Mitochondrial genome evidence reveals successful Late Paleolithic settlement on the Tibetan Plateau
Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved October 21, 2009
Abstract
Due to its numerous environmental extremes, the Tibetan Plateau—the world's highest plateau—is one of the most challenging areas of modern human settlement. Archaeological evidence dates the earliest settlement on the plateau to the Late Paleolithic, while previous genetic studies have traced the colonization event(s) to no earlier than the Neolithic. To explore whether the genetic continuity on the plateau has an exclusively Neolithic time depth, we studied mitochondrial DNA (mtDNA) genome variation within 6 regional Tibetan populations sampled from Tibet and neighboring areas. Our results confirm that the vast majority of Tibetan matrilineal components can trace their ancestry to Epipaleolithic and Neolithic immigrants from northern China during the mid-Holocene. Significantly, we also identified an infrequent novel haplogroup, M16, that branched off directly from the Eurasian M founder type. Its nearly exclusive distribution in Tibetan populations and ancient age (>21 kya) suggest that M16 may represent the genetic relics of the Late Paleolithic inhabitants on the plateau. This partial genetic continuity between the Paleolithic inhabitants and the contemporary Tibetan populations bridges the results and inferences from archaeology, history, and genetics.
Data Availability
Data deposition: All of the sequences obtained in the present study have been deposited into GenBank, with accession numbers FJ544230-FJ544243, FJ968772-FJ968775, and GU014563-GU014569 (for whole mtDNA genomes) and FJ543469-FJ544148 (for control region sequences).
Acknowledgments.
We thank the volunteers for participating in the project. This work was supported by grants from the National Natural Science Foundation of China (30900797 and 30621092), the Chinese Academy of Sciences (Special Grant for the President Scholarship Winner), the Natural Science Foundation of Yunnan Province, and the Kunming Institute of Zoology, CAS (Special Grant for Young Researchers).
Supporting Information
Table S1 (PDF)
Supporting Information
- Download
- 13.93 KB
Table S2 (PDF)
Supporting Information
- Download
- 21.83 KB
Supporting Information (PDF)
Supporting Information
- Download
- 410.96 KB
ST3.xls
- Download
- 227.50 KB
ST4.xls
- Download
- 83.00 KB
ST5.xls
- Download
- 32.50 KB
References
1
DD Zhang, SH Li, Optical dating of Tibetan human hand- and footprints: An implication for the palaeoenvironment of the last glaciation of the Tibetan Plateau. Geophys Res Lett 29, 1072–1074 (2002).
2
M Aldenderfer, Y Zhang, The prehistory of the Tibetan Plateau to the seventh century AD: Perspectives and research from China and the West since 1950. J World Prehist 18, 1–55 (2004).
3
B Yuan, W Huang, D Zhang, New evidence for human occupation of the northern Tibetan Plateau, China during the Late Pleistocene. Chin Sci Bull 52, 2675–2679 (2007).
4
LL Cavalli-Sforza, P Menozzi, A Piazza The History and Geography of Human Genes (Princeton Univ Press, Princeton, NJ), pp. 206 (1994).
5
F-R Wang History of Chinese Ethnic Groups, ed Z-H Wang (China Social Sciences Press, Beijing) Vol 4, 363 (1994).
6
W-W Huang Early Humankind in China, eds R-K Wu, X-Z Wu, S-S Zhang (Science Press, Beijing), pp. 234–235 (1989).
7
W Huo, Archaeological discoveries and research in Tibet in the last decade. Cultural Relics, pp. 85–95 (2000).
8
Y-X Li Original Art in Tibet (Hebei Education Press, Hebei, China), pp. 10–37 (2000).
9
Y-P Qian, et al., Multiple origins of Tibetan Y chromosomes. Hum Genet 106, 453–454 (2000).
10
B Su, et al., Y chromosome haplotypes reveal prehistorical migrations to the Himalayas. Hum Genet 107, 582–590 (2000).
11
A Torroni, et al., Mitochondrial DNA analysis in Tibet: Implications for the origin of the Tibetan population and its adaptation to high altitude. Am J Phys Anthropol 93, 189–199 (1994).
12
Y-G Yao, et al., Genetic relationship of Chinese ethnic populations revealed by mtDNA sequence diversity. Am J Phys Anthropol 118, 63–76 (2002).
13
B Wen, et al., Analyses of genetic structure of Tibeto-Burman populations reveals sex-biased admixture in southern Tibeto-Burmans. Am J Hum Genet 74, 856–865 (2004).
14
T Gayden, et al., The Himalayas as a directional barrier to gene flow. Am J Hum Genet 80, 884–894 (2007).
15
H Shi, et al., Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations. BMC Biol 6, 45 (2008).
16
Y-G Yao, Q-P Kong, C-Y Wang, C-L Zhu, Y-P Zhang, Different matrilineal contributions to genetic structure of ethnic groups in the Silk Road region in China. Mol Biol Evol 21, 2265–2280 (2004).
17
Y-P Qian, et al., Mitochondrial DNA polymorphisms in Yunnan nationalities in China. J Hum Genet 46, 211–220 (2001).
