Population genetic analysis of the DARC locus (Duffy) reveals adaptation from standing variation associated with malaria resistance in humans

PLoS Genetics

Volumn 13, Issue 3, 2017, Pages

  McManus, Kimberly F ^a   Taravella, Angela M ^b   Henn, Brenna M ^b   Bustamante, Carlos D ^a   Sikora, Martin ^a,c   Cornejo, Omar E ^a,d  

^a STANFORD UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ALLELE; ARTICLE; ASIA; CONTROLLED STUDY; DARC GENE; EVOLUTIONARY ADAPTATION; GENE; GENE LOCUS; GENE MUTATION; GENE SEGREGATION; GENETIC SELECTION; GENETIC VARIATION; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HUMAN; HUMAN GENOME; MALARIA; NEXT GENERATION SEQUENCING; PHYLOGENY; POPULATION GENETICS; POSITIVE SELECTION; ANIMAL; BLOOD GROUP DUFFY SYSTEM; DISEASE RESISTANCE; GENE FREQUENCY; GENETICS; GEOGRAPHY; GORILLA GORILLA; METABOLISM; MUTATION; ORANGUTAN; PAN PANISCUS; PAN TROGLODYTES; PLASMODIUM VIVAX MALARIA; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM;

CELL SURFACE RECEPTOR; DARC PROTEIN, HUMAN;

AFRICA; ALLELES; ANIMALS; ASIA; DISEASE RESISTANCE; DUFFY BLOOD-GROUP SYSTEM; GENE FREQUENCY; GENETICS, POPULATION; GENOME, HUMAN; GEOGRAPHY; GORILLA GORILLA; HAPLOTYPES; HUMANS; MALARIA, VIVAX; MUTATION; PAN PANISCUS; PAN TROGLODYTES; POLYMORPHISM, SINGLE NUCLEOTIDE; PONGO; PROMOTER REGIONS, GENETIC; RECEPTORS, CELL SURFACE;

EID: 85016648869     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006560     Document Type: Article

References (117)

1. Haldane J, Disease and evolution. Ric Sci Suppl. 1949;19:68–76.
2. Kwiatkowski DP, How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 2005;77(2):171–192. doi: 10.1086/432519 16001361
3. Gething PW, Elyazar IRF, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6(9):e1814. doi: 10.1371/journal.pntd.0001814 22970336
4. Howes RE, Patil AP, Piel FB, Nyangiri OA, Kabaria CW, Gething PW, et al. The global distribution of the Duffy blood group. Nat Commun. 2011;2:266. doi: 10.1038/ncomms1265 21468018
5. Cutbush M, Mollison PL, Parkin DM, A new human blood group. Nature. 1950;165:188–189. doi: 10.1038/165188b0
6. Miller LH, Mason SJ, Clyde DF, McGinniss MH, The resistance factor to Plasmodium vivax in blacks: the Duffy-blood-group genotype, FyFy. N Engl J Med. 1976;295(6):302–304. doi: 10.1056/NEJM197608052950602 778616
7. Nurse G, Lane A, Jenkins T, Sero-genetic studies on the Dama of South West Africa. Ann Hum Biol. 1976;3(1):33–50. doi: 10.1080/03014467600001121 818940
8. Nurse GT, Jenkins T, Serogenetic studies on the Kavango peoples of South West Africa. Ann Hum Biol. 1977;4(5):465–478. doi: 10.1080/03014467700002451 414652
9. Nurse G, Botha M, Jenkins T, Sero-genetic studies on the San of south West Africa. Hum Hered. 1977;27(2):81–98. doi: 10.1159/000152855 405311
10. Tournamille C, Colin Y, Cartron JP, Le Van Kim C, Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy–negative individuals. Nature Genet. 1995;10(2):224–228. doi: 10.1038/ng0695-224 7663520
11. Kasehagen LJ, Mueller I, Kiniboro B, Bockarie MJ, Reeder JC, Kazura JW, et al. Reduced Plasmodium vivax erythrocyte infection in PNG Duffy-negative heterozygotes. PLoS One. 2007;2(3):e336. doi: 10.1371/journal.pone.0000336 17389925
12. Weber SS, Tadei WP, Martins AS, Polymorphism of the Duffy blood group system influences the susceptibility to Plasmodium vivax infection in the specific area from Brazilian Amazon. Brazilian Journal of Pharmacy. 2012;93(1):33–37.
