMAN EVOLUTION; HUNTER-GATHERER; LOCAL ADAPTATION; PERSISTENCE; POPULATION GENETICS; STATISTICAL ANALYSIS; UNCERTAINTY ANALYSIS;

ADAPTATION; AFRICAN; ALLELE; ANCESTRY GROUP; ARTICLE; EAST ASIAN; EUROPEAN; EVOLUTION; GENE FREQUENCY; GENETIC ASSOCIATION; HUMAN; HUMAN CHROMOSOME; HUMAN GENOME; LOCAL ADAPTATION; NATURAL SELECTION; POPULATION DIFFERENTIATION; SINGLE NUCLEOTIDE POLYMORPHISM; ASIAN CONTINENTAL ANCESTRY GROUP; CAUCASIAN; GENETICS; HAPLOTYPE; OVERLAPPING GENE; POPULATION GENETICS;

EURASIA; EUROPE;

ADAPTATION, BIOLOGICAL; ALLELES; ASIAN CONTINENTAL ANCESTRY GROUP; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENES, OVERLAPPING; GENETICS, POPULATION; GENOME, HUMAN; HAPLOTYPES; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84961805950     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10775     Document Type: Article

References (67)

1. Manica, A., Prugnolle, F., Balloux, F. Geography is a better determinant of human genetic differentiation than ethnicity. Hum. Genet. 118, 366-371 (2005).
2. Coop, G. et al. The role of geography in human adaptation. PLoS Genet. 5, e1000500 (2009).
3. Voight, B. F., Kudaravalli, S., Xiaoquan, W., Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).
4. Grossman, S. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703-713 (2013).
5. Bersaglieri, T. et al. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 74, 1111-1120 (2004).
6. Key, F. M. et al. Selection on a variant associated with improved viral clearance drives local, adaptive pseudogenization of interferon lambda 4 (IFNL4). PLoS Genet. 10, e1004681 (2014).
7. Hamblin, M. T., Rienzo, A. D. Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am. J. Hum. Genet. 66, 1669-1679 (2000).
8. Barreiro, L. B., Laval, G., Quach, H., Patin, E., Quintana-Murci, L. Natural selection has driven population differentiation in modern humans. Nat. Genet. 40, 340-345 (2008).
9. 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).
10. Pritchard, J. K., Di Rienzo, A. Adaptation-not by sweeps alone. Nat. Rev. Genet. 11, 665-667 (2010).
11. Turchin, M. C. et al. Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nat. Genet. 44, 1015-1019 (2012).
12. Berg, J. J., Coop, G. A population genetic signal of polygenic adaptation. PLoS Genet. 10, e1004412 (2014).
13. Daub, J. T. et al. Evidence for polygenic adaptation to pathogens in the human genome. Mol. Biol. Evol. 30, 1544-1558 (2013).
14. Voight, B. F. et al. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc. Natl Acad. Sci. USA 102, 18508-18513 (2005).
15. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172 (2015).
16. Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).
17. Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499-503 (2015).
18. Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225-228 (2014).
19. 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).
20. McVean, G. A. et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
21. Busing, F. M., Meijer, E., Van Der Leeden, R. Delete-m jackknife for unequal m. Stat. Comput. 9, 3-8 (1999).
22. Charlesworth, B., Nordborg, M., Charlesworth, D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet. Res. 70, 155-174 (1997).
23. Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445-449 (2014).
24. Keinan, A., Mullikin, J. C., Patterson, N., Reich, D. Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat. Genet. 39, 1251-1255 (2007).
25. Llorente, M. G. et al. Ancient Ethiopian genome reveals extensive Eurasian admixture throughout the African continent. Science 350, 820-822 (2015).
26. Gravel, S. et al. Demographic history and rare allele sharing among human populations. Proc. Natl Acad. Sci. USA 108, 11983-11988 (2011).
27. Hofer, T., Ray, N., Wegmann, D., Excoffier, L. Large allele frequency differences between human continental groups are more likely to have occurred by drift during range expansions than by selection. Ann. Hum. Genet. 73, 95-108 (2009).
28. Harris, K. Evidence for recent, population-specific evolution of the human mutation rate. Proc. Natl Acad. Sci. USA 112, 3439-3444 (2015).
29. Vernot, B., Akey, J. M. Resurrecting surviving Neandertal lineages from modern human genomes. Science 343, 1017-1021 (2014).
30. Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222-226 (2012).
