courses-img1News
New Collaborator Announcement for the journal Synthetic Biology a New Collaborator Announcement for the journal Clean Energy and Su The 15th Edition of International Conference on Catalysis, Chemic Glance of 2021 Nobel Prizes SCIEPublish Open Beta
Login In Sign Up Submit

Journals Article Details

Nature Anthropology-logo
Submit to Nat. Anthropol.
Article Open Access

Fine-scale Genetic Structure of Geographically Distinct Patrilineal Lineages Delineates Southward Migration Routes for Han Chinese

Nature Anthropology. 2023, 1(1), 10004; https://doi.org/10.35534/natanthropol.2023.10004
Yichen Tao 1, 2,    Juanjuan Zhou 3,    Letong Liang 1,    Edward Allen 4,    Yetao Zou 5,    Zishuai Huang 1,    Hui Li 3, 5, 6, *   
1
State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, China
2
Greater Bay Area Institute of Precision Medicine (Guangzhou), Fudan University, Nansha District, Guangzhou 511458, China
3
MOE Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, China
4
Department of Cultural Heritage and Museology, Fudan University, Shanghai 200438, China
5
Human Phenome Institute, Fudan University, Shanghai 200438, China
6
Fudan-Datong Institute of Chinese Origin, Datong 037006, China
*
Authors to whom correspondence should be addressed.

Received: 25 Apr 2023    Accepted: 11 Jul 2023    Published: 20 Jul 2023   

Full-Text HTML Full-Text PDF Download PDF Supplementary Download

Abstract

The Han Chinese (HAN) represent the world’s largest ethnic group, and their genetic structure has been the focus of numerous studies. Yet previous studies failed to draw out finer population stratification of patrilineal HAN, due to limitations in sample size and genetic marker density. This essay employs a Y-haplogroup frequency dataset from virtually whole China aiming to draw out a detailed genetic structure of the patrilineal HAN. We provide an overview of the Y chromosome haplogroup distributions, and find that the patrilineal HAN can be divided into five geographic subgroups. Analysis of Molecular Variance (AMOVA) provided further support for the five-substructure model. By comparing patrilineal and matrilineal descent, we revealed stronger geographical aggregation for patrilineal HAN. Moreover, populations with patrilineal descent showed lower levels of haplogroup diversity (HD) compared to those with matrilineal descent, suggesting potential population bottleneck of patrilineal HAN. The larger HD among northern patrilines verified historical migration of HAN from north to south, which validated by neighbor joining tree (NJ-tree). Overall, we speculate the southward migration routes for Han Chinese, and the HAN south of the Nanling Mountains may have entered via the middle reaches of the Yangtze River, rather than via eastern coastal provinces.

Keywords

Y chromosome haplogroup; Han Chinese; Population genetics; Genetic structure; Sex bias

