Distinct genetic variation and heterogeneity of the Iranian population
Autoři:
Zohreh Mehrjoo aff001; Zohreh Fattahi aff001; Maryam Beheshtian aff001; Marzieh Mohseni aff001; Hossein Poustchi aff002; Fariba Ardalani aff001; Khadijeh Jalalvand aff001; Sanaz Arzhangi aff001; Zahra Mohammadi aff002; Shahrouz Khoshbakht aff001; Farid Najafi aff003; Pooneh Nikuei aff004; Mohammad Haddadi aff005; Elham Zohrehvand aff001; Morteza Oladnabi aff006; Akbar Mohammadzadeh aff001; Mandana Hadi Jafari aff001; Tara Akhtarkhavari aff001; Ehsan Shamsi Gooshki aff008; Aliakbar Haghdoost aff010; Reza Najafipour aff012; Lisa-Marie Niestroj aff013; Barbara Helwing aff014; Yasmina Gossmann aff015; Mohammad Reza Toliat aff013; Reza Malekzadeh aff002; Peter Nürnberg aff013; Kimia Kahrizi aff001; Hossein Najmabadi aff001; Michael Nothnagel aff013
Působiště autorů:
Genetics Research Center, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran
aff001; Digestive Disease Research Centre, Digestive Disease Research Institute, Shariati Hospital, Tehran University of Medical Sciences, Tehran, Iran
aff002; Research Center for Environmental Determinants of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran
aff003; Molecular Medicine Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
aff004; Department of Biology, University of Zabol, Zabol, Iran
aff005; Congenital Malformations Research Center, Golestan University of Medical Sciences, Gorgan, Iran
aff006; Department of Medical Genetics, Faculty of Advanced Medical Technologies, School of Advanced Technologies in Medicine, Golestan University of Medical Sciences, Gorgan, Iran
aff007; Medical Ethics and History of Medicine Research Center, Tehran University of Medical Sciences, Tehran, Iran
aff008; Department of Medical Ethics, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, Iran
aff009; Modeling in Health Research Center, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Iran
aff010; Regional Knowledge Hub, and WHO Collaborating Centre for HIV Surveillance, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Iran
aff011; Cellular and Molecular Research Centre, Genetic Department, Qazvin University of Medical Sciences, Qazvin, Iran
aff012; Cologne Center for Genomics, University of Cologne, Cologne, Germany
aff013; Department of Archaeology, The University of Sydney, Australia
aff014; Noncommunicable Disease Research Center, Shiraz University of Medical Science, Shiraz, Iran
aff015; University Hospital Cologne, Cologne, Germany
aff016
Vyšlo v časopise:
Distinct genetic variation and heterogeneity of the Iranian population. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008385
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008385
Souhrn
Iran, despite its size, geographic location and past cultural influence, has largely been a blind spot for human population genetic studies. With only sparse genetic information on the Iranian population available, we pursued its genome-wide and geographic characterization based on 1021 samples from eleven ethnic groups. We show that Iranians, while close to neighboring populations, present distinct genetic variation consistent with long-standing genetic continuity, harbor high heterogeneity and different levels of consanguinity, fall apart into a cluster of similar groups and several admixed ones and have experienced numerous language adoption events in the past. Our findings render Iran an important source for human genetic variation in Western and Central Asia, will guide adequate study sampling and assist the interpretation of putative disease-implicated genetic variation. Given Iran’s internal genetic heterogeneity, future studies will have to consider ethnic affiliations and possible admixture.
Klíčová slova:
Arabic people – Asia – Language – Population genetics – Iran – Paleogenetics – Persian people – Ancient DNA
Zdroje
1. Gallego-Llorente M, Connell S, Jones ER, Merrett DC, Jeon Y, Eriksson A, et al. The genetics of an early Neolithic pastoralist from the Zagros, Iran. Sci Rep. 2016;6:31326. doi: 10.1038/srep31326 27502179
2. Lazaridis I, Nadel D, Rollefson G, Merrett DC, Rohland N, Mallick S, et al. Genomic insights into the origin of farming in the ancient Near East. Nature. 2016;536(7617):419–24. doi: 10.1038/nature19310 27459054
3. Rodriguez-Flores JL, Fakhro K, Agosto-Perez F, Ramstetter MD, Arbiza L, Vincent TL, et al. Indigenous Arabs are descendants of the earliest split from ancient Eurasian populations. Genome Res. 2016;26(2):151–62. doi: 10.1101/gr.191478.115 26728717
4. Grugni V, Battaglia V, Hooshiar Kashani B, Parolo S, Al-Zahery N, Achilli A, et al. Ancient migratory events in the Middle East: new clues from the Y-chromosome variation of modern Iranians. PLoS One. 2012;7(7):e41252. doi: 10.1371/journal.pone.0041252 22815981
5. Regueiro M, Cadenas AM, Gayden T, Underhill PA, Herrera RJ. Iran: tricontinental nexus for Y-chromosome driven migration. Hum Hered. 2006;61(3):132–43. doi: 10.1159/000093774 16770078
6. Broushaki F, Thomas MG, Link V, Lopez S, van Dorp L, Kirsanow K, et al. Early Neolithic genomes from the eastern Fertile Crescent. Science. 2016;353(6298):499–503. doi: 10.1126/science.aaf7943 27417496
7. Anthony DW, Ringe D. The Indo-European Homeland from Linguistic and Archaeological Perspectives. Annu Rev Linguist. 2015;1:199–219. doi: 10.1146/annurev-linguist-030514-124812
8. Curtis GE, Hooglund E. Iran: a country study. 5th ed. Washington, DC: Library of Congress. Federal Research Division; 2008.
