.2024 Jul 3;41(7):msae122.

doi: 10.1093/molbev/msae122.

Multiple Human Population Movements and Cultural Dispersal Events Shaped the Landscape of Chinese Paternal Heritage

Mengge Wang^{1 2 3}, Yuguo Huang¹, Kaijun Liu^{4 5}, Zhiyong Wang^{1 6}, Menghan Zhang^{7 8}, Haibing Yuan², Shuhan Duan^{1 9}, Lanhai Wei¹⁰, Hongbing Yao¹¹, Qiuxia Sun^{1 12}, Jie Zhong¹, Renkuan Tang¹², Jing Chen^{1 13}, Yuntao Sun^{1 14}, Xiangping Li^{1 6}, Haoran Su^{1 15}, Qingxin Yang^{1 6}, Liping Hu⁶, Libing Yun¹⁴, Junbao Yang¹⁶, Shengjie Nie⁶, Yan Cai¹⁵, Jiangwei Yan¹³, Kun Zhou⁵, Chuanchao Wang¹⁷; 10K_CPGDP Consortium; Bofeng Zhu^{18 19}, Chao Liu^{18 20}, Guanglin He^{1 2}

Collaborators, Affiliations

Collaborators

10K_CPGDP Consortium:
Guanglin He, Chao Liu, Mengge Wang, Renkuan Tang, Libing Yun, Junbao Yang, Chuan-Chao Wang, Jiangwei Yan, Bofeng Zhu, Liping Hu, Shengjie Nie, Hongbing Yao

Affiliations

¹ Institute of Rare Diseases, West China Hospital of Sichuan University, Sichuan University, Chengdu 610000, China.
² Center for Archaeological Science, Sichuan University, Chengdu 610000, China.
³ Faculty of Forensic Medicine, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510275, China.
⁴ School of International Tourism and Culture, Guizhou Normal University, Guiyang 550025, China.
⁵ MoFang Human Genome Research Institute, Tianfu Software Park, Chengdu, Sichuan 610042, China.
⁶ School of Forensic Medicine, Kunming Medical University, Kunming 650500, China.
⁷ Institute of Modern Languages and Linguistics, Fudan University, Shanghai 200433, China.
⁸ Research Institute of Intelligent Complex Systems, Fudan University, Shanghai 200433, China.
⁹ School of Basic Medical Sciences, North Sichuan Medical College, Nanchong 637100, China.
¹⁰ School of Ethnology and Anthropology, Institute of Humanities and Human Sciences, Inner Mongolia Normal University, Hohhot 010022, China.
¹¹ Belt and Road Research Center for Forensic Molecular Anthropology Gansu University of Political Science and Law, Lanzhou 730000, China.
¹² Department of Forensic Medicine, College of Basic Medicine, Chongqing Medical University, Chongqing 400331, China.
¹³ School of Forensic Medicine, Shanxi Medical University, Jinzhong 030001, China.
¹⁴ Institute of Forensic Medicine, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu 610041, China.
¹⁵ School of Laboratory Medicine and Center for Genetics and Prenatal Diagnosis, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637007, China.
¹⁶ Institute of Basic Medicine and Forensic Medicine, North Sichuan Medical College and Center for Genetics and Prenatal Diagnosis, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637007, China.
¹⁷ State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen 361005, China.
¹⁸ Guangzhou Key Laboratory of Forensic Multi-Omics for Precision Identification, School of Forensic Medicine, Southern Medical University, Guangzhou 510515, China.
¹⁹ Microbiome Medicine Center, Department of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, China.
²⁰ Anti-Drug Technology Center of Guangdong Province, Guangzhou 510230, China.

PMID:38885310
PMCID: PMC11232699
DOI: 10.1093/molbev/msae122

Multiple Human Population Movements and Cultural Dispersal Events Shaped the Landscape of Chinese Paternal Heritage

Mengge Wang et al. Mol Biol Evol.2024.

.2024 Jul 3;41(7):msae122.

doi: 10.1093/molbev/msae122.