References

1.
Fatumo S, Chikowore T, Choudhury A, Ayub M, Martin AR, Kuchenbaecker K. A roadmap to increase diversity in genomic studies.  Nat. Med. 2022, 28, 243–250. [Google Scholar]
2.
Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, et al. A global reference for human genetic variation.  Nature 2015, 526, 68–74. [Google Scholar]
3.
Fairley S, Lowy-Gallego E, Perry E, Flicek P. The International Genome Sample Resource (IGSR) collection of open human genomic variation resources.  Nucleic Acids Res. 2020, 48, D941–D947. [Google Scholar]
4.
Xue FH, Wang Y, Xu SH, Zhang F, Wen B, Wu XS, et al. A spatial analysis of genetic structure of human populations in China reveals distinct difference between maternal and paternal lineages.  Eur. J. Hum. Genet. 2008, 16, 705–717. [Google Scholar]
5.
Xue Y, Zerjal T, Bao W, Zhu S, Shu Q, Xu J, et al. Male demography in East Asia: a north-south contrast in human population expansion times.  Genetics 2006, 172, 2431–2439. [Google Scholar]
6.
Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, et al. Genetic Structure of Human Populations.  Science 2002, 298, 2381–2385. [Google Scholar]
7.
Ma X, Yang W, Gao Y, Pan Y, Lu Y, Chen H, et al. Genetic Origins and Sex-Biased Admixture of the Huis.  Mol. Biol. Evol. 2021, 38, 3804–3819. [Google Scholar]
8.
Pan Y, Wen J, Ning Z, Yuan Y, Liu X, Yang Y, et al. Comparative Genomic and Transcriptomic Analyses Reveal the Impacts of Genetic Admixture in Kazaks, Uyghurs, and Huis.  Mol. Biol. Evol. 2023, 40, msad054. [Google Scholar]
9.
Yin C, Su K, He Z, Zhai D, Guo K, Chen X, et al. Genetic Reconstruction and Forensic Analysis of Chinese Shandong and Yunnan Han Populations by Co-Analyzing Y Chromosomal STRs and SNPs.  Genes 2020, 11, 743. [Google Scholar]
10.
Yao H, Wang M, Zou X, Li Y, Yang X, Li A, et al. New insights into the fine-scale history of western-eastern admixture of the northwestern Chinese population in the Hexi Corridor via genome-wide genetic legacy.  Mol. Genet. Genom. 2021, 296, 631–651. [Google Scholar]
11.
Li YC, Ye WJ, Jiang CG, Zeng Z, Tian JY, Yang LQ, et al. River Valleys Shaped the Maternal Genetic Landscape of Han Chinese.  Mol. Biol. Evol. 2019, 36, 1643–1652. [Google Scholar]
12.
Xu S, Yin X, Li S, Jin W, Lou H, Yang L, et al. Genomic dissection of population substructure of Han Chinese and its implication in association studies. Am. J. Hum. Genet. 2009, 85, 762–774. [Google Scholar]
13.
Chiang CWK, Mangul S, Robles C, Sankararaman S. A Comprehensive Map of Genetic Variation in the World’s Largest Ethnic Group-Han Chinese.  Mol. Biol. Evol. 2018, 35, 2736–2750. [Google Scholar]
14.
Gao Y, Zhang C, Yuan L, Ling Y, Wang X, Liu C, et al. PGG.Han: the Han Chinese genome database and analysis platform.  Nucleic Acids Res. 2020, 48, D971–D976. [Google Scholar]
15.
Li L, Huang P, Sun X, Wang S, Xu M, Liu S, et al. The ChinaMAP reference panel for the accurate genotype imputation in Chinese populations.  Cell Res. 2021, 31, 1308–1310. [Google Scholar]
16.
Cong PK, Bai WY, Li JC, Yang MY, Khederzadeh S, Gai SR, et al. Genomic analyses of 10,376 individuals in the Westlake BioBank for Chinese (WBBC) pilot project.  Nat. Commun. 2022, 13, 2939. [Google Scholar]
17.
Chu JY, Huang W, Kuang SQ, Wang JM, Xu JJ, Chu ZT, et al. Genetic relationship of populations in China.  Proc. Natl. Acad. Sci. USA 1998, 95, 11763–11768. [Google Scholar]
18.
Wen B, Li H, Lu D, Song X, Zhang F, He Y, et al. Genetic evidence supports demic diffusion of Han culture.  Nature 2004, 431, 302–305. [Google Scholar]
19.
Sul JH, Martin LS, Eskin E. Population structure in genetic studies: Confounding factors and mixed models.  PLoS Genet. 2018, 14, e1007309. [Google Scholar]
20.
Yan S, Wang C-C, Zheng H-X, Wang W, Qin Z-D, Wei L-H, et al. Y Chromosomes of 40% Chinese Descend from Three Neolithic Super-Grandfathers.  PLoS ONE 2014, 9, e105691. [Google Scholar]
