5.9
CiteScore
5.9
Impact Factor
Turn off MathJax
Article Contents

Ancient mitochondrial genome depicts sheep maternal dispersal and migration in eastern Asia

doi: 10.1016/j.jgg.2023.06.002
Funds:  We express sincere thanks to Prof. Jing Yuan (Institute of Archaeology, Chinese Academy of Social Science) for generously providing the ancient samples. This work was funded by the National Key Research and Development Program of China (2021YFF1000701), the Young S&T Talent Training Program of Guangdong Provincial Association for S&T, China (SKXRC202205), the Foundation for the Creative Team and Key Laboratory in Higher Education of Guangdong (2019KCXTD006 and 2019KSYS011), and the National Natural Science Foundations of China (31961133031).
  • Received Date: 2023-04-22
  • Revised Date: 2023-05-20
  • Accepted Date: 2023-06-05
  • Available Online: 2023-06-15
  • Sheep have been one of the most important groups of animals since ancient times. However, the knowledge of their migration routes and genetic relationships is still poorly understood. To investigate sheep maternal migration histories alongside Eurasian communications routes, in this study, we obtain mitochondrial genomes (mitogenomes) from 17 sheep remains in 6 Chinese sites and 1 Uzbekistan site dated 4429–3100 years before present (BP). By obtaining the mitogenomes from the sheep (4429–3556 years old) found in Tongtian Cave site in Xinjiang, Altai region of northwest China, our results support the emergence of haplogroup C sheep in Xinjiang as early as 4429–3556 BP. The combined phylogenetic analyses with extant ancient and modern sheep mitogenomes suggest that the Uzbekistan-Altai region might have been a migration hub for early sheep in eastern Asia. At least two migration events have taken place for sheep crossing Eurasia to China, one passing by Uzbekistan and Northwest China to the middle and lower reaches of the Yellow River at approximately 4000 BP and another following the Altai region to middle Inner Mongolia from 4429–2500 BP. Overall, this study provides further evidence for early sheep utilization and migration patterns in eastern Asia.
  • loading
  • [1]
    Atag, G., Vural, K. B., Kaptan, D., Ozkan, M., Koptekin, D., Saglican, E., Dogramaci, S., Koz, M., Yilmaz, A., Soylev, A., 2022. MTaxi: A comparative tool for taxon identification of ultra low coverage ancient genomes [version 1; peer review: 1 approved]. Open Research Europe 2, 1-17.
    [2]
    Atti, N., Bocquier, F., Khaldi, G., 2004. Performance of the fat-tailed Barbarine sheep in its environment: adaptive capacity to alternation of underfeeding and re-feeding periods. A review. Anim. Res. 53, 165-176.
    [3]
    Barbato, M., Hailer, F., Orozco-terWengel, P., Kijas, J., Mereu, P., Cabras, P., Mazza, R., Pirastru, M., Bruford, M. W., 2017. Genomic signatures of adaptive introgression from European mouflon into domestic sheep. Sci. Rep. 7, 1-13.
    [4]
    Ben, G., 1979. The tomb of Majiayao type No.1 in Minhe Walnut village, Qinghai Province(in Chinese). Cult. Relics. 29-32.
    [5]
    Brunson, K. He, N., Dai, X., 2016. Sheep, cattle, and specialization: New zooarchaeological perspectives on the Taosi Longshan. Int. J. Osteoarchaeol. 26, 460-475.
    [6]
    Cai, D.-W., Han, L., Zhang, X.-L., Zhou, H., Zhu, H., 2007. DNA analysis of archaeological sheep remains from China. J. Archaeol. Sci. 34, 1347-1355.
    [7]
    Cai, D., Tang, Z., Chen, Q., Han, L., Zhou, H., 2010a. Molecular archaeological studies on the origin of Chinese sheep (in Chinese). Research of China's Frontier Archaeology 9, 291-300.
    [8]
    Cai, D., Tang, Z., Yu, H., Han, L., Ren, X., Zhao, X., Zhu, H., Zhou, H., 2010b. Early history of Chinese domestic sheep indicated by ancient DNA analysis of Bronze Age individuals. J. Archaeol. Sci. 38, 896-902.