Authors

Collaborators

10K_CPGDP Consortium:
Guanglin He, Chao Liu, Mengge Wang, Renkuan Tang, Libing Yun, Junbao Yang, Chuan-Chao Wang, Jiangwei Yan, Bofeng Zhu, Liping Hu, Shengjie Nie, Hongbing Yao

Affiliations

¹ Institute of Rare Diseases, West China Hospital of Sichuan University, Sichuan University, Chengdu 610000, China.
² Center for Archaeological Science, Sichuan University, Chengdu 610000, China.
³ Faculty of Forensic Medicine, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510275, China.
⁴ School of International Tourism and Culture, Guizhou Normal University, Guiyang 550025, China.
⁵ MoFang Human Genome Research Institute, Tianfu Software Park, Chengdu, Sichuan 610042, China.
⁶ School of Forensic Medicine, Kunming Medical University, Kunming 650500, China.
⁷ Institute of Modern Languages and Linguistics, Fudan University, Shanghai 200433, China.
⁸ Research Institute of Intelligent Complex Systems, Fudan University, Shanghai 200433, China.
⁹ School of Basic Medical Sciences, North Sichuan Medical College, Nanchong 637100, China.
¹⁰ School of Ethnology and Anthropology, Institute of Humanities and Human Sciences, Inner Mongolia Normal University, Hohhot 010022, China.
¹¹ Belt and Road Research Center for Forensic Molecular Anthropology Gansu University of Political Science and Law, Lanzhou 730000, China.
¹² Department of Forensic Medicine, College of Basic Medicine, Chongqing Medical University, Chongqing 400331, China.
¹³ School of Forensic Medicine, Shanxi Medical University, Jinzhong 030001, China.
¹⁴ Institute of Forensic Medicine, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu 610041, China.
¹⁵ School of Laboratory Medicine and Center for Genetics and Prenatal Diagnosis, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637007, China.
¹⁶ Institute of Basic Medicine and Forensic Medicine, North Sichuan Medical College and Center for Genetics and Prenatal Diagnosis, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637007, China.
¹⁷ State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen 361005, China.
¹⁸ Guangzhou Key Laboratory of Forensic Multi-Omics for Precision Identification, School of Forensic Medicine, Southern Medical University, Guangzhou 510515, China.
¹⁹ Microbiome Medicine Center, Department of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, China.
²⁰ Anti-Drug Technology Center of Guangdong Province, Guangzhou 510230, China.

PMID:38885310
PMCID: PMC11232699
DOI: 10.1093/molbev/msae122

Abstract

Large-scale genomic projects and ancient DNA innovations have ushered in a new paradigm for exploring human evolutionary history. However, the genetic legacy of spatiotemporally diverse ancient Eurasians within Chinese paternal lineages remains unresolved. Here, we report an integrated Y-chromosome genomic database encompassing 15,563 individuals from both modern and ancient Eurasians, including 919 newly reported individuals, to investigate the Chinese paternal genomic diversity. The high-resolution, time-stamped phylogeny reveals multiple diversification events and extensive expansions in the early and middle Neolithic. We identify four major ancient population movements, each associated with technological innovations that have shaped the Chinese paternal landscape. First, the expansion of early East Asians and millet farmers from the Yellow River Basin predominantly carrying O2/D subclades significantly influenced the formation of the Sino-Tibetan people and facilitated the permanent settlement of the Tibetan Plateau. Second, the dispersal of rice farmers from the Yangtze River Valley carrying O1 and certain O2 sublineages reshapes the genetic makeup of southern Han Chinese, as well as the Tai-Kadai, Austronesian, Hmong-Mien, and Austroasiatic people. Third, the Neolithic Siberian Q/C paternal lineages originated and proliferated among hunter-gatherers on the Mongolian Plateau and the Amur River Basin, leaving a significant imprint on the gene pools of northern China. Fourth, the J/G/R paternal lineages derived from western Eurasia, which were initially spread by Yamnaya-related steppe pastoralists, maintain their presence primarily in northwestern China. Overall, our research provides comprehensive genetic evidence elucidating the significant impact of interactions with culturally distinct ancient Eurasians on the patterns of paternal diversity in modern Chinese populations.

Keywords: Y-chromosome phylogeny; YanHuang cohort; evolutionary history; founding lineage.

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Conflict of interest statement

Conflict of Interest The authors declare that they have no competing interests.