9. Amanolahi S. A note on ethnicity and ethnic groups in Iran. Iran & the Caucasus. 2005;9(1):37–41.
10. Hassan HD. Iran: Ethnic and Religious Minorities. 2008.
11. Price M. Iran’s Diverse Peoples: a Reference Source Book. Santa Barbara, CA: ABC-CLIO; 2005.
12. Mostofi K, Afary J, others. Iran https://www.britannica.com/place/Iran/People: Encyclopædia Britannica, inc.; November 1, 2017 [Dezember 12, 2017].
13. Bittles AH, Black ML. Evolution in health and medicine Sackler colloquium: Consanguinity, human evolution, and complex diseases. Proc Natl Acad Sci U S A. 2010;107 Suppl 1:1779–86. doi: 10.1073/pnas.0906079106 19805052
14. Romeo G, Bittles AH. Consanguinity in the contemporary world. Hum Hered. 2014;77(1–4):6–9. doi: 10.1159/000363352 25060264
15. Borck G, Ur Rehman A, Lee K, Pogoda HM, Kakar N, von Ameln S, et al. Loss-of-function mutations of ILDR1 cause autosomal-recessive hearing impairment DFNB42. Am J Hum Genet. 2011;88(2):127–37. doi: 10.1016/j.ajhg.2010.12.011 21255762
16. Hu H, Wienker TF, Musante L, Kalscheuer VM, Kahrizi K, Najmabadi H, et al. Integrated sequence analysis pipeline provides one-stop solution for identifying disease-causing mutations. Hum Mutat. 2014;35(12):1427–35. doi: 10.1002/humu.22695 25219469
17. Kahrizi K, Hu CH, Garshasbi M, Abedini SS, Ghadami S, Kariminejad R, et al. Next generation sequencing in a family with autosomal recessive Kahrizi syndrome (OMIM 612713) reveals a homozygous frameshift mutation in SRD5A3. Eur J Hum Genet. 2011;19(1):115–7. doi: 10.1038/ejhg.2010.132 20700148
18. Kuss AW, Garshasbi M, Kahrizi K, Tzschach A, Behjati F, Darvish H, et al. Autosomal recessive mental retardation: homozygosity mapping identifies 27 single linkage intervals, at least 14 novel loci and several mutation hotspots. Hum Genet. 2011;129(2):141–8. doi: 10.1007/s00439-010-0907-3 21063731
19. Larti F, Kahrizi K, Musante L, Hu H, Papari E, Fattahi Z, et al. A defect in the CLIP1 gene (CLIP-170) can cause autosomal recessive intellectual disability. Eur J Hum Genet. 2015;23(3):331–6. doi: 10.1038/ejhg.2014.13 24569606
20. Mehrjoo Z, Babanejad M, Kahrizi K, Najmabadi H. Two novel mutations in ILDR1 gene cause autosomal recessive nonsyndromic hearing loss in consanguineous Iranian families. J Genet. 2015;94(3):483–7. 26440088
21. Najmabadi H, Hu H, Garshasbi M, Zemojtel T, Abedini SS, Chen W, et al. Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature. 2011;478(7367):57–63. doi: 10.1038/nature10423 21937992
22. Erzurumluoglu AM, Shihab HA, Rodriguez S, Gaunt TR, Day IN. Importance of genetic studies in consanguineous populations for the characterization of novel human gene functions. Ann Hum Genet. 2016;80(3):187–96. doi: 10.1111/ahg.12150 27000383
23. Alkuraya FS. Autozygome decoded. Genet Med. 2010;12(12):765–71. doi: 10.1097/GIM.0b013e3181fbfcc4 21189493
24. Alsalem AB, Halees AS, Anazi S, Alshamekh S, Alkuraya FS. Autozygome sequencing expands the horizon of human knockout research and provides novel insights into human phenotypic variation. PLoS Genet. 2013;9(12):e1004030. doi: 10.1371/journal.pgen.1004030 24367280
25. MacArthur DG, Balasubramanian S, Frankish A, Huang N, Morris J, Walter K, et al. A systematic survey of loss-of-function variants in human protein-coding genes. Science. 2012;335(6070):823–8. doi: 10.1126/science.1215040 22344438
26. Farhud DD, Mahmoudi M, Kamali MS, Marzban M, Andonian L, Saffari R. Consanguinity in Iran. Iranian J Publ Health. 1991;20(1–4):1–16.