    [9]
    Cai, Q., 2002. The Guchengzhai Longshan City Site and the Formation of Civilization in Central Plains (in Chinese). Cultural Relics of Central China 6, 27-32.
    [10]
    Chen, S., Zhou, Y., Chen, Y., Gu, J., 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884-i890.
    [11]
    Chessa, B., Pereira, F., Arnaud, F., Amorim, A., Goyache, F., Mainland, I., Kao, R. R., Pemberton, J. M., Beraldi, D., Stear, M. J., 2009. Revealing the history of domesticated sheep using retrovirus integrations. Science 324, 532-536.
    [12]
    Christian, D., 2000. Silk roads or steppe roads? The silk roads in world history. Journal of World History, 1-26.
    [13]
    Dabney, J., Knapp, M., Glocke, I., Gansauge, M.-T., Weihmann, A., Nickel, B., Valdiosera, C., Garcia, N., Paabo, S., Arsuaga, J.-L., 2013. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. 110, 15758-15763.
    [14]
    Dabney, J., Meyer, M., 2019. Extraction of highly degraded DNA from ancient bones and teeth. Ancient DNA. Humana Press, New York. p. 25-29.
    [15]
    Dani, A. H., 1992. History of Civilizations of Central Asia. UNESCO Paris.
    [16]
    Darriba, D., Taboada, G. L., Doallo, R., Posada, D., 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772-772.
    [17]
    Deng, J., Xie, X.-L., Wang, D.-F., Zhao, C., Lv, F.-H., Li, X., Yang, J., Yu, J.-L., Shen, M., Gao, L., 2020. Paternal origins and migratory episodes of domestic sheep. Curr. Biol. 30, 4085-4095.
    [18]
    DePristo, M. A., Banks, E., Poplin, R., Garimella, K. V., Maguire, J. R., Hartl, C., Philippakis, A. A., Del Angel, G., Rivas, M. A., Hanna, M., 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498.
    [19]
    Dong, G., Du, L., Wei, W., 2021. The impact of early trans-Eurasian exchange on animal utilization in northern China during 5000-2500 BP. The Holocene 31, 294-301.
    [20]
    Drummond, A. J., Suchard, M. A., Xie, D., Rambaut, A., 2012. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
    [21]
    Dymova, M. A., Zadorozhny, A. V., Mishukova, O. V., Khrapov, E. A., Druzhkova, A. S., Trifonov, V. A., Kichigin, I. G., Tishkin, A. A., Grushin, S. P., Filipenko, M. L., 2017. Mitochondrial DNA analysis of ancient sheep from Altai. Anim. Genet. 48, 615-618.
    [22]
    Excoffier, L., Lischer, H. E. L., 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567.
    [23]
    Green, R. E., Malaspinas, A.-S., Krause, J., Briggs, A. W., Johnson, P. L. F., Uhler, C., Meyer, M., Good, J. M., Maricic, T., Stenzel, U. et al., 2008. A complete neandertal mitochondrial genome sequence determined by high-throughput Sequencing. Cell 134, 416-426.
    [24]
    Guo, W., 2012. Archaeological research on the late prehistoric society in Xinjiang (in Chinese). Shanghai Classics Publishing House Shanghai.
    [25]
    Han, L., Cai, D., Yu, H., Zhang, X., Zhou, H., Zhu, H., 2009. Mitochondrial DNA analysis of ancient sheep in Inner Mongolia during the spring and autumn and the warring states period (in Chinese). Progr. Nat. Sci. 19, 1049-1055.
    [26]
    He, G. L., Wang, M. G., Zou, X., Yeh, H. Y., Liu, C. H., Liu, C., Chen, G., Wang, C. C., 2023. Extensive ethnolinguistic diversity at the crossroads of North China and South Siberia reflects multiple sources of genetic diversity. J. Syst. Evol. 61, 230-250.
    [27]
    Hemphill, B. E., 1999. Foreign elites from the Oxus civilization? A craniometric study of anomalous burials from Bronze Age Tepe Hissar. Am. J. Phys. Anthropol. 110, 421-434.
