Ancient DNA reveals the maternal genetic history of East Asian domestic pigs

Ming Zhang; Yichen Liu; Zhipeng Li; Peng Lü; Jacob D. Gardner; Maolin Ye; Jihuai Wang; Miaomiao Yang; Jing Shao; Weilin Wang; Qingyan Dai; Peng Cao; Ruowei Yang; Feng Liu; Xiaotian Feng; Lizhao Zhang; Enwei Li; Yunzheng Shi; Zehui Chen; Shilun Zhu; Weiwei Zhai; Tao Deng; Ziyuan Duan; E. Andrew Bennett; Songmei Hu; Qiaomei Fu

doi:10.1016/j.jgg.2021.11.014

Volume 49 Issue 6

Jun. 2022

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Article Navigation > Journal of Genetics and Genomics > 2022 > 49(6): 537-546

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Ancient DNA reveals the maternal genetic history of East Asian domestic pigs

doi: 10.1016/j.jgg.2021.11.014

a. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China;
b. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Beijing 100044, China;
c. Shanghai Qi Zhi Institute, Shanghai 200232, China;
d. Institute of Archaeology, Chinese Academy of Social Sciences, Beijing 100710, China;
e. School of History and Culture, Lanzhou University, Lanzhou, Gansu 730000, China;
f. Shaanxi Academy of Archaeology, Xi’an, Shaanxi 710054, China;
g. School of History and Culture, Shanxi University, Taiyuan, Shanxi 030006, China;
h. Xingtai Cultural Relics Administration, Xingtai, Hebei 054000, China;
i. Institute of Genetics and Developmental Biology Chinese Academy of Sciences, Beijing 100101, China;
j. University of Chinese Academy of Sciences, Beijing 100049, China

Funds:

We are grateful to the following people and institutions for providing samples, support, and advice: Jing Yuan (Institute of Archaeology, Chinese Academy of Social Science), Albert Min-Shan Ko (Department of Biomedical Sciences, Chang Gung University), and Xiaowei Mao (Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences). This work was supported by the Chinese Academy of Sciences (CAS, XDB26000000), the Ministry of Finance of the People’s Republic of China (YSBR-019), the National Natural Science Foundation of China (41925009), the Tencent Foundation (through the XPLORER PRIZE), the Howard Hughes Medical Institute (grant 55008731), and the Shanghai Qi Zhi Institute.

Received Date: 2021-07-28
Accepted Date: 2021-11-30
Rev Recd Date: 2021-11-30
Publish Date: 2022-06-30

Abstract

Abstract

Zoo-archaeological and genetic evidence suggest that pigs were domesticated independently in Central China and Eastern Anatolia along with the development of agricultural communities and civilizations. However, the genetic history of domestic pigs, especially in China, has not been fully explored. In this study, we generate 42 complete mitochondrial DNA sequences from ~7500- to 2750-year-old individuals from the Yellow River basin. Our results show that the maternal genetic continuity of East Asian domestic pigs dates back to at least the Early to Middle Neolithic. In contrast, the Near Eastern ancestry in European domestic pigs saw a near-complete genomic replacement by the European wild boar. The majority of East Asian domestic pigs share close haplotypes, and the most recent common ancestor of most branches dates back to less than 20,000 years before present, inferred using new substitution rates of whole mitogenomes or combined protein-coding regions. Two major population expansion events of East Asian domestic pigs coincided with changes in climate, widespread adoption of introduced crops, and the development of agrarian societies. These findings add to our understanding of the maternal genetic composition and help to complete the picture of domestic pig evolutionary history in East Asia.
- Ancient mitogenomes,
- Sus scrofa,
- Pig domestication,
- Genetic history,
- East Asia

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References

Ameen, C., Feuerborn, T.R., Brown, S.K., Linderholm, A., Hulme-Beaman, A., Lebrasseur, O., Sinding, M.S., Lounsberry, Z.T., Lin, A.T., Appelt, M., et al., 2019. Specialized sledge dogs accompanied Inuit dispersal across the North American Arctic. Proc. Biol. Sci. 286, 20191929

An, C.B., Feng, Z.D., Barton, L., 2004. Environmental change and cultural response between 8000 and 4000 cal. J. Quat. Sci. 19, 529-535

