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Peopling of Tibet Plateau and Multiple Waves of Admixture of Tibetans

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bioRxiv preprint doi: https://doi.org/10.1101/2020.07.03.185884; this version posted July 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Peopling of Tibet Plateau and multiple waves of admixture of Tibetans 2 inferred from both modern and ancient genome-wide data 3 4 Mengge Wang1,*, Xing Zou1,*, Hui-Yuan Ye2,*, Zheng Wang1, Yan Liu3, Jing Liu1, Fei Wang1, Hongbin 5 Yao4, Pengyu Chen5, Ruiyang Tao1, Shouyu Wang1, Lan-Hai Wei6, Renkuan Tang7,#, Chuan-Chao 6 Wang6,# , Guanglin He1,6,# 7 8 1Institute of Forensic Medicine, West China School of Basic Science and Forensic Medicine, Sichuan 9 University, Chengdu, China 10 2School of Humanities, Nanyang Technological University, Nanyang, 639798, Singapore 11 3College of Basic Medicine, Chuanbei Medical University 12 4 Belt and Road Research Center for Forensic Molecular Anthropology, Key Laboratory of Evidence 13 Science of Gansu Province, Gansu University of Political Science and Law, Lanzhou 730070, China 14 5Center of Forensic Expertise, Affiliated hospital of Zunyi Medical University, Zunyi, Guizhou, China 15 6Department of Anthropology and Ethnology, Institute of Anthropology, National Institute for Data 16 Science in Health and Medicine, and School of Life Sciences, Xiamen University, Xiamen, China 17 7Department of Forensic Medicine, College of Basic Medicine, Chongqing Medical University, 18 Chongqing, China 19 20 *These authors contributed equally to this work and should be considered co-first authors. 21 22 #Corresponding author 23 Renkuan Tang 24 Department of Forensic Medicine, College of Basic Medicine, Chongqing Medical University, 25 Chongqing, China 26 Email: [email protected] 27 Chuan-Chao Wang 28 Affiliation: Department of Anthropology and Ethnology, Institute of Anthropology, National Institute for 29 Data Science in Health and Medicine, Xiamen University, 30 Xiamen, China. 31 E-mail: [email protected] 32 Guanglin He 33 Affiliation: Department of Anthropology and Ethnology, Institute of Anthropology, National Institute for 34 Data Science in Health and Medicine, Xiamen University, 35 Xiamen, China. 36 E-mail: [email protected] 37 38 39 Abstract 40 Archeologically attested human occupation on the Tibet Plateau (TP) can be traced back to 160 thousand 41 years ago (kya, Xiahe) via archaic people and 30~40 kya via anatomically modern human in Nwya Devu. 42 However, the past human movements and peopling of the TP keep in its infancy in the modern/ancient 43 DNA studies. Here, we performed the first modern/ancient genomic meta-analysis among 3,017 44 Paleolithic to present-day eastern Eurasian genomes (2,444 modern individuals from 183 populations 45 (including 98 Ü-Tsang/Ando/Kham Tibetans) and 573 ancients (including 161 Chinese ancients first 46 meta-analyzed here)). Closer genetic connection between ancient-modern highland Tibetans and lowland 47 island/coastal Neolithic northern East Asians was identified, reflecting the main ancestry of high-altitude 48 Tibeto-Burman speakers originated from the ancestors of Houli/Yangshao/Longshan ancients in the 49 middle and lower Yellow River basin, consistent with the common North-China origin of Sino-Tibetan 50 language and dispersal pattern of millet farmers. Although the shared common northern East Asian 51 lineage between Tibetans and lowland East Asians, we still identified genetic differentiation between 52 Highlanders and lowland northern East Asians, the former harboring more deeply diverged 53 Hoabinhian/Onge ancestry and the latter possessing more modern Neolithic southern East Asian and 54 Siberian ancestry, which suggested the co-existence of Paleolithic and Neolithic ancestries in modern 55 and Neolithic East Asian Highlanders. Tibetans from Ü-Tsang/Ando/Kham Tibetan regions showed 56 strong population stratifications consistent with their cultural backgrounds and geographic terrains 57 (showed as barriers for human movements): stronger Chokhopani affinity in Ü-Tsang Tibetans, more 58 western Eurasian ancestry in Ando and greater Neolithic southern East Asian ancestry in Kham Tibetan. 59 Modern combined ancient genomes documented multiple waves of human migrations in TP past: the bioRxiv preprint doi: https://doi.org/10.1101/2020.07.03.185884; this version posted July 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 60 first layer of local Hunter-Gatherer mixed with Qijia Farmer arose the Chokhopani-associated Proto- 61 Tibetan-Burman, admixture with the additional genetic materials from the western Eurasian steppe, 62 Yellow River and Yangtze River respectively gave rise to modern Ando, Ü-Tsang and Kham Tibetans. 