27. Saadat M, Ansari-Lari M, Farhud DD. Consanguineous marriage in Iran. Ann Hum Biol. 2004;31(2):263–9. doi: 10.1080/03014460310001652211 15204368
28. Hosseini-Chavoshi M, Abbasi-Shavazi MJ, Bittles AH. Consanguineous marriage, reproductive behaviour and postnatal mortality in contemporary Iran. Hum Hered. 2014;77(1–4):16–25. doi: 10.1159/000358403 25060266
29. McQuillan R, Leutenegger AL, Abdel-Rahman R, Franklin CS, Pericic M, Barac-Lauc L, et al. Runs of homozygosity in European populations. Am J Hum Genet. 2008;83(3):359–72. doi: 10.1016/j.ajhg.2008.08.007 18760389
30. Nothnagel M, Lu TT, Kayser M, Krawczak M. Genomic and geographic distribution of SNP-defined runs of homozygosity in Europeans. Hum Mol Genet. 2010;19(15):2927–35. doi: 10.1093/hmg/ddq198 20462934
31. Pemberton TJ, Absher D, Feldman MW, Myers RM, Rosenberg NA, Li JZ. Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet. 2012;91(2):275–92. doi: 10.1016/j.ajhg.2012.06.014 22883143
32. Browning SR, Browning BL. Accurate non-parametric estimation of recent effective population size from segments of identity by descent. Am J Hum Genet. 2015;97(3):404–18. doi: 10.1016/j.ajhg.2015.07.012 26299365
33. Scott EM, Halees A, Itan Y, Spencer EG, He Y, Azab MA, et al. Characterization of Greater Middle Eastern genetic variation for enhanced disease gene discovery. Nat Genet. 2016;48(9):1071–6. doi: 10.1038/ng.3592 27428751
34. Yang X, Al-Bustan S, Feng Q, Guo W, Ma Z, Marafie M, et al. The influence of admixture and consanguinity on population genetic diversity in Middle East. J Hum Genet. 2014;59(11):615–22. doi: 10.1038/jhg.2014.81 25253659
35. Pemberton TJ, Rosenberg NA. Population-genetic influences on genomic estimates of the inbreeding coefficient: a global perspective. Hum Hered. 2014;77(1–4):37–48. doi: 10.1159/000362878 25060268
36. Najmabadi H, Nishimura C, Kahrizi K, Riazalhosseini Y, Malekpour M, Daneshi A, et al. GJB2 mutations: passage through Iran. Am J Med Genet A. 2005;133A(2):132–7. doi: 10.1002/ajmg.a.30576 15666300
37. Najmabadi H, Karimi-Nejad R, Sahebjam S, Pourfarzad F, Teimourian S, Sahebjam F, et al. The beta-thalassemia mutation spectrum in the Iranian population. Hemoglobin. 2001;25(3):285–96. doi: 10.1081/HEM-100105221 11570721
38. Shearer AE, Eppsteiner RW, Booth KT, Ephraim SS, Gurrola J 2nd, Simpson A, et al. Utilizing ethnic-specific differences in minor allele frequency to recategorize reported pathogenic deafness variants. Am J Hum Genet. 2014;95(4):445–53. doi: 10.1016/j.ajhg.2014.09.001 25262649
39. Ghasemi Firouzabadi S, Vameghi R, Kariminejad R, Darvish H, Banihashemi S, Firouzkouhi Moghaddam M, et al. Analysis of copy number variations in patients with autism using cytogenetic and MLPA techniques: report of 16p13.1p13.3 and 10q26.3 duplications. Int J Mol Cell Med. 2016;5(4):236–45. 28357200
40. Consortium HP-AS, Abdulla MA, Ahmed I, Assawamakin A, Bhak J, Brahmachari SK, et al. Mapping human genetic diversity in Asia. Science. 2009;326(5959):1541–5. doi: 10.1126/science.1177074 20007900
41. Genomes Project C, Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, et al. A map of human genome variation from population-scale sequencing. Nature. 2010;467(7319):1061–73. doi: 10.1038/nature09534 20981092
42. Genomes Project C, Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, et al. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491(7422):56–65. doi: 10.1038/nature11632 23128226
43. Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, et al. A global reference for human genetic variation. Nature. 2015;526(7571):68–74. doi: 10.1038/nature15393 26432245
44. Mallick S, Li H, Lipson M, Mathieson I, Gymrek M, Racimo F, et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature. 2016;538(7624):201–6. doi: 10.1038/nature18964 27654912
45. Metspalu M, Romero IG, Yunusbayev B, Chaubey G, Mallick CB, Hudjashov G, et al. Shared and unique components of human population structure and genome-wide signals of positive selection in South Asia. Am J Hum Genet. 2011;89(6):731–44. doi: 10.1016/j.ajhg.2011.11.010 22152676
