Article

Mitochondrial genomes uncover the maternal history of the Pamir populations

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Abstract

The Pamirs, among the world’s highest mountains in Central Asia, are one of homelands with the most extreme high altitude for several ethnic groups. The settlement history of modern humans on the Pamirs remains still opaque. Herein, we have sequenced the mitochondrial DNA (mtDNA) genomes of 382 individuals belonging to eight populations from the Pamirs and the surrounding lowlands in Central Asia. We construct the Central Asian (including both highlanders and lowlanders) mtDNA haplogroup tree at the highest resolution. All the matrilineal components are assigned into the defined mtDNA haplogroups in East and West Eurasians. No basal lineages that directly emanate from the Eurasian founder macrohaplogroups M, N, and R are found. Our data support the origin of Central Asian being the result of East–West Eurasian admixture. The coalescence ages for more than 93% mtDNA lineages in Central Asians are dated after the last glacial maximum (LGM). The post-LGM and/or later dispersals/admixtures play dominant roles in shaping the maternal gene pool of Central Asians. More importantly, our analyses reveal the mtDNA heterogeneity in the Pamir highlanders, not only between the Turkic Kyrgyz and the Indo-European Tajik groups, but also among three highland Tajiks. No evidence supports positive selection or relaxation of selective constraints in the mtDNAs of highlanders as compared to that of lowlanders. Our results suggest a complex history for the peopling of Pamirs by multiple waves of migrations from various genetic resources during different time scales.

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References

  1. 1.

    Simonson TS. Altitude adaptation: a glimpse through various lenses. High Alt Med Biol. 2015;16:125–37.

  2. 2.

    Keay J. When men and mountains meet: the explorers of the Western Himalayas 1820–1875. 1st ed. Karachi: Oxford University Press; 1994.

  3. 3.

    Aldashev A, Naeije R, (eds). Problems of high altitude medicine and biology. Dordrecht: Springer; 2007.

  4. 4.

    Liu M. Migration and adaptation: the ethnography of the Tajik in the Pamirs. Beijing: Social Sciences Academic Press; 2014.

  5. 5.

    Dani AH, Masson VM. History of civilizations of Central Asia: development in contrast: from the sixteenth to the mid-nineteenth century. UNESCO; 2003.

  6. 6.

    Baumer C. The history of Central Asia: the age of the Steppe Warriors. I.B. Tauris; 2012.

  7. 7.

    Kuzʹmina EE, Mallory JP. The origin of the Indo-Iranians. Brill; 2007.

  8. 8.

    Han K. The racial anthropological study of the ancient Xinjiang inhabitants. Urumqi: Xinjiang People’s Publishing House; 1994.

  9. 9.

    Comas D, Calafell F, Mateu E, et al. Trading genes along the silk road: mtDNA sequences and the origin of central Asian populations. Am J Hum Genet. 1998;63:1824–38.

  10. 10.

    Comas D, Plaza S, Wells RS, et al. Admixture, migrations, and dispersals in Central Asia: evidence from maternal DNA lineages. Eur J Hum Genet. 2004;12:495–504.

  11. 11.

    Heyer E, Balaresque P, Jobling MA, et al. Genetic diversity and the emergence of ethnic groups in Central Asia. BMC Genet. 2009;10:49.

  12. 12.

    Ricaut FX, Keyser-Tracqui C, Cammaert L, Crubézy E, Ludes B. Genetic analysis and ethnic affinities from two Scytho-Siberian skeletons. Am J Phys Anthropol 2004;123:351–60.

  13. 13.

    Li C, Li H, Cui Y, et al. Evidence that a West-East admixed population lived in the Tarim Basin as early as the early Bronze Age. BMC Biol 2010;8:15.

  14. 14.

    Ovchinnikov IV, Malek MJ, Drees K, Kholina OI. Mitochondrial DNA variation in Tajiks living in Tajikistan. Leg Med. 2014;16:390–95.

  15. 15.

    Duggan AT, Stoneking M. A highly unstable recent mutation in human mtDNA. Am J Hum Genet. 2013;92:279–84.

  16. 16.

    Ning C, Gao S, Deng B, et al. Ancient mitochondrial genome reveals trace of prehistoric migration in the east Pamir by pastoralists. J Hum Genet. 2016;61:103–8.

  17. 17.