    [28]
    Hermes, T. R., Tishkin, A. A., Kosintsev, P. A., Stepanova, N. F., Krause-Kyora, B., Makarewicz, C. A., 2020. Mitochondrial DNA of domesticated sheep confirms pastoralist component of Afanasievo subsistence economy in the Altai Mountains (3300-2900 cal BC). Archaeol. Res. Asia. 24, 100232.
    [29]
    Huang, Y., 1996. Identification and study of the animal bones from the Zhukaigou site, Inner Mongolia (in Chinese). Acta. Archaeol. Sin. 28.
    [30]
    Institute of Archaeology, C. A. o. S. S., 2003. Shizhaocun and Xishanping (in Chinese). Encyclopedia of China Publishing House Beijing.
    [31]
    Jeong, C., Wang, K., Wilkin, S., Taylor, W. T. T., Miller, B. K., Bemmann, J. H., Stahl, R., Chiovelli, C., Knolle, F., Ulziibayar, S., 2020. A dynamic 6,000-year genetic history of Eurasia’s Eastern Steppe. Cell 183, 890-904.
    [32]
    Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403-1405.
    [33]
    Jonsson, H., Ginolhac, A., Schubert, M., Johnson, P. L., Orlando, L., 2013. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682-1684.
    [34]
    Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
    [35]
    Kumar, V., Wang, W., Zhang, J., Wang, Y., Ruan, Q., Yu, J., Wu, X., Hu, X., Wu, X., Guo, W., 2022. Bronze and Iron Age population movements underlie Xinjiang population history. Science 376, 62-69.
    [36]
    Kuzmina, E. E., 2008. The prehistory of the Silk Road. University of Pennsylvania Press, Philadelphia.
    [37]
    Larson, G., Liu, R., Zhao, X., Yuan, J., Fuller, D., Barton, L., Dobney, K., Fan, Q., Gu, Z., Liu, X.-H., 2010. Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc. Natl. Acad. Sci. 107, 7686-7691.
    [38]
    Legge, A., 1992. The exploitation of sheep and goat at Jeitun. Academy of Sciences of Turkmenistan, Ashkabad.
    [39]
    Li, H., 2011. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987-2993.
    [40]
    Li, H., Durbin, R., 2009. Fast and Accurate Short Read Alignment with Burrows-Wheeler Transform. Bioinformatics 25, 1754-1760.
    [41]
    Li, W., 2004. The utilization of animal resources in Erlitou Culture (in Chinese). Cultural Relics of Central China 2, 40-45.
    [42]
    Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
    [43]
    Lv, F.-H., Peng, W.-F., Yang, J., Zhao, Y.-X., Li, W.-R., Liu, M.-J., Ma, Y.-H., Zhao, Q.-J., Yang, G.-L., Wang, F., 2015. Mitogenomic Meta-Analysis Identifies Two Phases of Migration in the History of Eastern Eurasian Sheep. Mol. Biol. Evol. 32, 2515-2533.
    [44]
    Lv, P., 2009. Identification and study of animal remains at Wadian Site in Yu County (in Chinese). Chinese Civilization Exploration Project: Technology and Economy Volume 1. Science Press, Beijing.
    [45]
    Meadows, J. R. S., Cemal, I., Karaca, O., Gootwine, E., Kijas, J. W., 2007. Five ovine mitochondrial lineages identified from sheep breeds of the near East. Genetics 175, 1371-1379.
    [46]
    Meadows, J. R. S., Kantanen, J., Tapio, M., Sipos, W., Pardeshi, V., Gupta, V., Calvo, J. H., Whan, V., Norris, B., Kijas, J. W., 2005. Mitochondrial sequence reveals high levels of gene flow between breeds of domestic sheep from Asia and Europe. J. Hered. 96, 494-501.
    [47]
    Miller, M. A., Schwartz, T., Pickett, B. E., He, S., Klem, E. B., Scheuermann, R. H., Passarotti, M., Kaufman, S., O’Leary, M. A., 2015. A RESTful API for Access to Phylogenetic Tools via the CIPRES Science Gateway. Evol. Bioinform. 11, 43-48.