18
T Kivisild, et al., The role of selection in the evolution of human mitochondrial genomes. Genetics 172, 373–387 (2006).
19
Q-P Kong, et al., Phylogeny of East Asian mitochondrial DNA lineages inferred from complete sequences. Am J Hum Genet 73, 671–676 (2003).
20
S Anderson, et al., Sequence and organization of the human mitochondrial genome. Nature 290, 457–465 (1981).
21
RM Andrews, et al., Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23, 147 (1999).
22
Y-G Yao, X-M Lu, H-R Luo, W-H Li, Y-P Zhang, Gene admixture in the silk road region of China: Evidence from mtDNA and melanocortin 1 receptor polymorphism. Genes Genet Syst 75, 173–178 (2000).
23
Y-G Yao, Q-P Kong, X-Y Man, H-J Bandelt, Y-P Zhang, Reconstructing the evolutionary history of China: A caveat about inferences drawn from ancient DNA. Mol Biol Evol 20, 214–219 (2003).
24
Q-P Kong, et al., Updating the East Asian mtDNA phylogeny: A prerequisite for the identification of pathogenic mutations. Hum Mol Genet 15, 2076–2086 (2006).
25
M Palanichamy, et al., Phylogeny of mitochondrial DNA macrohaplogroup N in India, based on complete sequencing: Implications for the peopling of South Asia. Am J Hum Genet 75, 966–978 (2004).
26
C Sun, et al., The dazzling array of basal branches in the mtDNA macrohaplogroup M from India as inferred from complete genomes. Mol Biol Evol 23, 683–690 (2006).
27
H-W Wang, et al., Strikingly different penetrance of LHON in two Chinese families with primary mutation G11778A is independent of mtDNA haplogroup background and secondary mutation G13708A. Mutat Res 643, 48–53 (2008).
28
Q-P Kong, et al., Distilling artificial recombinants from large sets of complete mtDNA genomes. PLoS ONE 3, e3016 (2008).
29
Y-G Yao, Q-P Kong, A Salas, H-J Bandelt, Pseudomitochondrial genome haunts disease studies. J Med Genet 45, 769–772 (2008).
30
Y-G Yao, Q-P Kong, H-J Bandelt, T Kivisild, Y-P Zhang, Phylogeographic differentiation of mitochondrial DNA in Han Chinese. Am J Hum Genet 70, 635–651 (2002).
31
H-J Bandelt, V Macaulay, M Richards, Median networks: Speedy construction and greedy reduction, one simulation, and two case studies from human mtDNA. Mol Phylogenet Evol 16, 8–28 (2000).
32
P Forster, R Harding, A Torroni, H-J Bandelt, Origin and evolution of Native American mtDNA variation: A reappraisal. Am J Hum Genet 59, 935–945 (1996).
33
J Saillard, P Forster, N Lynnerup, H-J Bandelt, S Norby, MtDNA variation among Greenland Eskimos: The edge of the Beringian expansion. Am J Hum Genet 67, 718–726 (2000).
34
UA Perego, et al., Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Curr Biol 19, 1–8 (2009).
35
P Soares, et al., Correcting for purifying selection: An improved human mitochondrial molecular clock. Am J Hum Genet 84, 740–759 (2009).
36
L Pereira, et al., The diversity present in 5140 human mitochondrial genomes. Am J Hum Genet 84, 628–640 (2009).
37
C Sun, Q-P Kong, Y-P Zhang, The role of climate in human mitochondrial DNA evolution: A reappraisal. Genomics 89, 338–342 (2007).
38
M Tanaka, et al., Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome Res 14, 1832–1850 (2004).
39
M Ingman, H Kaessmann, S Pääbo, U Gyllensten, Mitochondrial genome variation and the origin of modern humans. Nature 408, 708–713 (2000).
40
P Soares, et al., Climate change and postglacial human dispersals in southeast Asia. Mol Biol Evol 25, 1209–1218 (2008).
Information & Authors
Information
Published in
Classifications
Copyright
© 2009.
Data Availability
Data deposition: All of the sequences obtained in the present study have been deposited into GenBank, with accession numbers FJ544230-FJ544243, FJ968772-FJ968775, and GU014563-GU014569 (for whole mtDNA genomes) and FJ543469-FJ544148 (for control region sequences).
Submission history
Received: July 14, 2009
Published online: December 15, 2009
Published in issue: December 15, 2009
Keywords
Acknowledgments
We thank the volunteers for participating in the project. This work was supported by grants from the National Natural Science Foundation of China (30900797 and 30621092), the Chinese Academy of Sciences (Special Grant for the President Scholarship Winner), the Natural Science Foundation of Yunnan Province, and the Kunming Institute of Zoology, CAS (Special Grant for Young Researchers).
Notes
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0907844106/DCSupplemental.
Authors
Competing Interests
The authors declare no conflicts of interest.
Metrics & Citations
Metrics
Citation statements
Altmetrics
Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.
Cited by
Loading...
View Options
View options
PDF format
Download this article as a PDF file
DOWNLOAD PDFGet Access
Login options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.