Paleolithic divergence and multiple Neolithic expansions of ancestral nomadic emperor-related paternal lineages

Mengge Wang; Qiuxia Sun; Yuhang Feng; Lan-Hai Wei; Kaijun Liu; Lintao Luo; Yuguo Huang; Kun Zhou; Haibing Yuan; Hongliang Lv; Yu Lu; Jing Cheng; Shaoqing Wen; Chuan-Chao Wang; Renkuan Tang; Fengxiao Bu; Chao Liu; Huijun Yuan; Zhiyong Wang; Guanglin He

doi:10.1016/j.jgg.2024.11.012

Volume 52 Issue 4

Apr. 2025

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2025 > 52(4): 502-512

PDF( 0 KB)

Paleolithic divergence and multiple Neolithic expansions of ancestral nomadic emperor-related paternal lineages

doi: 10.1016/j.jgg.2024.11.012

a. Institute of Rare Diseases, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University, Chengdu, Sichuan 610000, China;
b. Center for Archaeological Science, Sichuan University, Chengdu, Sichuan 610000, China;
c. Anti-Drug Technology Center of Guangdong Province, Guangzhou, Guangdong 510230, China;
d. Department of Forensic Medicine, College of Basic Medicine, Chongqing Medical University, Chongqing 400331, China;
e. Human Genetics and Forensic Genomics Research Institute, College of Basic Medicine, Chongqing Medical University, Chongqing 400331, China;
f. Institute of Humanities and Human Sciences, Inner Mongolia Normal University, Hohhot, Inner Mongolia 010022, China;
g. Institute of 23Mofang, Tianfu Software Park, Chengdu, Sichuan 610042, China;
h. MOE Laboratory for National Development and Intelligent Governance, Fudan University, Shanghai 200433, China;
i. State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, China

Funds:

We acknowledge the financial support received from the National Natural Science Foundation of China (82202078) for M.W. and from the National Social Science Foundation of China (23&ZD203) for G.H. Additional support for G.H. includes National Natural Science Foundation of China (82402203), the Open Project of the Key Laboratory of Forensic Genetics of the Ministry of Public Security (2022FGKFKT05), the Center for Archaeological Science of Sichuan University (23SASA01), the 1·3·5 Project for Disciplines of Excellence at West China Hospital, Sichuan University (ZYJC20002), and the Sichuan Science and Technology Program (2024NSFSC1518).

Received Date: 2024-06-11
Accepted Date: 2024-11-20
Rev Recd Date: 2024-11-17

Available Online: 2025-07-11

Publish Date: 2025-04-28

Abstract

Abstract

The reconstruction of demographic history using ancient and modern genomic resources reveals extensive interactions and admixture between ancient nomadic pastoralists and the social organizations of the Chinese Central Plain. However, the extent to which Y-chromosome genetic legacies from nomadic emperor-related ancestral lineages influence the Chinese paternal gene pool remains unclear. Here, we genotype 2717 ethnolinguistically diverse samples belonging to C2a lineages, perform whole-genome sequencing on 997 representative samples, and integrate these data with ancient genomic sequences. We reconstruct the evolutionary histories of Northern Zhou-, Qing emperor-, and pastoralist-related lineages to assess their genetic impact on modern Chinese populations. This reassembled fine-scale Y-chromosome phylogeny identifies deep divergence and five Neolithic expansion events contributing differently to the formation of northern Chinese populations. Phylogeographic modeling indicates that the nomadic empires of the Northern Zhou and Qing dynasties genetically originated from the Mongolian Plateau. Phylogenetic topology and shared haplotype patterns show that three upstream ancestors of Northern Zhou (C2a1a1b1a2a1b-FGC28857), Donghu tribe (C2a1a1b1-F1756), and Qing (C2a1a3a2-F10283) emperor-related lineages expanded during the middle Neolithic, contributing significantly to genetic flow between ancient northeastern Asians and modern East Asians. Notably, this study reveals limited direct contributions of Emperor Wu of Northern Zhou's lineages to modern East Asians.
- Paternal lineage,
- Founding lineage,
- Genetic origin,
- Emperor lineage,
- Y-chromosome

FullText(HTML)

References(47)

References

Bergstrom, A., McCarthy, S.A., Hui, R., Almarri, M.A., Ayub, Q., Danecek, P., Chen, Y., Felkel, S., Hallast, P.,Kamm, J., 2020. Insights into human genetic variation and population history from 929 diverse genomes. Science 367, eaay5012.

