A study of the mitochondrial genome of ancient inhabitants from the Latuotanggu cemetery, Tibet, China

doi:10.16359/j.cnki.cn11-1963/q.2020.0078

Abstract

Abstract:

With rapid advances in next generation sequencing technologies, we have extracted three ancient DNA from samples from Tibet. With a dataset of present-day East Asians, we tried to reconstruct the history of this region using population genetic methods. Using the mtDNA genome, our study focused on the maternal relationship between ancient Tibetans living in 700BP and present-day populations, which revealed a genetic continuity on Tibetan plateau between the LaTuoTangGu (LTTG) cemetery and present-day Tibetans. This study is the first mtDNA genomic research of high elevation Tibetans.

Key words: Tibet, Ancient DNA, Mitochondrial genome, Latuotanggu, Neolithic

CLC Number:

Q987

DING Manyu, HE Wei, WANG Tianyi, Shargan Wangdue, ZHANG Ming, CAO Peng, LIU Feng, DAI Qingyan, FU Qiaomei. A study of the mitochondrial genome of ancient inhabitants from the Latuotanggu cemetery, Tibet, China[J]. Acta Anthropologica Sinica, 2021, 40(01): 1-11.

Figures/Tables 6

References 49

[1]	Zhang XL, Ha BB, Wang SJ, et al. The earliest human occupation of the high-altitude Tibetan Plateau 40 thousand to 30 thousand years ago[J]. Science, 2018, 362(6418): 1049-1051 doi: 10.1126/science.aat8824 URL pmid: 30498126
[2]	Lu D, Lou H, Kai Y, et al. Ancestral origins and genetic history of Tibetan highlanders[J]. American Journal of Human Genetics, 2016, 99(3): 580-594 doi: 10.1016/j.ajhg.2016.07.002 URL pmid: 27569548
[3]	Li J, Zeng W, Zhang Y, et al. Ancient DNA reveals genetic connections between early Di-Qiang and Han Chinese[J]. BMC Evolutionary Biology, 2017, 17(1): 239 doi: 10.1186/s12862-017-1082-0 URL pmid: 29202706
[4]	Yong-Bin Z, Hong-Jie L, Sheng-Nan L, et al. Ancient DNA evidence supports the contribution of Di-Qiang people to the Han Chinese gene pool[J]. American Journal of Physical Anthropology, 2011, 144(2): 258-268 doi: 10.1002/ajpa.21399 URL pmid: 20872743
[5]	Handt O, Krings M, Ward RH, et al. The retrieval of ancient human DNA sequences[J]. American Journal of Human Genetics, 1996, 59(2): 368-76 URL pmid: 8755923
[6]	Jeong C, Ozga AT, Witonsky DB, et al. Long-term genetic stability and a high-altitude East Asian origin for the peoples of the high valleys of the Himalayan arc[J]. Proceedings of the National Academy of Sciences, 2016, 113(27): 7485 doi: 10.1073/pnas.1520844113 URL
[7]	Duong NT, Macholdt E, Ton ND, et al. Complete human mtDNA genome sequences from Vietnam and the phylogeography of Mainland Southeast Asia[J]. Scientific Reports, 2018, 8(1): 11651. doi: 10.1038/s41598-018-29989-0 URL pmid: 30076323
[8]	Lippold S, Xu H, Ko A, et al. Human paternal and maternal demographic histories: Insights from high-resolution Y chromosome and mtDNA sequences[J]. Investigative Genetics, 2014, 5(1): 13. doi: 10.1186/2041-2223-5-13 URL
[9]	Zhendong Q, Yajun Y, Longli K, et al. A mitochondrial revelation of early human migrations to the Tibetan Plateau before and after the last glacial maximum[J]. American Journal of Physical Anthropology, 2010, 143(4): 555-569 doi: 10.1002/ajpa.21350 URL pmid: 20623602
[10]	Mian Z, Qing-Peng K, Hua-Wei W, et al. Mitochondrial genome evidence reveals successful Late Paleolithic settlement on the Tibetan Plateau[J]. Proceedings of the National Academy of Sciences, 2009, 106(50): 21230-5 doi: 10.1073/pnas.0907844106 URL
[11]	Peng MS, Palanichamy MG, Yao YG, et al. Inland post-glacial dispersal in East Asia revealed by mitochondrial haplogroup M9a’b[J]. BMC Biology, 2011, 9(1): 2. doi: 10.1186/1741-7007-9-2 URL
[12]	Peng MS, Xu W, Song JJ, et al. Mitochondrial genomes uncover the maternal history of the Pamir populations[J]. European Journal of Human Genetics, 2017. doi: 10.1038/s41431-020-00807-4 URL pmid: 33495594