46. Pagani L, Lawson DJ, Jagoda E, Morseburg A, Eriksson A, Mitt M, et al. Genomic analyses inform on migration events during the peopling of Eurasia. Nature. 2016;538(7624):238–42. doi: 10.1038/nature19792 27654910
47. Platt DE, Haber M, Dagher-Kharrat MB, Douaihy B, Khazen G, Ashrafian Bonab M, et al. Mapping post-glacial expansions: the peopling of Southwest Asia. Sci Rep. 2017;7:40338. doi: 10.1038/srep40338 28059138
48. Yunusbayev B, Metspalu M, Jarve M, Kutuev I, Rootsi S, Metspalu E, et al. The Caucasus as an asymmetric semipermeable barrier to ancient human migrations. Mol Biol Evol. 2012;29(1):359–65. doi: 10.1093/molbev/msr221 21917723
49. Haber M, Mezzavilla M, Xue Y, Comas D, Gasparini P, Zalloua P, et al. Genetic evidence for an origin of the Armenians from Bronze Age mixing of multiple populations. Eur J Hum Genet. 2016;24(6):931–6. doi: 10.1038/ejhg.2015.206 26486470
50. Behar DM, Yunusbayev B, Metspalu M, Metspalu E, Rosset S, Parik J, et al. The genome-wide structure of the Jewish people. Nature. 2010;466(7303):238–42. doi: 10.1038/nature09103 20531471
51. Elhaik E, Tatarinova T, Chebotarev D, Piras IS, Maria Calo C, De Montis A, et al. Geographic population structure analysis of worldwide human populations infers their biogeographical origins. Nat Commun. 2014;5:3513. doi: 10.1038/ncomms4513 24781250
52. Haber M, Doumet-Serhal C, Scheib C, Xue Y, Danecek P, Mezzavilla M, et al. Continuity and admixture in the last five millennia of Levantine history from ancient Canaanite and present-day Lebanese genome sequences. Am J Hum Genet. 2017;101(2):274–82. doi: 10.1016/j.ajhg.2017.06.013 28757201
53. Walter H, Farhud DD, Danker-Hopfe H, Amirshahi P. Investigations on the ethnic variability of the ABO blood group polymorphism in Iran. Z Morphol Anthropol. 1991;78(3):289–306. 1887659
54. Papiha SS, Amirshahi P, Sunderland E, Farhud DD, Tavakoli SH, Daneshmand P. Population genetics of the people of Iran II. Genetic differentiation and population structure. Intl Jnl Anthropology. 1992;7(3):11–8. doi: 10.1007/bf02447605
55. Derenko M, Malyarchuk B, Bahmanimehr A, Denisova G, Perkova M, Farjadian S, et al. Complete mitochondrial DNA diversity in Iranians. PLoS One. 2013;8(11):e80673. doi: 10.1371/journal.pone.0080673 24244704
56. Zarei F, Rajabi-Maham H. Phylogeography, genetic diversity and demographic history of the Iranian Kurdish groups based on mtDNA sequences. J Genet. 2016;95(4):767–76. 27994175
57. Terreros MC, Rowold DJ, Mirabal S, Herrera RJ. Mitochondrial DNA and Y-chromosomal stratification in Iran: relationship between Iran and the Arabian Peninsula. J Hum Genet. 2011;56(3):235–46. doi: 10.1038/jhg.2010.174 21326310
58. Nasidze I, Quinque D, Rahmani M, Alemohamad SA, Stoneking M. Close genetic relationship between Semitic-speaking and Indo-European-speaking groups in Iran. Ann Hum Genet. 2008;72(Pt 2):241–52. doi: 10.1111/j.1469-1809.2007.00413.x 18205892
59. Malyarchuk B, Derenko M, Wozniak M, Grzybowski T. Y-chromosome variation in Tajiks and Iranians. Ann Hum Biol. 2013;40(1):48–54. doi: 10.3109/03014460.2012.747628 23198991
60. Lashgary Z, Khodadadi A, Singh Y, Houshmand SM, Mahjoubi F, Sharma P, et al. Y chromosome diversity among the Iranian religious groups: a reservoir of genetic variation. Ann Hum Biol. 2011;38(3):364–71. doi: 10.3109/03014460.2010.535562 21329477
61. Di Cristofaro J, Pennarun E, Mazieres S, Myres NM, Lin AA, Temori SA, et al. Afghan Hindu Kush: where Eurasian sub-continent gene flows converge. PLoS One. 2013;8(10):e76748. doi: 10.1371/journal.pone.0076748 24204668
62. Omberg L, Salit J, Hackett N, Fuller J, Matthew R, Chouchane L, et al. Inferring genome-wide patterns of admixture in Qataris using fifty-five ancestral populations. BMC Genet. 2012;13:49. doi: 10.1186/1471-2156-13-49 22734698
63. Hunter-Zinck H, Musharoff S, Salit J, Al-Ali KA, Chouchane L, Gohar A, et al. Population genetic structure of the people of Qatar. Am J Hum Genet. 2010;87(1):17–25. doi: 10.1016/j.ajhg.2010.05.018 20579625
