Peopling History of the Tibetan Plateau and Multiple Waves of Admixture of Tibetans Inferred From Both Ancient and Modern Genome-Wide Data

Abstract

Archeologically attested human occupation on the Tibetan Plateau (TP) can be traced back to 160 thousand years ago (kya) via the archaic Xiahe people and 30∼40 kya via the Nwya Devu anatomically modern human. However, the history of the Tibetan populations and their migration inferred from the ancient and modern DNA remains unclear. Here, we performed the first ancient and modern genomic meta-analysis among 3,017 Paleolithic to present-day Eastern Eurasian genomes (2,444 modern individuals from 183 populations and 573 ancient individuals). We identified a close genetic connection between the ancient-modern highland Tibetans and lowland island/coastal Neolithic Northern East Asians (NEA). This observed genetic affinity reflected the primary ancestry of high-altitude Tibeto-Burman speakers originated from the Neolithic farming populations in the Yellow River Basin. The identified pattern was consistent with the proposed common north-China origin hypothesis of the Sino-Tibetan languages and dispersal patterns of the northern millet farmers. We also observed the genetic differentiation between the highlanders and lowland NEAs. The former harbored more deeply diverged Hoabinhian/Onge-related ancestry and the latter possessed more Neolithic southern East Asian (SEA) or Siberian-related ancestry. Our reconstructed qpAdm and qpGraph models suggested the co-existence of Paleolithic and Neolithic ancestries in the Neolithic to modern East Asian highlanders. Additionally, we found that Tibetans from Ü-Tsang/Ando/Kham regions showed a strong population stratification consistent with their cultural background and geographic terrain. Ü-Tsang Tibetans possessed a stronger Chokhopani-affinity, Ando Tibetans had more Western Eurasian related ancestry and Kham Tibetans harbored greater Neolithic southern EA ancestry. Generally, ancient and modern genomes documented multiple waves of human migrations in the TP's past. The first layer of local hunter-gatherers mixed with incoming millet farmers and arose the Chokhopani-associated Proto-Tibetan-Burman highlanders, which further respectively mixed with additional genetic contributors from the western Eurasian Steppe, Yellow River and Yangtze River and finally gave rise to the modern Ando, Ü-Tsang and Kham Tibetans.

Keywords: East Asian; Sino-Tibetan; Tibetan Plateau; ancient genomes; genetic history.

FIGURE 1

The geographical position of the focused Tibetans and genetic patterns of East Asians. (A) Sampling place of eleven geographically different modern Tibetan populations mainly discussed in the present study from the five provinces (Tibet Tibetan Autonomous Region, Qinghai, Gansu, Sichuan, and Yunnan) from western China. China map is presented in the top-left of A and five studied western provinces were zoom-in as the presented Google map. (B) Principal component analysis (PCA) showed the genetic similarities and differences between the ancient/modern East Asians from geographically/linguistically/culturally different populations. Spatial-temporally diverse ancient populations were projected onto the two-dimensional genetic background of modern East Asians. (C) Admixture ancestry estimation based on the model-based ADMIXTURE. Here, the optimal predefined ten ancestral populations were used. EN, early Neolithic; MN, middle Neolithic; LN, late Neolithic; IA, iron age; BA, bronze Age; LBIA, late bronze age and iron age; Lc, loc coverage; O, outlier.

FIGURE 2

Maximum likelihood phylogeny reconstruction based on the genetic variation from both modern Tibetan and Eurasian modern reference populations. (A), modern Tibetan and Neolithic-to-historic East Asian (B). Mbuti was used as the root. Focused on the phylogenetic relationship among all modern populations, we used the patterns of genetic relationship with zero migration events. And evaluating the evolutionary history among modern Tibetan and ancient Chinese, we included three migration events. To better present our result, the drift branch length of Mlabri was shortened as the third of the truth drift branch length due to the strong genetic drift that occurred in Mlabri.

FIGURE 3

The genomic affinity between our Shigatse Tibetan populations and other modern and ancient spatial-temporally different eastern Eurasian populations. The red color denoted a stronger genetic affinity with Shigatse Tibetans, and the blue color showed a lower genetic affinity.

FIGURE 4

The genomic affinity between Chamdo Tibetans and other eastern Eurasian ancient populations inferred from four population affinity-f₄ statistics of the form f₄(Ancient Eastern Eurasian1, Ancient Eastern Eurasian; Tibetan_Chamdo, Mbuti). Red color with statistically significant f₄-values (marked with “+”) demoted Chamdo Tibetans shared more derived alleles with Ancient Eastern Eurasian1 (right population lists) compared with Ancient Eastern Eurasian2 (bottom population lists). Blue color with significant f₄-values denoted Chamdo Tibetans shared more Ancient Eastern Eurasian1-related derived alleles relative to their counterpart.

FIGURE 5

Results of qpAdm showed the main ancestry composition of ancient/modern Tibetans and Jomon Hunter-Gatherer were the results of the mixing of ancient NEA and one deep lineage associated with South Asian Hunter-Gatherer Onge or Southeast Hunter-Gatherer Hoabinhian (the early Asian). Heatmap showed the NEA-related ancestry in the two-way admixture model of Onge and the early Neolithic East Asian (A–F), Middle-Neolithic NEA (G–K), and Late-Neolithic NEA (L–Q). Onge-related ancestry was presented with three cases (R,S,U). Bar plots showed the ancestry composition of the two-way model of Hoabinhian and East Asian for modern Tibetan, Jomon and Ancient Nepal Mebrak and Samdzong people, and three-way model for Qinghai and Gansu Tibetans.

FIGURE 6

Admixture graph model of East Asians and modern Tibetans based on the Human Origin dataset. Admixture history of highland Tibetan from Lhasa (A) and lowland Tibetan from Yunnan (B). Heatmap showed the ancestry composition of modern Tibetans from three source populations: deep hunter-gatherer One-related ancestry (C), the first batch of Neolithic farmer-associated ancestry (D) and the second batch of Neolithic farmer related ancestry (E). Denisovan and Central African of Mbuti were used as the Archaic and modern roots respectively. Western Eurasian was represented by Loschbour. Deep southern Eurasian (SEE) and northern Eurasian (NEE) were represented by South Asian Hunter-Gatherers of Onge and 40,000-year-old Tianyuan people. East Asian subsequently diverged as NEA (NEA) and SEA (SEA). All f₄-statistics of included populations are predicted to within 3 standard errors of their observed values. Branch lengths are given in units of 1000 times the f₂ drift distance (rounded to the nearest integer). Pound signs denoted the modern populations added to the basic model of A,B with larger Z-scores or Zero internal branch length. Blue dotted lines denoted admixture events with admixture proportions as shown.

FIGURE 7

Admixture graph model of East Asians and modern Tibetans from the northeast Tibetan Plateau based on the Human Origin dataset. Admixture history of Tibetan from Xunhua (A), Tibetan from Gangcha (B), and Tibetan from Gannan (C).

FIGURE 8

Admixture graph model of East Asians and modern lowland Tibetans based on the Human Origin dataset. Admixture history of lowland Tibetan from Yunnan (A), Tibetan from Xinlong (B), and Tibetan from Yajiang (C).

FIGURE 9

Admixture graph model of modern highland and lowland Tibetans based on the Human Origin dataset using Late-Neolithic Wadian people as the source of the second migration into Tibetan Plateau. Admixture history of lowland Tibetan from Yunnan (A), Tibetan from Yajiang (B), and highland Tibetan from Lhasa (C).

FIGURE 10

qpGraph-based admixture models showed the differentiated Denisovan admixture landscape between East Asians and Oceanians.