21.
Sun N, Ma PC, Yan S, Wen SQ, Sun C, Du PX, et al. Phylogeography of Y-chromosome haplogroup Q1a1a-M120, a paternal lineage connecting populations in Siberia and East Asia.  Ann. Hum. Biol. 2019, 46, 261–266. [Google Scholar]
22.
Wang L-X, Lu Y, Zhang C, Wei L-H, Yan S, Huang Y-Z, et al. Reconstruction of Y-chromosome phylogeny reveals two neolithic expansions of Tibeto-Burman populations.  Mol. Genet. Genom. 2018, 293, 1293–1300. [Google Scholar]
23.
Lu Q, Cheng HZ, Li L, Yao HB, Ru K, Wen SQ, et al. Paternal heritage of the Han Chinese in Henan province (Central China): high diversity and evidence of in situ Neolithic expansions.  Ann. Hum. Biol. 2020, 47, 294–299. [Google Scholar]
24.
Wang C-C, Yan S, Qin Z-D, Lu Y, Ding Q-L, Wei L-H, et al. Late Neolithic expansion of ancient Chinese revealed by Y chromosome haplogroup O3a1c-002611.  J. Syst. Evol. 2013, 51, 280–286. [Google Scholar]
25.
Zhong H, Shi H, Qi XB, Xiao CJ, Jin L, Ma RZ, et al. Global distribution of Y-chromosome haplogroup C reveals the prehistoric migration routes of African exodus and early settlement in East Asia.  J. Hum. Genet. 2010, 55, 428–435. [Google Scholar]
26.
Shi H, Zhong H, Peng Y, Dong YL, Qi XB, Zhang F, et al. Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations.  BMC Biol. 2008, 6, 45. [Google Scholar]
27.
Xue Y, Zerjal T, Bao W, Zhu S, Shu Q, Xu J, et al. Male demography in East Asia: a north-south contrast in human population expansion times.  Genetics 2006, 172, 2431–2439. [Google Scholar]
28.
Cai X, Qin Z, Wen B, Xu S, Wang Y, et al. Human migration through bottlenecks from Southeast Asia into East Asia during Last Glacial Maximum revealed by Y chromosomes.  PLoS ONE 2011, 6, e24282. [Google Scholar]
29.
Al-Zahery N, Pala M, Battaglia V, Grugni V, Hamod MA, Hooshiar Kashani B, et al. In search of the genetic footprints of Sumerians: a survey of Y-chromosome and mtDNA variation in the Marsh Arabs of Iraq.  BMC Evol. Biol. 2011, 11, 288. [Google Scholar]
30.
Di Cristofaro J, Pennarun E, Mazières S, Myres NM, Lin AA, Temori SA, et al. Afghan Hindu Kush: where Eurasian sub-continent gene flows converge.  PLoS ONE 2013, 8, e76748. [Google Scholar]
31.
Dudás E, Vágó-Zalán A, Vándor A, Saypasheva A, Pomozi P, Pamjav H. Genetic history of Bashkirian Mari and Southern Mansi ethnic groups in the Ural region.  Mol. Genet. Genom. 2019, 294, 919–930. [Google Scholar]
32.
Dulik MC, Osipova LP, Schurr TG. Y-chromosome variation in Altaian Kazakhs reveals a common paternal gene pool for Kazakhs and the influence of Mongolian expansions.  PLoS ONE 2011, 6, e17548. [Google Scholar]
33.
Dulik MC, Zhadanov SI, Osipova LP, Askapuli A, Gau L, Gokcumen O, et al. Mitochondrial DNA and Y chromosome variation provides evidence for a recent common ancestry between Native Americans and Indigenous Altaians.  Am. J. Hum. Genet. 2012, 90, 229–246. [Google Scholar]
34.
Karafet TM, Osipova LP, Savina OV, Hallmark B, Hammer MF. Siberian genetic diversity reveals complex origins of the Samoyedic-speaking populations.  Am. J. Hum. Biol. 2018, 30, e23194. [Google Scholar]
35.
Khar’kov VN, Khamina KV, Medvedeva OF, Shtygasheva OV, Stepanov VA. Genetic diversity of Khakassian gene pool: subethnic differensiation and the structure of Y-chromosome haplogroups.  Mol. Biol. (Mosk.) 2011, 45, 446–458. [Google Scholar]
36.
Khar’kov VN, Medvedeva OF, Luzina FA, Kolbasko AV, Gafarov NI, Puzyrev VP, et al. Comparative characteristics of the gene pool of Teleuts inferred from Y-chromosomal marker data.  Genetika 2009, 45, 1132–1142. [Google Scholar]
37.
Kutanan W, Shoocongdej R, Srikummool M, Hübner A, Suttipai T, Srithawong S, et al. Cultural variation impacts paternal and maternal genetic lineages of the Hmong-Mien and Sino-Tibetan groups from Thailand.  Eur. J. Hum. Genet. 2020, 28, 1563–1579. [Google Scholar]