64. Chaubey G, Ayub Q, Rai N, Prakash S, Mushrif-Tripathy V, Mezzavilla M, et al. "Like sugar in milk": reconstructing the genetic history of the Parsi population. Genome Biol. 2017;18(1):110. doi: 10.1186/s13059-017-1244-9 28615043
65. Lopez S, Thomas MG, van Dorp L, Ansari-Pour N, Stewart S, Jones AL, et al. The genetic legacy of Zoroastrianism in Iran and India: insights into population structure, gene flow, and selection. Am J Hum Genet. 2017; 101(3):353–368. doi: 10.1016/j.ajhg.2017.07.013 28844488
66. Ayub Q, Mezzavilla M, Pagani L, Haber M, Mohyuddin A, Khaliq S, et al. The Kalash genetic isolate: ancient divergence, drift, and selection. Am J Hum Genet. 2015;96(5):775–83. doi: 10.1016/j.ajhg.2015.03.012 25937445
67. Cavalli-Sforza LL. Genes, peoples, and languages. Proc Natl Acad Sci U S A. 1997;94(15):7719–24. Epub 1997/07/22. doi: 10.1073/pnas.94.15.7719 9223254
68. Jobling MA, Hurles ME, Tyler-Smith C. Human Evolutionary Genetics: Origins, Peoples and Disease. 1st ed: Garland Publishing; 2004.
69. Comas D, Bosch E, Calafell F. Human genetics and languages. Chichester: Wiley; 2008.
70. Campbell L. Do languages and genes correlate? Some methodological issues. Language Dynamics and Change. 2015;5:202–26.
71. Kayser M, Lao O, Anslinger K, Augustin C, Bargel G, Edelmann J, et al. Significant genetic differentiation between Poland and Germany follows present-day political borders, as revealed by Y-chromosome analysis. Hum Genet. 2005;117(5):428–43. doi: 10.1007/s00439-005-1333-9 15959808
72. Lahermo P, Sajantila A, Sistonen P, Lukka M, Aula P, Peltonen L, et al. The genetic relationship between the Finns and the Finnish Saami (Lapps): analysis of nuclear DNA and mtDNA. Am J Hum Genet. 1996;58(6):1309–22. Epub 1996/06/01. 8651309
73. Lao O, Lu TT, Nothnagel M, Junge O, Freitag-Wolf S, Caliebe A, et al. Correlation between genetic and geographic structure in Europe. Curr Biol. 2008;18(16):1241–8. doi: 10.1016/j.cub.2008.07.049 18691889
74. Perez-Lezaun A, Calafell F, Comas D, Mateu E, Bosch E, Martinez-Arias R, et al. Sex-specific migration patterns in Central Asian populations, revealed by analysis of Y-chromosome short tandem repeats and mtDNA. Am J Hum Genet. 1999;65(1):208–19. Epub 1999/06/12. doi: 10.1086/302451 10364534
75. Ploski R, Wozniak M, Pawlowski R, Monies DM, Branicki W, Kupiec T, et al. Homogeneity and distinctiveness of Polish paternal lineages revealed by Y chromosome microsatellite haplotype analysis. Hum Genet. 2002;110(6):592–600. Epub 2002/07/11. doi: 10.1007/s00439-002-0728-0 12107446
76. Poloni ES, Semino O, Passarino G, Santachiara-Benerecetti AS, Dupanloup I, Langaney A, et al. Human genetic affinities for Y-chromosome P49a,f/TaqI haplotypes show strong correspondence with linguistics. Am J Hum Genet. 1997;61(5):1015–35. Epub 1997/11/01. doi: 10.1086/301602 9346874
77. Roewer L, Croucher PJ, Willuweit S, Lu TT, Kayser M, Lessig R, et al. Signature of recent historical events in the European Y-chromosomal STR haplotype distribution. Hum Genet. 2005;116(4):279–91. doi: 10.1007/s00439-004-1201-z 15660227
78. Kalaydjieva L, Calafell F, Jobling MA, Angelicheva D, de Knijff P, Rosser ZH, et al. Patterns of inter- and intra-group genetic diversity in the Vlax Roma as revealed by Y chromosome and mitochondrial DNA lineages. Eur J Hum Genet. 2001;9(2):97–104. Epub 2001/04/21. doi: 10.1038/sj.ejhg.5200597 11313742
79. Larmuseau MH, Vanoverbeke J, Gielis G, Vanderheyden N, Larmuseau HF, Decorte R. In the name of the migrant father-Analysis of surname origins identifies genetic admixture events undetectable from genealogical records. Heredity (Edinb). 2012;109(2):90–5. Epub 2012/04/19. doi: 10.1038/hdy.2012.17 22511074
80. Rodig H, Roewer L, Gross A, Richter T, de Knijff P, Kayser M, et al. Evaluation of haplotype discrimination capacity of 35 Y-chromosomal short tandem repeat loci. Forensic Sci Int. 2008;174(2–3):182–8. Epub 2007/06/05. doi: 10.1016/j.forsciint.2007.04.223 17543484
81. Haak W, Lazaridis I, Patterson N, Rohland N, Mallick S, Llamas B, et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature. 2015;522(7555):207–11. doi: 10.1038/nature14317 25731166