    Schönberg A, Theunert C, Li M, Stoneking M, Nasidze I. High-throughput sequencing of complete human mtDNA genomes from the Caucasus and West Asia: high diversity and demographic inferences. Eur J Hum Genet. 2011;19:988–94.

  18. 18.

    Derenko M, Malyarchuk B, Bahmanimehr A, et al. Complete mitochondrial DNA diversity in Iranians. PLoS ONE. 2013;8:e80673.

  19. 19.

    Fendt L, Zimmermann B, Daniaux M, Parson W. Sequencing strategy for the whole mitochondrial genome resulting in high quality sequences. BMC Genomics. 2009;10:139.

  20. 20.

    Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet. 1999;23:147–47.

  21. 21.

    Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178–92.

  22. 22.

    Weissensteiner H, Pacher D, Kloss-Brandstätter A, et al. HaploGrep 2: mitochondrial haplogroup classification in the era of high-throughput sequencing. Nucleic Acids Res. 2016;44:W58–63.

  23. 23.

    Fan L, Yao YG. An update to MitoTool: using a new scoring system for faster mtDNA haplogroup determination. Mitochondrion. 2013;13:360–63.

  24. 24.

    van Oven M, Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum Mutat. 2009;30:E386–94.

  25. 25.

    Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–67.

  26. 26.

    Liu J, Wang LD, Sun YB, et al. Deciphering the signature of selective constraints on cancerous mitochondrial genome. Mol Biol Evol. 2012;29:1255–61.

  27. 27.

    Forster P, Harding R, Torroni A, Bandelt HJ. Origin and evolution of native American mtDNA variation: a reappraisal. Am J Hum Genet. 1996;59:935–45.

  28. 28.

    Saillard J, Forster P, Lynnerup N, Bandelt HJ, Norby S. mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am J Hum Genet. 2000;67:718–26.

  29. 29.

    Perego UA, Achilli A, Angerhofer N, et al. Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Curr Biol. 2009;19:1–8.

  30. 30.

    Soares P, Ermini L, Thomson N, et al. Correcting for purifying selection: an improved human mitochondrial molecular clock. Am J Hum Genet. 2009;84:740–59.

  31. 31.

    Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73.

  32. 32.

    Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772.

  33. 33.

    Cornuet JM, Pudlo P, Veyssier J, et al. DIYABCv2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics. 2014;30:1187–89.

  34. 34.

    Seo SB, Zeng X, King JL, et al. Underlying data for sequencing the mitochondrial genome with the massively parallel sequencing platform Ion Torrent PGM. BMC Genomics. 2015;16:S4.

  35. 35.

    Avise JC. Phylogeography: the history and formation of species.. Cambridge: Harvard University Press; 2000.

  36. 36.

    Atkinson QD, Gray RD, Drummond AJ. mtDNA variation predicts population size in humans and reveals a major southern Asian chapter in human prehistory. Mol Biol Evol. 2008;25:468–74.

  37. 37.

    Clark PU, Dyke AS, Shakun JD, et al. The last glacial maximum. Science. 2009;325:710–14.

  38. 38.

    Heller R, Chikhi L, Siegismund HR. The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE. 2013;8:e62992.

  39. 39.

    Glantz MM. The history of hominin occupation of central Asia in review. In: Norton CJ, Braun DR, editors. Asian paleoanthropology: from Africa to China and beyond. Dordrecht: Springer; 2010.

  40. 40.

    Krause J, Orlando L, Serre D, et al. Neanderthals in Central Asia and Siberia. Nature. 2007;449:902–4.

  41. 41.

    Sawyer S, Renaud G, Viola B, et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals. Proc Natl Acad Sci USA. 2015;112:15696–700.

  42. 42.

    Ding Q, Hu Y, Xu S, Wang J, Jin L. Neanderthal introgression at chromosome 3p21.31 was under positive natural selection in East Asians. Mol Biol Evol. 2014;31:683–95.

  43. 43.

    Currat M, Excoffier L. Strong reproductive isolation between humans and Neanderthals inferred from observed patterns of introgression. Proc Natl Acad Sci USA. 2011;108:15129–34.

  44. 44.

    Wells RS, Yuldasheva N, Ruzibakiev R, et al. The Eurasian Heartland: a continental perspective on Y-chromosome diversity. Proc Natl Acad Sci USA. 2001;98:10244–49.

  45. 45.