63 Keywords: Ancient genomes, Tibetan Plateau, Sino-Tibetan, Genetic history, East Asian 64 65 Introduction 66 The Tibet Plateau (TP), widely known as the Third Pole of the world, forms the high-altitude core of 67 Asia with an average elevation of more than 4,000 meters above sea level (masl) and represents one of 68 the most demanding environments for human settlement due to perennial low temperatures, extreme 69 aridity, and severe hypoxia. However, archeological and genetic studies have indicated that archaic 70 hominins occupied the TP had well adapted to the high-altitude hypoxic environment long before the 71 arrival of modern Homo sapiens and present-day Tibetan Highlanders have adapted uniquely to extreme 72 high-altitude conditions since the initial colonization of the TP(Qi, et al. 2013; Jeong, et al. 2016; 73 Gnecchi-Ruscone, et al. 2018; Chen, Welker, et al. 2019). Besides, recent linguistic evidence suggested 74 that Tibeto-Burman populations diverged from Han Chinese with an average coalescence age of 75 approximately 5.9 thousand years ago (kya). At present, over seven million indigenous Tibetans (2016 76 census) have settled in the Plateau and are successfully adapted to the high-altitude hypoxic environment. 77 Genomic evidence supported that multiple variants may jointly deliver the fitness of the modern Tibetans 78 on the TP, and Denisovan introgression into modern Tibetans and surrounding populations including 79 positively selected haplotypes of HIF-1α prolyl hydroxylase1 (EGLN1) and Endothelial PAS domain 80 protein 1 (EPAS1) is significantly associated with the high-altitude adaptation to hypoxia(Simonson, et 81 al. 2010; Xu, et al. 2011; Xiang, et al. 2013; Huerta-Sanchez, et al. 2014; Lu, et al. 2016; Gnecchi- 82 Ruscone, et al. 2018; Chen, Welker, et al. 2019; Deng, et al. 2019). Compared to other parts of East 83 Asia(Reich 2018; Ning, et al. 2019; Jeong, et al. 2020; Ning, et al. 2020; Wang, Yeh, et al. 2020; Yang, 84 et al. 2020), the greatest problem facing researchers is the lack of excavated archaeological sites on the 85 TP, which means that certain types of critical data, such as zooarchaeological and archaeobotanical data 86 for reconstructing the subsistence strategy, ancient DNA (aDNA) for dissecting the genomic correlation 87 between ancient individuals and modern Tibetan-like Highlanders, are in short supply. 88 89 To date, whence and how the early human colonizers conquered the TP and who modern Tibetans 90 descended from are two key questions that remain to be solved, however, archaeological, 91 paleoanthropological and genetic researches on the peopling of the TP and demographic history of 92 Tibetan Highlanders are still in a developmental stage. As revealed by archaeological evidence, 93 handprints and footprints of Homo sapiens found in the southern TP (Quesang site) at 4,200 masl 94 suggested that the TP retains traces of an intermittent human presence from at least 20 kya(Zhang and Li 95 2002), but some scholars supporting at the early Holocene(Meyer, et al. 2017). The Nwya Devu site, 96 located nearly 4,600 masl in central Tibet, could be dated to at least 30 kya, which deepens considerably 97 the history of the peopling of the TP and the antiquity of human high-altitude adaptations(Zhang, et al. 98 2018). The palaeoproteomic analysis of a Xiahe Denisovan mandible indicated that the prehistoric 99 colonization of archaic hominins on the TP could be traced back to the Middle Pleistocene epoch (around 100 160 kya)(Chen, Welker, et al. 2019). Additionally, genomic evidence strongly suggested that modern 101 humans did exist on the TP before the Last Glacial Maximum (LGM), and the existence of genetic relics 102 of the Upper Paleolithic inhabitants in modern Tibetans indicated some genetic continuity between the 103 initial Paleolithic settlers and modern Tibetan Highlanders(Zhao, et al. 2009; Qin, et al. 2010; Qi, et al. 104 2013; Li, et al. 2015; Lu, et al. 2016). The archaeogenetic investigation of prehistoric Himalayan 105 populations provided supporting evidence for the high-elevation East Asian origin of the first inhabitants 106 of the Himalayas, indirectly indicating the pre-Neolithic human activities on the TP(Jeong, et al. 2016). 107 108 In contrast to the Late Pleistocene hunter-gatherer colonization, the timing and dynamics of the 109 permanent human occupation of the TP have provoked much debate(Aldenderfer 2011; Qi, et al. 2013; 110 Chen, et al. 2015; d’Alpoim Guedes 2015; Lu 2016; Rhode 2016; Hu, et al. 2019; Li, Tian, et al. 2019a; 111 Ren, et al. 2020). Archaeological and genomic findings revealed that the permanent settlement of the TP 112 was a relatively recent occurrence that coincided with
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