82. El-Sibai M, Platt DE, Haber M, Xue Y, Youhanna SC, Wells RS, et al. Geographical structure of the Y-chromosomal genetic landscape of the Levant: a coastal-inland contrast. Ann Hum Genet. 2009;73(Pt 6):568–81. Epub 2009/08/19. doi: 10.1111/j.1469-1809.2009.00538.x 19686289
83. Haber M, Platt DE, Badro DA, Xue Y, El-Sibai M, Bonab MA, et al. Influences of history, geography, and religion on genetic structure: the Maronites in Lebanon. Eur J Hum Genet. 2011;19(3):334–40. Epub 2010/12/02. doi: 10.1038/ejhg.2010.177 21119711
84. Jin HJ, Tyler-Smith C, Kim W. The peopling of Korea revealed by analyses of mitochondrial DNA and Y-chromosomal markers. PLoS One. 2009;4(1):e4210. Epub 2009/01/17. doi: 10.1371/journal.pone.0004210 19148289
85. Xue Y, Zerjal T, Bao W, Zhu S, Shu Q, Xu J, et al. Male demography in East Asia: a north-south contrast in human population expansion times. Genetics. 2006;172(4):2431–9. Epub 2006/02/21. doi: 10.1534/genetics.105.054270 16489223
86. Kayser M, Krawczak M, Excoffier L, Dieltjes P, Corach D, Pascali V, et al. An extensive analysis of Y-chromosomal microsatellite haplotypes in globally dispersed human populations. Am J Hum Genet. 2001;68(4):990–1018. Epub 2001/03/20. doi: 10.1086/319510 11254455
87. Shi W, Ayub Q, Vermeulen M, Shao RG, Zuniga S, van der Gaag K, et al. A worldwide survey of human male demographic history based on Y-SNP and Y-STR data from the HGDP-CEPH populations. Mol Biol Evol. 2010;27(2):385–93. Epub 2009/10/14. doi: 10.1093/molbev/msp243 19822636
88. Roewer L, Nothnagel M, Gusmao L, Gomes V, Gonzalez M, Corach D, et al. Continent-wide decoupling of Y-chromosomal genetic variation from language and geography in native South Americans. PLoS Genet. 2013;9(4):e1003460. doi: 10.1371/journal.pgen.1003460 23593040
89. Bosch E, Calafell F, Gonzalez-Neira A, Flaiz C, Mateu E, Scheil HG, et al. Paternal and maternal lineages in the Balkans show a homogeneous landscape over linguistic barriers, except for the isolated Aromuns. Ann Hum Genet. 2006;70(Pt 4):459–87. Epub 2006/06/09. doi: 10.1111/j.1469-1809.2005.00251.x 16759179
90. Hurles ME, Veitia R, Arroyo E, Armenteros M, Bertranpetit J, Perez-Lezaun A, et al. Recent male-mediated gene flow over a linguistic barrier in Iberia, suggested by analysis of a Y-chromosomal DNA polymorphism. Am J Hum Genet. 1999;65(5):1437–48. Epub 1999/10/16. doi: 10.1086/302617 10521311
91. Nasidze I, Sarkisian T, Kerimov A, Stoneking M. Testing hypotheses of language replacement in the Caucasus: evidence from the Y-chromosome. Hum Genet. 2003;112(3):255–61. doi: 10.1007/s00439-002-0874-4 12596050
92. Allentoft ME, Sikora M, Sjogren KG, Rasmussen S, Rasmussen M, Stenderup J, et al. Population genomics of Bronze Age Eurasia. Nature. 2015;522(7555):167–72. doi: 10.1038/nature14507 26062507
93. Cassidy LM, Martiniano R, Murphy EM, Teasdale MD, Mallory J, Hartwell B, et al. Neolithic and Bronze Age migration to Ireland and establishment of the insular Atlantic genome. Proc Natl Acad Sci U S A. 2016;113(2):368–73. doi: 10.1073/pnas.1518445113 26712024
94. 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):445–9. doi: 10.1038/nature13810 25341783
95. Fu Q, Posth C, Hajdinjak M, Petr M, Mallick S, Fernandes D, et al. The genetic history of Ice Age Europe. Nature. 2016;534(7606):200–5. doi: 10.1038/nature17993 27135931
96. Gallego Llorente M, Jones ER, Eriksson A, Siska V, Arthur KW, Arthur JW, et al. Ancient Ethiopian genome reveals extensive Eurasian admixture throughout the African continent. Science. 2015;350(6262):820–2. doi: 10.1126/science.aad2879 26449472
97. Gunther T, Valdiosera C, Malmstrom H, Urena I, Rodriguez-Varela R, Sverrisdottir OO, et al. Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques. Proc Natl Acad Sci U S A. 2015;112(38):11917–22. doi: 10.1073/pnas.1509851112 26351665
98. Hofmanova Z, Kreutzer S, Hellenthal G, Sell C, Diekmann Y, Diez-Del-Molino D, et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc Natl Acad Sci U S A. 2016;113(25):6886–91. doi: 10.1073/pnas.1523951113 27274049