    [48]
    Muigai, A. W., Hanotte, O., 2013. The origin of African sheep: archaeological and genetic perspectives. Afr. Archaeol. Rev. 30, 39-50.
    [49]
    Mwacharo, J.M., Kim, E-S., Elbeltagy, A. R., Aboul-Naga, A. M., Rischkowsky, B. A., Rothschild, M. F., 2017. Genomic footprints of dryland stress adaptation in Egyptian fat-tail sheep and their divergence from East African and western Asia cohorts. Sci. Rep. 7, 1-10.
    [50]
    Nishiaki, Y., Aripdjanov, O., Arai, S., Akashi, C., Nakata, H., Sayfullayev, B., Ergashev, O., Suleimanov, R., 2022. Neolithization during the 6th Millennium BCE in Western Central Asia: New Evidence from Kaynar Kamar Rockshelter, Hissar Mountains, Southeast Uzbekistan. Archaeological Research in Asia 30, 100352.
    [51]
    Nu, H., 2013. The Longshan period site of Taosi in southern Shanxi province. In: Underhill, A. P., editor. A companion to Chinese archaeology. Wiley-Blackwell, Malden. p. 255-277.
    [52]
    Okonechnikov, K., Conesa, A., Garcia-Alcalde, F., 2016. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32, 292-294.
    [53]
    Qiu, W., 1996. The great historical significance of the excavation of Longshan cultural site of the Taosi site (in Chinese). Historical Monthly 5, 78-83.
    [54]
    Rambaut, A., Drummond, A. J., Xie, D., Baele, G., Suchard, M. A., 2018. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst. Biol. 67, 901-904.
    [55]
    Ren, M., 2014. Archaeological survey of Tajikistan and Uzbekistan-Copperstone Age to Hellenistic Age (in Chinese). Cult. Rel. 7, 54-67.
    [56]
    Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., Huelsenbeck, J. P., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542.
    [57]
    Ryder, M., 1984. Sheep In: Mason IL, editor. Evolution of Domesticated Animals. London/New York: Longman Group.
    [58]
    Sassi-Zaidy, Y. B., Mohamed-Brahmi, A., Chaouch, M., Maretto, F., Cendron, F., Charfi-Cheikhrouha, F., Abderrazak, S. B., Djemali, M., Cassandro, M., 2022. Historical Westward Migration Phases of Ovis aries Inferred from the Population Structure and the Phylogeography of Occidental Mediterranean Native Sheep Breeds. Genes 13, 1421.
    [59]
    Simon, A., 2010. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom.
    [60]
    Spengler, R. N., Willcox, G., 2013. Archaeobotanical results from Sarazm, Tajikistan, an Early Bronze Age Settlement on the edge: Agriculture and exchange. Environ Archaeol 18, 211-221.
    [61]
    Tapio, M., Marzanov, N., Ozerov, M., Cinkulov, M., Gonzarenko, G., Kiselyova, T., Murawski, M., Viinalass, H., Kantanen, J., 2006. Sheep mitochondrial DNA variation in European, Caucasian, and Central Asian areas. Mol. Biol. Evol. 23, 1776-1783.
    [62]
    Taylor, W. T., Pruvost, M., Posth, C., Rendu, W., Krajcarz, M. T., Abdykanova, A., Brancaleoni, G., Spengler, R., Hermes, T., Schiavinato, S., 2021. Evidence for early dispersal of domestic sheep into Central Asia. Nature Human Behaviour 5, 1169-1179.
    [63]
    Thorvaldsdottir, H., Robinson, J. T., Mesirov, J. P., 2013. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178-192.
    [64]
    Wang, Q., Wang, Z., Liu, L., 2020. Excavation of Jinchankou Site in Huzhu County of Qinghai. Sichuan Cult. Relics. 1, 4-21.
    [65]
    Wang, Y., 2017. Identifying the beginnings of Sheep Husbandry in Westen China, University of Cambridge.