[13]	Kang L, Zheng HX, Zhang M, et al. MtDNA analysis reveals enriched pathogenic mutations in Tibetan highlanders[J]. Scientific Reports, 2016, 6(1): 31083 doi: 10.1038/srep31083 URL
[14]	Li YC, Wang HW, Tian JY, et al. Ancient inland human dispersals from Myanmar into interior East Asia since the Late Pleistocene[J]. Scientific Reports, 2015, 5:9473 doi: 10.1038/srep09473 URL pmid: 25826227
[15]	Adimoolam C, Satish K, Jwalapuram S, et al. Updating phylogeny of mitochondrial DNA macrohaplogroup m in India: Dispersal of modern human in South Asian corridor[J]. Plos One, 2009, 4(10): e7447 doi: 10.1371/journal.pone.0007447 URL pmid: 19823670
[16]	Summerer M, Horst J, Erhart G, et al. Large-scale mitochondrial DNA analysis in southeast Asia reveals evolutionary effects of cultural isolation in the multi-ethnic population of Myanmar[J]. BMC Evolutionary Biology, 2014, 14(1): 17 doi: 10.1186/1471-2148-14-17 URL
[17]	Wang HW, Li YC, Sun F, et al. Revisiting the role of the Himalayas in peopling Nepal: Insights from mitochondrial genomes[J]. Journal of Human Genetics, 2012, 57(4): 228 doi: 10.1038/jhg.2012.8 URL
[18]	Bhandari S, Zhang X, Cui C, et al. Genetic evidence of a recent Tibetan ancestry to Sherpas in the Himalayan region[J]. Scientific Reports, 2015, 5:16249 doi: 10.1038/srep16249 URL pmid: 26538459
[19]	Fornarino S, Pala M, Battaglia V, et al. Mitochondrial and Y-chromosome diversity of the Tharus (Nepal): A reservoir of genetic variation[J]. BMC Evolutionary Biology, 2009, 9(1): 154 doi: 10.1186/1471-2148-9-154 URL
[20]	Derenko M, Malyarchuk B, Denisova G, et al. Western Eurasian ancestry in modern Siberians based on mitogenomic data[J]. BMC Evolutionary Biology, 2014, 14(1): 217 doi: 10.1186/s12862-014-0217-9 URL
[21]	Albert Min-Shan K, Chung-Yu C, Qiaomei F, et al. Early Austronesians: into and out of Taiwan[J]. American Journal of Human Genetics, 2014, 94(3): 426-36 doi: 10.1016/j.ajhg.2014.02.003 URL
[22]	Kutanan W, Kampuansai J, Srikummool M, et al. Complete mitochondrial genomes of Thai and Lao populations indicate an ancient origin of Austroasiatic groups and demic diffusion in the spread of TaifKadai languages[J]. Human Genetics, 2017, 136(1): 85-98 doi: 10.1007/s00439-016-1742-y URL pmid: 27837350
[23]	Dabney J, Knapp M, Glocke I, et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(39): 15758-63 doi: 10.1073/pnas.1314445110 URL
[24]	Rohland N, Harney E, Mallick S, et al. Partial uracil-DNA-glycosylase treatment for screening of ancient DNA[J]. Philosophical Transactions of the Royal Society of London, 2015, 370(1660): 20130624 doi: 10.1098/rstb.2013.0624 URL pmid: 25487342
[25]	Jesse D, Matthias M. Length and GC-biases during sequencing library amplification: A comparison of various polymerase-buffer systems with ancient and modern DNA sequencing libraries[J]. Biotechniques, 2012, 52(2): 87-94 doi: 10.2144/000113809 URL
[26]	Kircher M, Sawyer S, Meyer M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform[J]. Nucleic Acids Research, 2012, 40(1): e3 doi: 10.1093/nar/gkr771 URL pmid: 22021376
[27]	Fu Q, Meyer M, Gao X, et al. DNA analysis of an early modern human from Tianyuan Cave, China[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(6): 2223 doi: 10.1073/pnas.1221359110 URL
[28]	Gabriel R, Udo S, Janet K. LeeHom: Adaptor trimming and merging for Illumina sequencing reads[J]. Nucleic Acids Research, 2014, 42(18): e141 doi: 10.1093/nar/gku699 URL pmid: 25100869
[29]	Gabriel R, Udo S, Tomislav M, et al. DeML: Robust demultiplexing of Illumina sequences using a likelihood-based approach[J]. Bioinformatics, 2014, 31(5): 770-2 doi: 10.1093/bioinformatics/btu719 URL pmid: 25359895