99. Jones ER, Gonzalez-Fortes G, Connell S, Siska V, Eriksson A, Martiniano R, et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat Commun. 2015;6:8912. doi: 10.1038/ncomms9912 26567969
100. Keller A, Graefen A, Ball M, Matzas M, Boisguerin V, Maixner F, et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat Commun. 2012;3:698. doi: 10.1038/ncomms1701 22426219
101. Kilinc GM, Omrak A, Ozer F, Gunther T, Buyukkarakaya AM, Bicakci E, et al. The Demographic Development of the First Farmers in Anatolia. Curr Biol. 2016;26(19):2659–66. doi: 10.1016/j.cub.2016.07.057 27498567
102. Lazaridis I, Mittnik A, Patterson N, Mallick S, Rohland N, Pfrengle S, et al. Genetic origins of the Minoans and Mycenaeans. Nature. 2017;548(7666):214–8. doi: 10.1038/nature23310 28783727
103. Lazaridis I, Patterson N, Mittnik A, Renaud G, Mallick S, Kirsanow K, et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature. 2014;513(7518):409–13. doi: 10.1038/nature13673 25230663
104. Lipson M, Szecsenyi-Nagy A, Mallick S, Posa A, Stegmar B, Keerl V, et al. Parallel palaeogenomic transects reveal complex genetic history of early European farmers. Nature. 2017;551(7680):368–72. doi: 10.1038/nature24476 29144465
105. Mathieson I, Alpaslan-Roodenberg S, Posth C, Szecsenyi-Nagy A, Rohland N, Mallick S, et al. The genomic history of southeastern Europe. Nature. 2018;555(7695):197–203. doi: 10.1038/nature25778 29466330
106. Mathieson I, Lazaridis I, Rohland N, Mallick S, Patterson N, Roodenberg SA, et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature. 2015;528(7583):499–503. doi: 10.1038/nature16152 26595274
107. Narasimhan VM, Patterson NJ, Moorjani P, Lazaridis I, Mark L, Mallick S, et al. The genomic formation of South and Central Asia. bioRxiv. 2018. doi: 10.1101/292581
108. Olalde I, Brace S, Allentoft ME, Armit I, Kristiansen K, Booth T, et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature. 2018;555(7695):190–6. doi: 10.1038/nature25738 29466337
109. Olalde I, Schroeder H, Sandoval-Velasco M, Vinner L, Lobon I, Ramirez O, et al. A common genetic origin for early farmers from Mediterranean Cardial and Central European LBK cultures. Mol Biol Evol. 2015;32(12):3132–42. doi: 10.1093/molbev/msv181 26337550
110. Raghavan M, Skoglund P, Graf KE, Metspalu M, Albrechtsen A, Moltke I, et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature. 2014;505(7481):87–91. doi: 10.1038/nature12736 24256729
111. Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655–64. doi: 10.1101/gr.094052.109 19648217
112. Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;8(11):e1002967. doi: 10.1371/journal.pgen.1002967 23166502
113. Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N, Zhan Y, et al. Ancient admixture in human history. Genetics. 2012;192(3):1065–93. doi: 10.1534/genetics.112.145037 22960212
114. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 2007;39(1):31–40. doi: 10.1038/ng1946 17159977
115. Voight BF, Kudaravalli S, Wen X, Pritchard JK. A map of recent positive selection in the human genome. PLoS Biol. 2006;4(3):e72. doi: 10.1371/journal.pbio.0040072 16494531
116. Stelzer G, Rosen N, Plaschkes I, Zimmerman S, Twik M, Fishilevich S, et al. The GeneCards suite: from gene data mining to disease genome sequence analyses. Curr Protoc Bioinformatics. 2016;54:1 30 1–1 3. doi: 10.1002/cpbi.5 27322403
117. Steffens M, Lamina C, Illig T, Bettecken T, Vogler R, Entz P, et al. SNP-based analysis of genetic substructure in the German population. Hum Hered. 2006;62(1):20–9. doi: 10.1159/000095850 17003564
118. Nasidze I, Risch GM, Robichaux M, Sherry ST, Batzer MA, Stoneking M. Alu insertion polymorphisms and the genetic structure of human populations from the Caucasus. Eur J Hum Genet. 2001;9(4):267–72. doi: 10.1038/sj.ejhg.5200615 11313770
119. Novembre J, Johnson T, Bryc K, Kutalik Z, Boyko AR, Auton A, et al. Genes mirror geography within Europe. Nature. 2008;456(7218):98–101. Epub 2008/09/02. doi: 10.1038/nature07331 18758442