13. Woldearegai TG, Kremsner PG, Kun JFJ, Mordmüller B, Plasmodium vivax malaria in Duffy-negative individuals from Ethiopia. T Roy Soc Trop Med H. 2013;107(5):328–331. doi: 10.1093/trstmh/trt016 23584375
14. Wurtz N, Mint Lekweiry K, Bogreau H, Pradines B, Rogier C, Ould Mohamed Salem Boukhary A, et al. Vivax malaria in Mauritania includes infection of a Duffy-negative individual. Malar J. 2011;10:336. doi: 10.1186/1475-2875-10-336 22050867
15. Cavasini CE, de Mattos LC, Couto AAD, Bonini-Domingos CR, Valencia SH, de Souza Neiras WC, et al. Plasmodium vivax infection among Duffy antigen-negative individuals from the Brazilian Amazon region: an exception?Trans R Soc Trop Med Hyg. 2007;101(10):1042–1044. doi: 10.1016/j.trstmh.2007.04.011 17604067
16. Ménard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA. 2010;107(13):5967–5971. doi: 10.1073/pnas.0912496107 20231434
17. Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, Koros J, et al. Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in Western Kenya. Am J Trop Med Hyg. 2006;75(4):575–581. 17038676
18. King CL, Adams JH, Xianli J, Grimberg BT, McHenry AM, Greenberg LJ, et al. Fya/Fyb antigen polymorphism in human erythrocyte Duffy antigen affects susceptibility to Plasmodium vivax malaria. Proc Natl Acad Sci USA. 2011;108(50):20113–20118. doi: 10.1073/pnas.1109621108 22123959
19. Chittoria A, Mohanty S, Jaiswal YK, Das A, Natural selection mediated association of the Duffy (FY) gene polymorphisms with Plasmodium vivax malaria in India. PloS one. 2012;7(9). doi: 10.1371/journal.pone.0045219 23028857
20. Carvalho TAA, Queiroz MG, Cardoso GL, Diniz IG, Silva ANLM, Pinto AYN, et al. Plasmodium vivax infection in Anajas, State of Para: no differential resistance profile among Duffy-negative and Duffy-positive individuals. Malar J. 2012;11:430. doi: 10.1186/1475-2875-11-430 23259672
21. Albuquerque SRL, Cavalcante FO, Sanguino EC, Tezza L, Chacon F, Castilho L, et al. FY polymorphisms and vivax malaria in inhabitants of Amazonas State, Brazil. Parasitol Res. 2010;106:1049–1053. doi: 10.1007/s00436-010-1745-x 20162434
22. Sabeti P, Schaffner S, Fry B, Lohmueller J, Varilly P, Shamovsky O, et al. Positive natural selection in the human lineage. Science. 2006;312(5780):1614–1620. doi: 10.1126/science.1124309 16778047
23. Vallender EJ, Lahn BT, Positive selection on the human genome. Hum Mol Gen. 2004;13(suppl 2):R245–R254. doi: 10.1093/hmg/ddh253 15358731
24. Wray GA, The evolutionary significance of cis-regulatory mutations. Nature Rev Genet. 2007;8(3):206–216. doi: 10.1038/nrg2063 17304246
25. Oleksyk TK, Smith MW, O’Brien SJ, Genome-wide scans for footprints of natural selection. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2010;365(1537):185–205. doi: 10.1098/rstb.2009.0219 20008396
26. Barreiro LB, Quintana-Murci L, From evolutionary genetics to human immunology: how selection shapes host defence genes. Nature Reviews Genetics. 2010;11(1):17–30. doi: 10.1038/nrg2698 19953080
27. Hamblin MT, Di Rienzo A, Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J of Hum Genet. 2000;66(5):1669–1679. doi: 10.1086/302879
28. Hamblin MT, Thompson EE, Di Rienzo A, Complex signatures of natural selection at the Duffy blood group locus. Am J of Hum Genet. 2002;70(2):369–383. doi: 10.1086/338628
29. Voight BF, Kudaravalli S, Wen X, Pritchard JK, A map of recent positive selection in the human genome. PLoS Biol. 2006;4(3):446. doi: 10.1371/journal.pbio.0040072
30. Sabeti PC, Varilly P, Fry B, Lohmueller J, Hostetter E, Cotsapas C, et al. Genome-wide detection and characterization of positive selection in human populations. Nature. 2007;449(7164):913–918. doi: 10.1038/nature06250 17943131
31. Akey JM, Constructing genomic maps of positive selection in humans: Where do we go from here?Genome Res. 2009;19(5):711–722. doi: 10.1101/gr.086652.108 19411596
32. Zhou H, Hu S, Matveev R, Yu Q, Li J, Khaitovich P, et al. A Chronological Atlas of Natural Selection in the Human Genome during the Past Half-million Years. bioRxiv. 2015;p. 018929.
33. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R, Localizing recent adaptive evolution in the human genome. PLoS Genet. 2007;3(6):e90. doi: 10.1371/journal.pgen.0030090 17542651
34. Wang ET, Kodama G, Baldi P, Moyzis RK, Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci USA. 2006;103(1):135–140. doi: 10.1073/pnas.0509691102 16371466
35. Tang K, Thornton KR, Stoneking M, A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol. 2007;5(7):e171. doi: 10.1371/journal.pbio.0050171 17579516
36. Kimura R, Fujimoto A, Tokunaga K, Ohashi J, A practical genome scan for population-specific strong selective sweeps that have reached fixation. PLoS one. 2007;2(3):e286–e286. doi: 10.1371/journal.pone.0000286 17356696
37. Kelley JL, Madeoy J, Calhoun JC, Swanson W, Akey JM, Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Res. 2006;16(8):980–989. doi: 10.1101/gr.5157306 16825663
38. Shortt H, Garnham P, Malamos B, Pre-erythrocytic stage of mammalian malaria. Br Med J. 1948;1(4543):192. doi: 10.1136/bmj.1.4543.192 18899048
39. Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, Halbwax M, et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 2010;6(2):e1000765. doi: 10.1371/journal.ppat.1000765 20169187
40. Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, et al. African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014;5.
41. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci USA. 2010;107(4):1458–1463. doi: 10.1073/pnas.0914440107 20133889
42. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, et al. A monkey’s tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci USA. 2005;102(6):1980–1985. doi: 10.1073/pnas.0409652102 15684081
43. Cornejo OE, Escalante AA, The origin and age of Plasmodium vivax. Trends Parasitol. 2006;22(12):558–563. doi: 10.1016/j.pt.2006.09.007 17035086
44. Wright GJ, Rayner JC, Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathog. 2014;10(3):e1003943. doi: 10.1371/journal.ppat.1003943 24651270
45. Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK, Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science. 1975;189(4202):561–563. doi: 10.1126/science.1145213 1145213
46. Tung J, Primus A, Bouley AJ, Severson TF, Alberts SC, Wray GA, Evolution of a malaria resistance gene in wild primates. Nature. 2009;460(7253):388–391. 19553936
47. Patin E, Laval G, Barreiro LB, Salas A, Semino O, Santachiara-Benerecetti S, et al. Inferring the demographic history of African farmers and pygmy hunter-gatherers using a multilocus resequencing data set. PLoS Genet. 2009;5(4):e1000448. doi: 10.1371/journal.pgen.1000448 19360089
48. Meyer M, Kircher M, Gansauge M, Li H, Racimo F, Mallick S, et al. A high-coverage genome sequence from an archaic Denisovan individual. Science. 2012;338(6104):222–226. doi: 10.1126/science.1224344 22936568
49. Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature. 2014;505(7481):43–49. doi: 10.1038/nature12886 24352235
50. Llorente MG, Jones E, Eriksson A, Siska V, Arthur K, Arthur J, et al. Ancient Ethiopian genome reveals extensive Eurasian admixture throughout the African continent. Science. 2015;p. aad2879. doi: 10.1126/science.aad2879
51. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM, Bondarev AA, et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature. 2014;514(7523):445–449. doi: 10.1038/nature13810 25341783
52. Pavlidis P, Živković D, Stamatakis A, Alachiotis N, SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol Biol Evol. 2013;30(9):2224–2234. doi: 10.1093/molbev/mst112 23777627
53. Nielsen R, Williamson S, Kim Y, Hubisz M, Clark A, Bustamante C, Genomic scans for selective sweeps using SNP data. Genome Res. 2005;15:1566–1575. doi: 10.1101/gr.4252305 16251466