    [66]
    Wang, Y., Chen, Q., Bao, S., Wang, L., 2017. Study on the Faunal Remains of the Nailingao Site, Inner Mongolia, 2015 (in Chinese). Steppe Cult. Relics. 1, 115-124.
    [67]
    Xie, D., 1975. Excavation of a Chichia Culture cemetrey at Ch`inwei-Chia in Yung-Ching County, Kansu province (in Chinese). Acta Archaeologlca Sinica 2, 57-96, 180-191.
    [68]
    Xu, Y.-X., Wang, B., Jing, J.-N., Ma, R., Luo, Y.-H., Li, X., Yan, Z., Liu, Y.-J., Gao, L., Ren, Y.-L., 2023. Whole-body adipose tissue multi-omic analyses in sheep reveal molecular mechanisms underlying local adaptation to extreme environments. Communications Biology 6, 159.
    [69]
    Yu, J., Wang, Y., He, J., Feng, Y., Li, Y., Li, W., 2018. The Tongtian Dong Site in Jeminay County, Xinjiang. Archaeology 7, 2+5-16.
    [70]
    Yuan, J., 2001. The origin of domestic animals in Neolithic China (in Chinese). Cult. Rel. 5, 51-58.
    [71]
    Yuan, J., 2008. The origins and development of animal domestication in China. Chinese Archaeology 8, 1-7.
    [72]
    Yuan, J., Huang, Y., Yang, M., 2007a. Zooarchaeology study in the Central Plains during 2,500-1,500 BC: A case study of the Taosi, Wang Chenggang, Xinzhai and Erlitou sites (in Chinese). Science for Archaeology (Ⅱ). Science Press Beijing. p. 12-24.
    [73]
    Yuan, J., Huang, Y., Yang, M., Lv, P., Tao, Y., Yang, J., 2007b. Animal archaeological study in the Zhongyuan region from 2500 to 1500 BC based on the examples of the Taosi, Wangchenggang, Xinzhai, and Erlitou sites (in Chinese). Archaeol. Sci. 2, 28.
    [74]
    Yuan, J., Roderick, C., Lorenzo, C., Chen, X., 2020. Subsistence and persistence: agriculture in the Central Plains of China through the Neolithic to Bronze Age transition. Antiquity 94, 900-915.
    [75]
    Yurtman, E., Ozer, O., Yuncu, E., Dagtas, N. D., Koptekin, D., Cakan, Y. G., Ozkan, M., Akbaba, A., Kaptan, D., Atag, G., 2021. Archaeogenetic analysis of Neolithic sheep from Anatolia suggests a complex demographic history since domestication. Communications Biology 4, 1279.
    [76]
    Zhang, L., 2022. Coupling relationship between climate and ecological environment in the agro-pastoral ecotone in northern China since Holocene, Lanzhou University, Lanzhou.
    [77]
    Zhang, X., Qiu, S., Cai, L., Bo, G., Wang, J., Zhong, J., 2008. Establishment and Perfection of the Archaeological Chronological Sequence of Xinzhai-Erlitou-Erligang Cultures (in Chinses). Archaeology 8, 74-89.
    [78]
    Zhao, E., Yu, Q., Zhang, N., Kong, D., Zhao, Y., 2013. Mitochondrial DNA diversity and the origin of Chinese indigenous sheep. Trop. Anim. Health Prod. 45, 1715-1722.
    [79]
    Zhao, Y.-X., Yang, J., Lv, F.-H., Hu, X.-J., Xie, X.-L., Zhang, M., Li, W.-R., Liu, M.-J., Wang, Y.-T., Li, J.-Q. et al., 2017. Genomic reconstruction of the history of native sheep reveals the peopling patterns of nomads and the expansion of early pastoralism in East Asia. Mol. Biol. Evol. 34, 2380-2395.
    [80]
    Zhou, X., Yu, J., Spengler, R. N., Shen, H., Zhao, K., Ge, J., Bao, Y., Liu, J., Yang, Q., Chen, G., 2020. 5,200-year-old cereal grains from the eastern Altai Mountains redate the trans-Eurasian crop exchange. Nat. Plants 6, 78-87.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (166) PDF downloads (16) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return