38.
Lang M, Liu H, Song F, Qiao X, Ye Y, Ren H, et al. Forensic characteristics and genetic analysis of both 27 Y-STRs and 143 Y-SNPs in Eastern Han Chinese population.  Forens. Sci. Int. Genet. 2019, 42, e13–e20. [Google Scholar]
39.
Pamjav H, Fothi A, Feher T, Fothi E. A study of the Bodrogkoz population in north-eastern Hungary by Y chromosomal haplotypes and haplogroups.  Mol. Genet. Genom. 2017, 292, 883–894. [Google Scholar]
40.
Pankratov V, Litvinov S, Kassian A, Shulhin D, Tchebotarev L, Yunusbayev B, et al. East Eurasian ancestry in the middle of Europe: genetic footprints of Steppe nomads in the genomes of Belarusian Lipka Tatars.  Sci. Rep. 2016, 6, 30197. [Google Scholar]
41.
Pimenoff VN, Comas D, Palo JU, Vershubsky G, Kozlov A, Sajantila A. Northwest Siberian Khanty and Mansi in the junction of West and East Eurasian gene pools as revealed by uniparental markers.  Eur. J. Hum. Genet. 2008, 16, 1254–1264. [Google Scholar]
42.
Qi X, Cui C, Peng Y, Zhang X, Yang Z, Zhong H, et al. Genetic evidence of paleolithic colonization and neolithic expansion of modern humans on the tibetan plateau.  Mol. Biol. Evol. 2013, 30, 1761–1778. [Google Scholar]
43.
Rowold DJ, Gayden T, Luis JR, Alfonso-Sanchez MA, Garcia-Bertrand R, Herrera RJ.  Investigating the genetic diversity and affinities of historical populations of Tibet.  Gene 2019, 682, 81–91. [Google Scholar]
44.
Song M, Wang Z, Zhang Y, Zhao C, Lang M, Xie M, et al. Forensic characteristics and phylogenetic analysis of both Y-STR and Y-SNP in the Li and Han ethnic groups from Hainan Island of China.  Forens. Sci. Int. Genet. 2019, 39, e14–e20. [Google Scholar]
45.
Wang CC, Wang LX, Shrestha R, Zhang M, Huang XY, Hu K, et al. Genetic structure of Qiangic populations residing in the western Sichuan corridor.  PLoS ONE 2014, 9, e103772. [Google Scholar]
46.
Wang M, He G, Zou X, Liu J, Ye Z, Ming T, et al. Genetic insights into the paternal admixture history of Chinese Mongolians via high-resolution customized Y-SNP SNaPshot panels.  Forens. Sci. Int. Genet. 2021, 54, 102565. [Google Scholar]
47.
Wen SQ, Du PX, Sun C, Cui W, Xu YR, Meng HL, et al. Dual origins of the Northwest Chinese Kyrgyz: the admixture of Bronze age Siberian and Medieval Niru’un Mongolian Y chromosomes.  J. Hum. Genet. 2022, 67, 175–180. [Google Scholar]
48.
Wen SQ, Sun C, Song DL, Huang YZ, Tong XZ, Meng HL, et al. Y-chromosome evidence confirmed the Kerei-Abakh origin of Aksay Kazakhs.  J. Hum. Genet. 2020, 65, 797–803. [Google Scholar]
49.
Xie M, Song F, Li J, Lang M, Luo H, Wang Z, et al. Genetic substructure and forensic characteristics of Chinese Hui populations using 157 Y-SNPs and 27 Y-STRs.  Forens. Sci. Int. Genet. 2019, 41, 11–18. [Google Scholar]
50.
Zhabagin M, Balanovska E, Sabitov Z, Kuznetsova M, Agdzhoyan A, Balaganskaya O, et al. The Connection of the Genetic, Cultural and Geographic Landscapes of Transoxiana.  Sci. Rep. 2017, 7, 3085. [Google Scholar]
51.
Zhang D, Cao G, Xie M, Cui X, Xiao L, Tian C, et al. RETRACTED ARTICLE: Y Chromosomal STR haplotypes in Chinese Uyghur, Kazakh and Hui ethnic groups and genetic features of DYS448 null allele and DYS19 duplicated allele.  Int. J. Leg. Med. 2021, 135, 1119. [Google Scholar]
52.
Zhang Y, Zhang R, Li M, Luo L, Zhang J, Ding J, et al. Genetic polymorphism of both 29 Y-STRs and 213 Y-SNPs in Han populations from Shandong Province, China. Leg. Med. (Tokyo) 2020, 47, 101738. [Google Scholar]
53.
Nei M, Tajima F. DNA polymorphism detectable by restriction endonucleases.  Genetics 1981, 97, 145–163. [Google Scholar]
Creative Commons

© 2023 by the authors; licensee SCIEPublish, SCISCAN co. Ltd. This article is an open access article distributed under the CC BY license (http://creativecommons.org/licenses/by/4.0/).