    Fregel R, Cabrera V, Larruga JM, Abu-Amero KK, González AM. Carriers of mitochondrial DNA macrohaplogroup N lineages reached Australia around 50,000 years ago following a northern Asian route. PLoS ONE. 2015;10:e0129839.

  46. 46.

    Jeong C, Alkorta-Aranburu G, Basnyat B, et al. Admixture facilitates genetic adaptations to high altitude in Tibet. Nat Commun. 2014;5:3281.

  47. 47.

    Gu M, Dong X, Shi L, Lin K, Huang X, Chu J. Differences in mtDNA whole sequence between Tibetan and Han populations suggesting adaptive selection to high altitude. Gene. 2012;496:37–44.

  48. 48.

    Kang L, Zheng HX, Chen F, et al. mtDNA lineage expansions in Sherpa population suggest adaptive evolution in Tibetan highlands. Mol Biol Evol. 2013;30:2579–87.

  49. 49.

    Olivieri A, Sidore C, Achilli A, et al. Mitogenome diversity in Sardinians: a genetic window onto an island’s past. Mol Biol Evol. 2017;34:1230–39.

  50. 50.

    Hey J. On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol. 2005;3:e193.

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Acknowledgments

We are grateful to all volunteers and samplers. We thank Ni-Ni Shi, Quan-Kuan Shen, Ya-Jiang Wu, Mu-Yang Wang, Yao-Ming Li, and Feng Xu for the technical assistance. This study was supported by grants from National Natural Science Foundation of China (31301026), Science & Technology Department of Xinjiang Uygur Autonomous Region (201491188), Research Center for Ecology and Environment of Central Asia, Chinese Academy of Sciences, and Bureau of Science and Technology of Yunnan Province. M.-S.P. thanks the support from the Youth Innovation Promotion Association, Chinese Academy of Sciences.

Author information

Author notes

    Affiliations

    1. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China

      • Min-Sheng Peng
      • , Jiao-Jiao Song
      • , Xing Chen
      • , He-Qun Liu
      • , Shi-Fang Wu
      • , Yun Gao
      •  & Ya-Ping Zhang
    2. Key Laboratory of the Chinese Ministry of Education and Xinjiang Uighur Autonomous Region for High-Incident Diseases in Uighur Ethnic Population, Xinjiang Medical University, Urumqi, 830011, China

      • Weifang Xu
      •  & Halmurat Upur
    3. Traditional Chinese Medicine Hospital Affiliated to Xinjiang Medical University, Urumqi, 830000, China

      • Weifang Xu
    4. Institute of Health Sciences, Anhui University, Hefei, 230601, China

      • Jiao-Jiao Song
    5. College of Uighur Medicine, Xinjiang Medical University, Urumqi, 830011, China

      • Xierzhatijiang Sulaiman
    6. The Second People’s Hospital of Kashi, Kashi, 844000, China

      • Liuhong Cai
    7. E.N. Pavlovsky Institute of Zoology and Parasitology, Academy of Sciences of Republic of Tajikistan, Dushanbe, 734025, Tajikistan

      • Najmudinov Tojiddin Abdulloevich
      • , Manilova Elena Afanasevna
      •  & Khudoidodov Behruz Ibrohimovich
    8. Research Center for Ecology and Environment of Central Asia, Chinese Academy of Sciences, Urumqi, 830011, China

      • Xi Chen
      • , Wei-Kang Yang
      •  & Miao Wu
    9. Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, 830011, China

      • Xi Chen
      • , Wei-Kang Yang
      •  & Miao Wu
    10. Kunming Biological Diversity Regional Center of Large Apparatus and Equipments, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China

      • Gui-Mei Li
    11. State Key Laboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, 650091, China

      • Xing-Yan Yang
      •  & Ya-Ping Zhang
    12. Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences & Yunnan Province, Kunming Institute of Zoology, Kunming, 650223, China

      • Allah Rakha
      •  & Yong-Gang Yao
    13. Department of Forensic Sciences, University of Health Sciences, Lahore, 54600, Pakistan

      • Allah Rakha
    14. KIZ/CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming, 650223, China

      • Yong-Gang Yao
      •  & Ya-Ping Zhang
    15. Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, 650204, China

      • Yong-Gang Yao
      •  & Ya-Ping Zhang

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    The authors declare that they have no competing interests.

    Corresponding authors

    Correspondence to Halmurat Upur or Ya-Ping Zhang.

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