[30]	Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform[J]. Bioinformatics, 2009, 25(14): 1754-60 doi: 10.1093/bioinformatics/btp324 URL pmid: 19451168
[31]	Anita KBT, Dominic P, Sebastian SN, et al. HaploGrep: A fast and reliable algorithm for automatic classification of mitochondrial DNA haplogroups[J]. Human Mutation, 2011, 32(1): 25-32 doi: 10.1002/humu.21382 URL
[32]	Oven MV. PhyloTree Build 17: Growing the human mitochondrial DNA tree[J]. Forensic Science International, Genetics Supplement, 2015.
[33]	Kutanan W, et al. New insights from Thailand into the maternal genetic history of mainland southeast Asia. Eur J Hum Genet, 2018, 26(6): 898-911 doi: 10.1038/s41431-018-0113-7 URL pmid: 29483671
[34]	Edgar RC. Muscle: Multiple sequence alignment with improved accuracy and speed[A]// Proceedings of the Computational Systems Bioinformatics Conference[C], IEEE, 2004.
[35]	Edgar RC. Muscle: A multiple sequence alignment method with reduced time and space complexity[J]. BMC Bioinformatics, 2004, 5:113 doi: 10.1186/1471-2105-5-113 URL pmid: 15318951
[36]	Bandelt HJ, Forster P. HLA. Median-joining networks for inferring intraspecific phylogenies[J]. Molecular Biology and Evolution, 1999, 16(1): 37-48 doi: 10.1093/oxfordjournals.molbev.a026036 URL pmid: 10331250
[37]	Leigh JW, Bryant D, Nakagawa S. Popart: Full-feature software for haplotype network construction[J]. Methods in Ecology and Evolution, 2015, 6(9): 1110-1116 doi: 10.1111/mee3.2015.6.issue-9 URL
[38]	Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10[J]. Virus Evolution, 2018, 4(1). doi: 10.1093/ve/vex043 URL pmid: 29340211
[39]	Excoffier L, Lischer H. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows[J]. Molecular Ecology Resources, 2010, 10(3): 564-567 doi: 10.1111/j.1755-0998.2010.02847.x URL pmid: 21565059
[40]	Hodges E, Xuan Z, Balija V, et al. Genome-wide in situ exon capture for selective resequencing[J]. Nature Genetics, 2007, 39(12): 1522-1527 doi: 10.1038/ng.2007.42 URL pmid: 17982454
[41]	Sawyer S, Renaud G, Viola B, et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(51): 15696 doi: 10.1073/pnas.1519905112 URL pmid: 26630009
[42]	Patterson N, Moorjani P, Luo Y, et al. Ancient admixture in human history[J]. Genetics, 2012, 192(3): 1065 doi: 10.1534/genetics.112.145037 URL
[43]	David P. jModelTest: Phylogenetic model averaging[J]. Molecular Biology & Evolution, 2008, 25(7): 1253-1256 doi: 10.1093/molbev/msn083 URL pmid: 18397919
[44]	Jose Manuel S, Diego D, Taboada GL, et al. jmodeltest.org: Selection of nucleotide substitution models on the cloud[J]. Bioinformatics, 2014, 30(9): 1310-1311 doi: 10.1093/bioinformatics/btu032 URL
[45]	Meyer MC, et al. Permanent human occupation of the central Tibetan Plateau in the early Holocene[J]. Science, 2017, 355(6320): 64-67 doi: 10.1126/science.aag0357 URL pmid: 28059763
[46]	Brantingham PJ, Xing G, Madsen DB, et al. Late occupation of the high-elevation northern Tibetan plateau based on cosmogenic, luminescence, and radiocarbon ages[J]. Geoarchaeology, 2013, 28(5): 413-431 doi: 10.1002/gea.2013.28.issue-5 URL
[47]	Chen FH, et al. , Agriculture facilitated permanent human occupation of the Tibetan Plateau after 3600 B.P[J]. Science, 2015, 347(6219): 248-250 doi: 10.1126/science.1259172 URL pmid: 25593179
[48]	Lu H. Colonization of the Tibetan plateau, permanent settlement, and the spread of agriculture: Reflection on current debates on the prehistoric archeology of the Tibetan plateau[J]. Archaeological Research in Asia, 2016, 5:12-15 doi: 10.1016/j.ara.2016.02.010 URL
[49]	Qi X, Cui C, Peng Y, et al. Genetic evidence of Paleolithic colonization and Neolithic expansion of modern humans on the Tibetan plateau[J]. Molecular Biology and Evolution, 2013, 30(8): 1761-78 doi: 10.1093/molbev/mst093 URL