120. Cuyler Young T Jr. The Iranian Migration into the Zagros. Iran. 1967;5:11–34.
121. Nasidze I, Stoneking M. Mitochondrial DNA variation and language replacements in the Caucasus. Proc Biol Sci. 2001;268(1472):1197–206. doi: 10.1098/rspb.2001.1610 11375109
122. Stoneking M. An Introduction to Molecular Anthropology: Wiley-Blackwell; 2016.
123. Yunusbayev B, Metspalu M, Metspalu E, Valeev A, Litvinov S, Valiev R, et al. The genetic legacy of the expansion of Turkic-speaking nomads across Eurasia. PLoS Genet. 2015;11(4):e1005068. doi: 10.1371/journal.pgen.1005068 25898006
124. Akbari MR, Fattahi Z, Beheshtian M, Mohseni M, Poustchi H, Sellars E, et al. Iranome: A human genome variation database of eight major ethnic groups that live in Iran and neighboring countries in the Middle East. ASHG Annual Meeting; Orlando, FL, USA2017.
125. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215. doi: 10.1093/nar/16.3.1215 3344216
126. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4:7. doi: 10.1186/s13742-015-0047-8 25722852
127. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2018.
128. Wang C, Zhan X, Liang L, Abecasis GR, Lin X. Improved ancestry estimation for both genotyping and sequencing data using projection procrustes analysis and genotype imputation. Am J Hum Genet. 2015;96(6):926–37. doi: 10.1016/j.ajhg.2015.04.018 26027497
129. Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38(6):1358–70. doi: 10.1111/j.1558-5646.1984.tb05657.x 28563791
130. Devlin B, Roeder K, Wasserman L. Genomic control, a new approach to genetic-based association studies. Theor Popul Biol. 2001;60(3):155–66. doi: 10.1006/tpbi.2001.1542 11855950
131. Milanesi M, Capomaccio S, Vajana E, Bomba L, Garcia JF, Ajmone-Marsan P, et al. BITE: an R package for biodiversity analyses. bioRxiv. 2017. https://doi.org/10.1101/181610
132. Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author Department of Genome Sciences, University of Washington, Seattle. 2005.
133. Moran PA. Notes on continuous stochastic phenomena. Biometrika. 1950;37(1–2):17–23. 15420245
134. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20(2):289–90. doi: 10.1093/bioinformatics/btg412 14734327
135. Delaneau O, Zagury JF, Marchini J. Improved whole-chromosome phasing for disease and population genetic studies. Nat Methods. 2013;10(1):5–6. doi: 10.1038/nmeth.2307 23269371
136. Gautier M, Naves M. Footprints of selection in the ancestral admixture of a New World Creole cattle breed. Mol Ecol. 2011;20(15):3128–43. doi: 10.1111/j.1365-294X.2011.05163.x 21689193
137. Gautier M, Klassmann A, Vitalis R. rehh 2.0: a reimplementation of the R package rehh to detect positive selection from haplotype structure. Mol Ecol Resour. 2017;17(1):78–90. doi: 10.1111/1755-0998.12634 27863062
138. Yang J, Lee SH, Goddard ME, Visscher PM. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011;88(1):76–82. doi: 10.1016/j.ajhg.2010.11.011 21167468
139. Szpiech ZA, Blant A, Pemberton TJ. GARLIC: Genomic Autozygosity Regions Likelihood-based Inference and Classification. Bioinformatics. 2017. doi: 10.1093/bioinformatics/btx102 28205676
140. Duong T. ks: Kernel Smoothing. R package version 1.10.4 ed2018.
141. Pebesma EJ, Bivand RS. Classes and methods for spatial data in R. R News. 2005;5(2).
142. Bivand RS, Pebesma E, Gomez-Rubio V. Applied spatial data analysis with R. Second Edition ed. New York: Springer; 2013.
143. Wickham H. ggplot2: Elegant Graphics for Data Analysis. New York: Springer; 2009.
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 9
- Primární hyperoxalurie – aktuální možnosti diagnostiky a léčby
- Srdeční frekvence embrya může být faktorem užitečným v předpovídání výsledku IVF
- Akutní intermitentní porfyrie
- Vztah užívání alkoholu a mužské fertility
- Šanci na úspěšný průběh těhotenství snižují nevhodné hladiny progesteronu vznikající při umělém oplodnění
Nejčtenější v tomto čísle
- Origins of DNA replication
- Environmental and epigenetic regulation of Rider retrotransposons in tomato
- Integrating transcriptomic network reconstruction and eQTL analyses reveals mechanistic connections between genomic architecture and Brassica rapa development
- Temperature preference can bias parental genome retention during hybrid evolution