Figures

**Fig. 1.**
Geographic location and phylogenetic characteristics of 919 newly sequenced Chinese minority individuals. a) A map of East Asia displays essential data for 919 individuals from 57 Chinese ethnic minority groups. Circle sizes on the map indicate the sample sizes of individual populations, while colored provinces represent sampling locations, with colors denoting the total sample size from those regions. Additionally, ancient subsistence strategies, such as pastoralism, hunter-gathering, and agriculture, from western Eurasia, the Mongolian Plateau, and the origin centers of Chinese agriculture in the Yellow and Yangtze River basins are depicted. b) The Y-chromosome phylogeny includes 914 individuals who passed quality control, illustrating the most recent common ancestors (TMRCA) of various prevalent paternal lineages. B-lineage-related representative haplotypes from the Simons Genome Diversity Project serve as an outgroup. Branch lengths correlate with the estimated TMRCA. Major lineages are indicated by colored triangles, with the base width of each triangle proportional to the sample size. A detailed, time-stamped phylogenetic tree is presented in supplementary fig. S1, Supplementary Material online, with scales of divergence times differentiated by varying background colors.

**Fig. 2.**
Maximum likelihood phylogenetic tree among modern and ancient Eurasian populations. This tree includes newly genotyped individuals from Chinese ethnic minorities and ancient Eurasian reference populations. The colored regions on the map signify the sampling locations of both ancient and modern Eurasian populations, with black triangles marking the sites where ancient Eurasian samples were collected. The branch lengths are proportional to the mutation counts, and the branch colors indicate the sampling locations, with solid lines representing modern individuals and dashed lines depicting ancient individuals. Inside the circle, different shapes and colors denote the language families of modern individuals: rosy for Sinitic; dark goldenrod for Tibeto-Burman; bluish violet for Mongolic; brown for Tungusic; gray for Turkic; lavender for Koreanic; green for Tai-Kadai; and medium sea green for Hmong-Mien. Due to the small sample sizes (fewer than five), Austronesian, Austroasiatic, and Indo-European-speaking populations are not labeled. The outer circle displays sample information and corresponding haplogroup results, with violet representing modern individuals and light blue for ancient ones. Enlargements of dominant lineages and their representative ancient genomes are highlighted at the four corners of the map. Detailed views of these branches are provided in supplementary figs. S9 to S12, Supplementary Material online.

**Fig. 3.**
Frequency spectrum of dominant Chinese paternal lineages in ancient Eurasians and modern East and Southeast Asians. a) The geographic distribution of 1,284 ancient individuals carrying 12 Y-chromosome lineages is depicted. Various haplogroups are represented by circles of different colors, with the size of each circle proportional to the frequency of the corresponding haplogroups. b and c) Frequencies of paternal lineages related to Western-origin and Siberian hunter-gatherers among eastern Eurasian populations are shown. Optimized hot spot analysis was employed to suggest the geographic origins of these focused lineages. d and e) Frequencies of sublineages associated with early East Asian-related D, ANEA millet farmer-related O2, and ancient Southern East Asian rice farmer-related O1 are displayed. Areas with high frequencies or significant phylogeographic relevance of the studied lineages are highlighted in hot red. Detailed frequency distributions of additional sublineages are provided in supplementary figs. S13 and S16 to S18, Supplementary Material online.

**Fig. 4.**
Admixture results and geographic distribution of ancestral sources. a) Model-based ADMIXTURE analysis was performed for modern and ancient East Asian populations using predefined ancestral sources ranging from 2 to 15. The optimal fit was achieved with a six-way admixture model, which exhibited the lowest cross-validation error. b to g) The distribution of admixture proportions across various Chinese populations is depicted, with red indicating the highest proportion of a specific ancestral component.

**Fig. 5.**
Correlation between the autosomal ancestral proportions and the frequencies of the Y-chromosome lineages. a to f) Scatter plots display statistically significant positive correlations between autosomal-based ancestral proportions and population-specific founding paternal lineages. g) Correlations between autosomal-based admixture estimates of ancestral proportions and frequencies of paternal lineages are shown. Correlations involving proportions of different ancestral sources were excluded, and the initial clustering positions of these correlations are marked with arrows. This visual analysis elucidates the complex interplay between autosomal and Y-chromosomal data in tracing genetic heritage and lineage dynamics.

See this image and copyright information in PMC

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Multiple Human Population Movements and Cultural Dispersal Events Shaped the Landscape of Chinese Paternal Heritage

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Multiple Human Population Movements and Cultural Dispersal Events Shaped the Landscape of Chinese Paternal Heritage

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