建库号Library ID	样本号 Sample ID	墓号 Cemetery ID	平均污染度 Average Contamination	污染95%置信区间 95% CI of Contamination	5’ C->T	测年 ¹⁴C Date(BP)	覆盖度 Coverage	单倍体型Haplotype
L7056	C3425	M4	0.04%	0.01-0.13	2.2 %	760~675	476.6	M9a1a1c1b1a
L7055	C3427	M6	0.76%	0.55-1.05	9 %	NA	372.0	M9a1a1c1b1a
L7054	C3428	M5②	0.69%	0.48-0.99	3.9 %	NA	396.1	A17

建库号Library ID	样本号 Sample ID	墓号 Cemetery ID	平均污染度 Average Contamination	污染95%置信区间 95% CI of Contamination	5’ C->T	测年 ¹⁴C Date(BP)	覆盖度 Coverage	单倍体型Haplotype
L7056	C3425	M4	0.04%	0.01-0.13	2.2 %	760~675	476.6	M9a1a1c1b1a
L7055	C3427	M6	0.76%	0.55-1.05	9 %	NA	372.0	M9a1a1c1b1a
L7054	C3428	M5②	0.69%	0.48-0.99	3.9 %	NA	396.1	A17

地区 Area	人群 Population	M9a Frequency	文献来源 Reference
中国西藏	LTTG	50%	本研究
尼泊尔	a.Nepal	50%	[6]
中国西藏	Nyingchi	13%	[9]
中国西藏	Lhasa	25%	[9]
中国西藏	Shigatse	25%	[9]
中国西藏	Chamdo	13%	[9]
中国西藏	Deng	39.56%	[13]
中国西藏	Monpa	41.17%	[13]
中国西藏	Lhoba	15.38%	[13]
中国西藏	Sherpa	18.40%	[13]
中国西藏	Ngari	24%	[9]
中国北方	Daur	10%	[8]
中国北方	Tu	10%	[8]
中国南方	Han	2%	[8]
尼泊尔	Nepal	12%	[19]
印度北部	NE.India	9%	[15]

地区 Area	人群 Population	M9a Frequency	文献来源 Reference
中国西藏	LTTG	50%	本研究
尼泊尔	a.Nepal	50%	[6]
中国西藏	Nyingchi	13%	[9]
中国西藏	Lhasa	25%	[9]
中国西藏	Shigatse	25%	[9]
中国西藏	Chamdo	13%	[9]
中国西藏	Deng	39.56%	[13]
中国西藏	Monpa	41.17%	[13]
中国西藏	Lhoba	15.38%	[13]
中国西藏	Sherpa	18.40%	[13]
中国西藏	Ngari	24%	[9]
中国北方	Daur	10%	[8]
中国北方	Tu	10%	[8]
中国南方	Han	2%	[8]
尼泊尔	Nepal	12%	[19]
印度北部	NE.India	9%	[15]