54. Schlamp F, van der Made J, Stambler R, Chesebrough L, Boyko AR, Messer PW, Evaluating the performance of selection scans to detect selective sweeps in domestic dogs. Mol Ecol. 2016;25(1):342–356. doi: 10.1111/mec.13485 26589239
55. Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, et al. Detecting recent positive selection in the human genome from haplotype structure. Nature. 2002;419(6909):832–837. doi: 10.1038/nature01140 12397357
56. Allentoft ME, Sikora M, Sjögren K, Rasmussen S, Rasmussen M, Stenderup J, et al. Population genomics of Bronze Age Eurasia. Nature. 2015;522(7555):167–172. doi: 10.1038/nature14507 26062507
57. Hedrick PW, Population genetics of malaria resistance in humans. Heredity. 2011;107(4):283–304. doi: 10.1038/hdy.2011.16 21427751
58. Peter BM, Huerta-Sanchez E, Nielsen R, Distinguishing between selective sweeps from standing variation and from a de novo mutation. PLOS Genet. 2012;p. e1003011. doi: 10.1371/journal.pgen.1003011
59. Csillery K, Francois O, Blum MGB, abc: an R package for approximate Bayesian computation (ABC). Methods Ecol Evol. 2012;.
60. Beaumont MA, Zhang W, Balding DJ, Approximate Bayesian computation in population genetics. Genetics. 2002;162(4):2025–2035. 12524368
61. Pritchard JK, Seielstad MT, Perez-Lezaun A, Feldman MW, Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol. 1999;16(12):1791–1798. doi: 10.1093/oxfordjournals.molbev.a026091 10605120
62. Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, et al. Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA. 2011;108(29):11983–11988. doi: 10.1073/pnas.1019276108 21730125
63. Schlebusch CM, Skoglund P, Sjödin P, Gattepaille LM, Hernandez D, Jay F, et al. Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science. 2012;338(6105):374–379. doi: 10.1126/science.1227721 22997136
64. Gurdasani D, Carstensen T, Tekola-Ayele F, Pagani L, Tachmazidou I, Hatzikotoulas K, et al. The African Genome Variation Project shapes medical genetics in Africa. Nature. 2015;517(7534):327–332. doi: 10.1038/nature13997 25470054
65. Batini C, Lopes J, Behar DM, Calafell F, Jorde LB, Van der Veen L, et al. Insights into the demographic history of African Pygmies from complete mitochondrial genomes. Mol Biology Evol. 2011;28(2):1099–1110. doi: 10.1093/molbev/msq294
66. Veeramah KR, Wegmann D, Woerner A, Mendez FL, Watkins JC, Destro-Bisol G, et al. An early divergence of KhoeSan ancestors from those of other modern humans is supported by an ABC-based analysis of autosomal resequencing data. Mol Biol Evol. 2012;29(2):617–630. doi: 10.1093/molbev/msr212 21890477
67. Verdu P, Austerlitz F, Estoup A, Vitalis R, Georges M, Théry S, et al. Origins and genetic diversity of pygmy hunter-gatherers from Western Central Africa. Curr Biol. 2009;19(4):312–318. doi: 10.1016/j.cub.2008.12.049 19200724
68. Quintana-Murci L, Quach H, Harmant C, Luca F, Massonnet B, Patin E, et al. Maternal traces of deep common ancestry and asymmetric gene flow between Pygmy hunter–gatherers and Bantu-speaking farmers. Proc Natl Acad Sci USA. 2008;105(5):1596–1601. doi: 10.1073/pnas.0711467105 18216239
69. Patin E, Siddle KJ, Laval G, Quach H, Harmant C, Becker N, et al. The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists. Nat Commun. 2014;5. doi: 10.1038/ncomms4163 24495941
70. Loh PR, Lipson M, Patterson N, Moorjani P, Pickrell JK, Reich D, et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics. 2013;193(4):1233–1254. doi: 10.1534/genetics.112.147330 23410830
71. Gething PW, Van Boeckel TP, Smith DL, Guerra CA, Patil AP, Snow RW, et al. Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasit Vectors. 2011;4(92):4.