31. Siepel, A. et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050 (2005).
32. Boyle, A. P. et al. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 22, 1790-1797 (2012).
33. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409 (2014).
34. Skoglund, P. et al. Origins and genetic legacy of neolithic farmers and huntergatherers in Europe. Science 336, 466-469 (2012).
35. Skoglund, P. et al. Genomic diversity and admixture differs for Stone-Age Scandinavian foragers and farmers. Science 344, 747-750 (2014).
36. Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87-91 (2013).
37. Günther, T. et al. Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques. Proc. Natl Acad. Sci. USA 112, 11917-11922 (2015).
38. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211 (2015).
39. Sturm, R. A., Duffy, D. L. Human pigmentation genes under environmental selection. Genome Biol. 13, 10-1186 (2012).
40. Grossman, S. R. et al. A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327, 883 (2010).
41. Soejima, M., Tachida, H., Ishida, T., Sano, A., Koda, Y. Evidence for recent positive selection at the human AIM1 locus in a European population. Mol. Biol. Evol. 23, 179-188 (2006).
42. 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).
43. Branicki, W., Brudnik, U., Wojas-Pelc, A. Interactions between HERC2, OCA2 and MC1R may influence human pigmentation phenotype. Ann. Hum. Genet. 73, 160-170 (2009).
44. Graf, J., Hodgson, R., van Daal, A. Single nucleotide polymorphisms in the MATP gene are associated with normal human pigmentation variation. Hum. Mutat. 25, 278-284 (2005).
45. Fernandez, L. P. et al. SLC45A2 : a novel malignant melanoma-associated gene. Hum. Mutat. 29, 1161-1167 (2008).
46. Jablonski, N. G., Chaplin, G. The evolution of human skin coloration. J. Hum. Evol. 39, 57-106 (2000).
47. Sher, L. The role of genetic factors in the etiology of seasonality and seasonal affective disorder: an evolutionary approach. Med. Hypotheses 54, 704-707 (2000).
48. Nischler, C. et al. Iris color and visual functions. Graefes Arch. Clin. Exp. Ophthalmol. 251, 195-202 (2013).
49. Laeng, B., Mathisen, R., Johnsen, J.-A. Why do blue-eyed men prefer women with the same eye color? Behav. Ecol. Sociobiol. 61, 371-384 (2007).
50. Scrimshaw, N. S., Murray, E. B. The acceptability of milk and milk products in populations with a high prevalence of lactose intolerance. Am. J. Clin. Nutr. 48, 1142-1159 (1988).
51. Cavalli-Sforza, L. L. Analytic review: some current problems of human population genetics. Am. J. Hum. Genet. 25, 82-104 (1973).
52. Evershed, R. P. et al. Earliest date for milk use in the Near East and southeastern Europe linked to cattle herding. Nature 455, 528-531 (2008).
53. Enattah, N. S. et al. Identification of a variant associated with adult-type hypolactasia. Nat. Genet. 30, 233-237 (2002).
54. Paten, B. et al. Genome-wide nucleotide-level mammalian ancestor reconstruction. Genome Res. 18, 1829 (2008).
55. Kvikstad, E. M., Duret, L. Strong heterogeneity in mutation rate causes misleading hallmarks of natural selection on indel mutations in the human genome. Mol. Biol. Evol. 31, 23-36 (2014).
56. Reich, D., Thangaraj, K., Patterson, N., Price, A. L., Singh, L. Reconstructing Indian population history. Nature 461, 489-494 (2009).
57. Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710-722 (2010).
58. Skoglund, P. et al. Genetic evidence for two founding populations of the Americas. Nature 525, 104-108 (2015).
59. Hudson, R. R. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18, 337-338 (2002).
60. Gutenkunst, R. N. A. H., Williamson, R. D. A., Bustamante, S. H. A., Carlos, C. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5, e1000695 (2009).
61. McVicker, G., Gordon, D., Davis, C., Green, P. Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet. 5, e1000471 (2009).
62. Sankararaman, S. et al. The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507, 354-357 (2014).
63. Edgar, R., Domrachev, M., Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210 (2002).
64. Consortium, E. P. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
65. Prüfer, K. et al. FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinformatics 8, 41 (2007).
66. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).
67. Jombart, T., Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070-3071 (2011).