Cao, Y.N., Li, L., Xu, M., Feng, Z.M., Sun, X.H., Lu, J.L., Xu, Y., Du, P.N., Wang, T.G., Hu, R.Y., et al., 2020. The chinamap analytics of deep whole genome sequences in 10,588 individuals. Cell Res. 30, 717-731.

Chen, H., Lu, Y., Lu, D.,Xu, S., 2021a. Y-lineagetracker: a high-throughput analysis framework for y-chromosomal next-generation sequencing data. BMC Bioinf. 22, 114.

Chen, T., Chen, X., Zhang, S., Zhu, J., Tang, B., Wang, A., Dong, L., Zhang, Z., Yu, C.,Sun, Y., 2021b. The genome sequence archive family: toward explosive data growth and diverse data types. Dev. Reprod. Biol. 19, 578-583.

Darriba, D., Taboada, G., Doallo, R.,Posada, D., 2012. Jmodeltest 2: more models, new heuristics and parallel computing. Nat meth 9: 772. (Go to original source Go to PubMed).

Du, P., Zhu, K., Qiao, H., Zhang, J., Meng, H., Huang, Z., Yu, Y., Xie, S., Allen, E., Xiong, J., et al., 2024. Ancient genome of the Chinese emperor Wu of northern zhou. Curr. Biol. 34, 1587-1595.e1585.

Forster, P., Harding, R., Torroni, A.,Bandelt, H.-J., 1996. Origin and evolution of native american mtdna variation: a reappraisal. Am. J. Hum. Genet. 59, 935.

Francalacci, P., Morelli, L., Angius, A., Berutti, R., Reinier, F., Atzeni, R., Pilu, R., Busonero, F., Maschio, A., Zara, I., et al., 2013. Low-pass DNA sequencing of 1200 sardinians reconstructs european y-chromosome phylogeny. Science 341, 565-569.

Fu, Q.M., Li, H., Moorjani, P., Jay, F., Slepchenko, S.M., Bondarev, A.A., Johnson, P.L.F., Aximu-Petri, A., Prufer, K., de Filippo, C., et al., 2014. Genome sequence of a 45,000-year-old modern human from western siberia. Nature 514, 445-+.

Guyon, L., Guez, J., Toupance, B., Heyer, E.,Chaix, R., 2024. Patrilineal segmentary systems provide a peaceful explanation for the post-neolithic y-chromosome bottleneck. Nat. Commun. 15, 3243.

He, G., Wang, M., Luo, L., Sun, Q., Yuan, H., Lv, H., Feng, Y., Liu, X., Cheng, J., Bu, F., et al., 2024a. Population genomics of central asian peoples unveil ancient trans-eurasian genetic admixture and cultural exchanges. hLife.

He, G., Wang, P., Chen, J., Liu, Y., Sun, Y., Hu, R., Duan, S., Sun, Q., Tang, R., Yang, J., et al., 2024b. Differentiated genomic footprints suggest isolation and long-distance migration of Hmong-mien populations. BMC Biol. 22, 18.

Jagadeesan, A., Ebenesersdottir, S.S., Gudhmundsdottir, V.B., Thordardottir, E.L., Moore, K.H.,Helgason, A., 2021. Haplogrouper: a generalized approach to haplogroup classification. Bioinformatics 37, 570-572.

Jeong, C., Wang, K., Wilkin, S., Taylor, W.T.T., Miller, B.K., Bemmann, J.H., Stahl, R., Chiovelli, C., Knolle, F., Ulziibayar, S., et al., 2020. A dynamic 6,000-year genetic history of eurasia's eastern steppe. Cell 183, 890-904 e829.

Ji, H., Chen, J., Huang, P., Feng, Z., Hu, W., Dai, M., Sun, X., Jin, X., Chen, G., Ning, G., et al., 2023. Multi-omics analyses of g6pd deficiency variants in Chinese population. J Genet Genomics.

Karmin, M., Flores, R., Saag, L., Hudjashov, G., Brucato, N., Crenna-Darusallam, C., Larena, M., Endicott, P.L., Jakobsson, M., Lansing, J.S., et al., 2022. Episodes of diversification and isolation in island southeast asian and near oceanian male lineages. Mol. Biol. Evol. 39, msac045.