72. Prezeworski M, Coop G, Wall JD, The signature of positive selection on standing genetic variation. Evolution. 2005;59(11):2312–2323. doi: 10.1111/j.0014-3820.2005.tb00941.x
73. Seixas S, Ferrand N, Rocha J, Microsatellite variation and evolution of the human Duffy blood group polymorphism. Mol Biol Evol. 2002;19(10):1802–1806. doi: 10.1093/oxfordjournals.molbev.a004003 12270907
74. Hodgson JA, Pickrell JK, Pearson LN, Quillen EE, Prista A, Rocha J, et al. Natural selection for the Duffy-null allele in the recently admixed people of Madagascar. Proc R Soc B. 2014;281. doi: 10.1098/rspb.2014.0930
75. Schiffels S, Durbin R, Inferring human population size and separation history from multiple genome sequences. Nature genetics. 2014;. doi: 10.1038/ng.3015 24952747
76. Li H, Durbin R, Inference of human population history from individual whole-genome sequences. Nature. 2011;475(7357):493–496. doi: 10.1038/nature10231 21753753
77. McEvoy BP, Powell JE, Goddard ME, Visscher PM, Human population dispersal “Out of Africa” estimated from linkage disequilibrium and allele frequencies of SNPs. Genome research. 2011;21(6):821–829. doi: 10.1101/gr.119636.110 21518737
78. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, et al. Rate of de novo mutations and the importance of father/’s age to disease risk. Nature. 2012;488(7412):471–475. doi: 10.1038/nature11396 22914163
79. Campbell CD, Chong JX, Malig M, Ko A, Dumont BL, Han L, et al. Estimating the human mutation rate using autozygosity in a founder population. Nature genetics. 2012;44(11):1277–1281. doi: 10.1038/ng.2418 23001126
80. Ségurel L, Wyman MJ, Przeworski M, Determinants of mutation rate variation in the human germline. Annual review of genomics and human genetics. 2014;15:47–70. doi: 10.1146/annurev-genom-031714-125740 25000986
81. Michaelson JJ, Shi Y, Gujral M, Zheng H, Malhotra D, Jin X, et al. Whole-genome sequencing in autism identifies hot spots for de novo germline mutation. Cell. 2012;151(7):1431–1442. doi: 10.1016/j.cell.2012.11.019 23260136
82. O’Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, Coe BP, et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature. 2012;485(7397):246–250. doi: 10.1038/nature10989 22495309
83. Neale BM, Kou Y, Liu L, Ma’Ayan A, Samocha KE, Sabo A, et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature. 2012;485(7397):242–245. doi: 10.1038/nature11011 22495311
84. Sanders SJ, Murtha MT, Gupta AR, Murdoch JD, Raubeson MJ, Willsey AJ, et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature. 2012;485(7397):237–241. doi: 10.1038/nature10945 22495306
85. Lipson M, Loh P, Sankararaman S, Patterson N, Berger B, Reich D, Calibrating the Human Mutation Rate via Ancestral Recombination Density in Diploid Genomes. PLoS Genet;11(11):e1005550. doi: 10.1371/journal.pgen.1005550 26562831
86. Palamara PF, Francioli LC, Wilton PR, Genovese G, Gusev A, Finucane HK, et al. Leveraging Distant Relatedness to Quantify Human Mutation and Gene-Conversion Rates. The American Journal of Human Genetics. 2015;97(6):775–789. doi: 10.1016/j.ajhg.2015.10.006 26581902
87. Kimura M, Some problems of stochastic processes in genetics. Ann of Math Stat. 1957;p. 882–901. doi: 10.1214/aoms/1177706791
88. Kimura M, On the probability of fixation of mutant genes in a population. Genetics. 1962;47(6):713. 14456043
89. Mu J, Joy DA, Duan J, Huang Y, Carlton J, Walker J, et al. Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol. 2005;22(8):1686–1693. doi: 10.1093/molbev/msi160 15858201
90. Henn BM, Botigué LR, Peischl S, Dupanloup I, Lipatov M, Maples BK, et al. Distance from sub-Saharan Africa predicts mutational load in diverse human genomes. Proc Natl Acad Sci. 2105;.