Karmin, M., Saag, L., Vicente, M., Wilson Sayres, M.A., Jarve, M., Talas, U.G., Rootsi, S., Ilumae, A.M., Magi, R., Mitt, M., et al., 2015. A recent bottleneck of y chromosome diversity coincides with a global change in culture. Genome Res. 25, 459-466.

Letunic, I.,Bork, P., 2024. Interactive tree of life (itol) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res., gkae268.

Li, H., 2013. Aligning sequence reads, clone sequences and assembly contigs with bwa-mem. arXiv preprint arXiv:13033997.

Li, X., Wang, M., Su, H., Duan, S., Sun, Y., Chen, H., Wang, Z., Sun, Q., Yang, Q., Chen, J., et al., 2024. Evolutionary history and biological adaptation of han Chinese people on the Mongolian plateau. hLife 2, 296-313.

Liu, Y., Wang, T., Wu, X., Fan, X., Wang, W., Xie, G., Li, Z., Yang, Q., Cao, P., Yang, R., et al., 2021. Maternal genetic history of southern east asians over the past 12,000 years. J Genet Genomics 48, 899-907.

Luo, L., Wang, M., Liu, Y., Li, J., Bu, F., Yuan, H., Tang, R., Liu, C.,He, G., 2024. Sequencing and characterizing human mitochondrial genomes in the biobankbased genomic research paradigm. Sci. China Life Sci.

Mao, X.W., Zhang, H.C., Qiao, S.Y., Liu, Y.C., Chang, F.Q., Xie, P., Zhang, M., Wang, T.Y., Li, M.A., Cao, P., et al., 2021. The deep population history of northern east asia from the late pleistocene to the holocene. Cell 184, 3256-+.

Martiniano, R., De Sanctis, B., Hallast, P.,Durbin, R., 2022. Placing ancient DNA sequences into reference phylogenies. Mol. Biol. Evol. 39.

McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S.,Daly, M., 2010. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.

Miao, B., Liu, Y., Gu, W., Wei, Q., Wu, Q., Wang, W., Zhang, M., Ding, M., Wang, T., Liu, J., et al., 2021. Maternal genetic structure of a neolithic population of the yangshao culture. J Genet Genomics 48, 746-750.

Nei, M.,Li, W.-H., 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76, 5269-5273.

Ning, C., Li, T., Wang, K., Zhang, F., Li, T., Wu, X., Gao, S., Zhang, Q., Zhang, H.,Hudson, M.J., 2020. Ancient genomes from northern China suggest links between subsistence changes and human migration. Nat. Commun. 11, 2700.

Pinotti, T., Bergstrom, A., Geppert, M., Bawn, M., Ohasi, D., Shi, W., Lacerda, D.R., Solli, A., Norstedt, J., Reed, K., et al., 2019. Y chromosome sequences reveal a short beringian standstill, rapid expansion, and early population structure of native american founders. Curr. Biol. 29, 149-157 e143.

Poznik, G.D., Henn, B.M., Yee, M.C., Sliwerska, E., Euskirchen, G.M., Lin, A.A., Snyder, M., Quintana-Murci, L., Kidd, J.M., Underhill, P.A., et al., 2013. Sequencing y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341, 562-565.

Poznik, G.D., Xue, Y., Mendez, F.L., Willems, T.F., Massaia, A., Wilson Sayres, M.A., Ayub, Q., McCarthy, S.A., Narechania, A., Kashin, S., et al., 2016. Punctuated bursts in human male demography inferred from 1,244 worldwide y-chromosome sequences. Nat. Genet. 48, 593-599.

Stamatakis, A., 2014. Raxml version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.

Sun, Q., Wang, M., Lu, T., Duan, S., Liu, Y., Chen, J., Wang, Z., Sun, Y., Li, X., Wang, S., et al., 2024a. Differentiated adaptative genetic architecture and language-related demographical history in south China inferred from 619 genomes from 56 populations. BMC Biol. 22, 55.

Sun, Y., Wang, M., Sun, Q., Liu, Y., Duan, S., Wang, Z., Zhou, Y., Zhong, J., Huang, Y., Huang, X., et al., 2024b. Distinguished biological adaptation architecture aggravated population differentiation of tibeto-burman-speaking people. J Genet Genomics 51, 517-530.

Wang, C.-Z., Wei, L.-H., Wang, L.-X., Wen, S.-Q., Yu, X.-E., Shi, M.-S.,Li, H., 2019. Relating clans ao and aisin gioro from northeast China by whole y-chromosome sequencing. J. Hum. Genet. 64, 775-780.

Wang, C.C., Yeh, H.Y., Popov, A.N., Zhang, H.Q., Matsumura, H., Sirak, K., Cheronet, O., Kovalev, A., Rohland, N., Kim, A.M., et al., 2021a. Genomic insights into the formation of human populations in east asia. Nature 591, 413-+.

Wang, M., Chen, H., Luo, L., Huang, Y., Duan, S., Yuan, H., Tang, R., Liu, C.,He, G., 2024a. Forensic investigative genetic genealogy: expanding pedigree tracing and genetic inquiry in the genomic era. J Genet Genomics.

Wang, M., Huang, Y., Liu, K., Wang, Z., Zhang, M., Yuan, H., Duan, S., Wei, L., Yao, H.,Sun, Q., 2024b. Multiple human population movements and cultural dispersal events shaped the landscape of Chinese paternal heritage. Mol. Biol. Evol. 41, msae122.

Wang, M., Yao, H., Sun, Q., Duan, S., Tang, R., Chen, J., Wang, Z., Sun, Y., Li, X., Wang, S., et al., 2024c. Pilot work of the 10k Chinese people genomic diversity project along the silk road suggests a complex east-west admixture landscape and biological adaptations. Sci. China Life Sci., 2023.2002.2026.530053.

Wang, T.Y., Wang, W., Xie, G.M., Li, Z., Fan, X.C., Yang, Q.P., Wu, X.C., Cao, P., Liu, Y.C., Yang, R.W., et al., 2021b. Human population history at the crossroads of east and southeast asia since 11,000 years ago. Cell 184, 3829-+.

Wang, Z., Wang, M., Liu, K., Yuan, H., Duan, S., Liu, Y., Luo, L., Jiang, X., Chen, S., Wei, L., et al., 2023. Paternal genomic resources from the YanHuang cohort suggested a Weakly-Differentiated Multi-source Admixture model for the formation of Han’s founding ancestral lineages. bioRxiv. https://doi.org/10.1101/2023.11.08.566335.

Wei, L.-H., Huang, Y.-Z., Yan, S., Wen, S.-Q., Wang, L.-X., Du, P.-X., Yao, D.-L., Li, S.-L., Yang, Y.-J.,Jin, L., 2017a. Phylogeny of y-chromosome haplogroup c3b-f1756, an important paternal lineage in altaic-speaking populations. J. Hum. Genet. 62, 915-918.

Wen, S.-Q., Yao, H.-B., Du, P.-X., Wei, L.-H., Tong, X.-Z., Wang, L.-X., Wang, C.-C., Zhou, B.-Y., Shi, M.-S.,Zhabagin, M., 2019. Molecular genealogy of tusi lu's family reveals their paternal relationship with jochi, genghis khan's eldest son. J. Hum. Genet. 64, 815-820.

Yang, M.A., Fan, X.C., Sun, B., Chen, C.Y., Lang, J.F., Ko, Y.C., Tsang, C.H., Chiu, H.L., Wang, T.Y., Bao, Q.C., et al., 2020. Ancient DNA indicates human population shifts and admixture in northern and southern China. Science 369, 282-+.

Zeng, T.C., Aw, A.J.,Feldman, M.W., 2018. Cultural hitchhiking and competition between patrilineal kin groups explain the post-neolithic y-chromosome bottleneck. Nat. Commun. 9, 2077.

Zhang, G., Cui, C., Wangdue, S., Lu, H., Chen, H., Xi, L., He, W., Yuan, H., Tsring, T., Chen, Z., et al., 2023. Maternal genetic history of ancient tibetans over the past 4,000 years. J Genet Genomics.

Zhou, T., Xu, K., Zhao, F., Liu, W., Li, L., Hua, Z.,Zhou, X., 2023. Itol. Toolkit accelerates working with itol (interactive tree of life) by an automated generation of annotation files. Bioinformatics 39, btad339.

Relative Articles

Supplements(0)

Cited By

Proportional views