91. Uren C, Kim M, Martin AR, Bobo D, Gignoux CR, van Helden PD, et al. Fine-scale human population structure in southern Africa reflects ecogeographic boundaries. Genetics. 2016;204(1):303–314. doi: 10.1534/genetics.116.187369 27474727
92. Consortium GP, et al. A global reference for human genetic variation. Nature. 2015;526(7571):68–74. doi: 10.1038/nature15393
93. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–2079. doi: 10.1093/bioinformatics/btp352 19505943
94. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–1303. doi: 10.1101/gr.107524.110 20644199
95. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet. 2011;43(5):491–498. doi: 10.1038/ng.806 21478889
96. Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, et al. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;p. 11–10. doi: 10.1002/0471250953.bi1110s43 25431634
97. Browning SR, Browning BL, Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007;81(5):1084–1097. doi: 10.1086/521987 17924348
98. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, et al. Ensembl 2015. Nucleic Acids Res. 2015;43(D1):D662–D669. doi: 10.1093/nar/gku1010 25352552
99. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, et al. Great ape genetic diversity and population history. Nature. 2013;499(7459):471–475. doi: 10.1038/nature12228 23823723
100. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, et al. Ensembl 2014. Nucleic Acids Res. 2013;p. gkt1196.
101. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012;6(2):80–92. doi: 10.4161/fly.19695 22728672
102. popArt;. http://popart.otago.ac.nz.
103. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–2158. doi: 10.1093/bioinformatics/btr330 21653522
104. Weir BS, Cockerham CC, Estimating F-statistics for the analysis of population structure. Evolution. 1984;p. 1358–1370. doi: 10.2307/2408641
105. Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A, et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature. 2010;467(7319):1099–1103. doi: 10.1038/nature09525 20981099
106. Gautier M, Vitalis R, rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics. 2012;28(8):1176–1177. doi: 10.1093/bioinformatics/bts115 22402612
107. Slatkin M, Hudson RR, Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics. 1991;129(2):555–562. 1743491
108. Ewing G, Hermisson J, MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics. 2010;26(16):2064–2065. doi: 10.1093/bioinformatics/btq322 20591904
109. Beaumont MA, Renfrew C, Matsumura S, Forster P, Joint determination of topology, divergence time, and immigration in population trees. Simulation, Genetics and Human Prehistory, McDonald Institute Monographs. 2008;p. 134–1541.
110. Fagundes NJR, Ray N, Beaumont M, Neuenschwander S, Salzano FM, Bonatto SL, et al. Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA. 2007;104(45):17614–17619. doi: 10.1073/pnas.0708280104 17978179
111. Garud NR, Messer PW, Buzbas EO, Petrov DA, Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps. PLoS Genet. 2015;11(2):e1005004. doi: 10.1371/journal.pgen.1005004 25706129
112. Cao KL, Gonzalez I, Dejean S. mixOmics: Omics Data Integration Project; 2015. R package version 5.0-4. Available from: http://CRAN.R-project.org/package=mixOmics.
113. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, et al. Worldwide human relationships inferred from genome-wide patterns of variation. science. 2008;319(5866):1100–1104. doi: 10.1126/science.1153717 18292342
114. Alexander DH, Novembre J, Lange K, Fast model-based estimation of ancestry in unrelated individuals. Genome research. 2009;19(9):1655–1664. doi: 10.1101/gr.094052.109 19648217
115. Maples BK, Gravel S, Kenny EE, Bustamante CD, RFMix: a discriminative modeling approach for rapid and robust local-ancestry inference. Am J Hum Genet. 2013;93(2):278–288. doi: 10.1016/j.ajhg.2013.06.020 23910464
116. O’Connell J, Gurdasani D, Delaneau O, Pirastu N, Ulivi S, Cocca M, et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 2014;10(4):e1004234. doi: 10.1371/journal.pgen.1004234 24743097
117. LTD FT. Network Publisher ver 2.0.0.1; 2013.