Caliebe, A., Nebel, A., Makarewicz, C., Krawczak, M., Krause-Kyora, B., 2017. Insights into early pig domestication provided by ancient DNA analysis. Sci. Rep. 7, 44550

Cannon, M.V., Brandebourg, T.D., Kohn, M.C., Ethikic, D., Irwin, M.H., Pinkert, C.A., 2015. Mitochondrial DNA sequence and phylogenetic evaluation of geographically disparate Sus scrofa breeds. Anim. Biotechnol. 26, 17-28

Choi, S.K., Kim, K.S., Ranyuk, M., Babaev, E., Voloshina, I., Bayarlkhagva, D., Chong, J.R., Ishiguro, N., Yu, L., Min, M.S., et al., 2020. Asia-wide phylogeography of wild boar (Sus scrofa) based on mitochondrial DNA and Y-chromosome:Revising the migration routes of wild boar in Asia. PLoS One 15, e0238049

Choi, S.K., Lee, J.E., Kim, Y.J., Min, M.S., Voloshina, I., Myslenkov, A., Oh, J.G., Kim, T.H., Markov, N., Seryodkin, I., et al., 2014. Genetic structure of wild boar (Sus scrofa) populations from East Asia based on microsatellite loci analyses. BMC Genet. 15, 85

Conolly, J., Colledge, S., Dobney, K., Vigne, J.-D., Peters, J., Stopp, B., Manning, K., Shennan, S., 2011. Meta-analysis of zooarchaeological data from SW Asia and SE Europe provides insight into the origins and spread of animal husbandry. J. Archaeol. Sci. 38, 538-545

Cucchi, T., Hulme-Beaman, A., Yuan, J., Dobney, K., 2011. Early Neolithic pig domestication at Jiahu, Henan Province, China:clues from molar shape analyses using geometric morphometric approaches. J. Archaeol. Sci. 38, 11-22

Dabney, J., Knapp, M., Glocke, I., Gansauge, M.T., Weihmann, A., Nickel, B., Valdiosera, C., Garcia, N., Paabo, S., Arsuaga, J.L., et al., 2013. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. U. S. A. 110, 15758-15763

Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. jModelTest 2:more models, new heuristics and parallel computing. Nat. Methods 9, 772-772

Diamond, J., Bellwood, P., 2003. Farmers and their languages:The first expansions. Science 300, 597-603

Dong, N., Yuan, J., 2020. Rethinking pig domestication in China:regional trajectories in central China and the Lower Yangtze Valley. Antiquity 94, 864-879

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

Edgar, R.C., 2004. MUSCLE:multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797

Ervynck, A., Hongo, H., Dobney, K., Meadow, R., 2001. Born free?New evidence for the status of Sus scrofa at Neolithic Cayonu Tepesi (Southeastern Anatolia, Turkey). Paleorient 27, 47-73

Excoffier, L., Lischer, H.E., 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

Frantz, L., Meijaard, E., Gongora, J., Haile, J., Groenen, M.A., Larson, G., 2016. The evolution of Suidae. Annu. Rev. Anim. Biosci. 4, 61-85

Frantz, L.A., Schraiber, J.G., Madsen, O., Megens, H.J., Cagan, A., Bosse, M., Paudel, Y., Crooijmans, R.P., Larson, G., Groenen, M.A., 2015. Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nat. Genet. 47, 1141-1148

Frantz, L.A.F., Bradley, D.G., Larson, G., Orlando, L., 2020. Animal domestication in the era of ancient genomics. Nat. Rev. Genet. 21, 449-460

Frantz, L.A.F., Haile, J., Lin, A.T., Scheu, A., Georg, C., Benecke, N., Alexander, M., Linderholm, A., Mullin, V.E., Daly, K.G., et al., 2019. Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe. Proc. Natl. Acad. Sci. U. S. A. 116, 17231-17238

Fu, Q., Meyer, M., Gao, X., Stenzel, U., Burbano, H.A., Kelso, J., Paabo, S., 2013. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl. Acad. Sci. U. S. A. 110, 2223-2227

Greig, K., Boocock, J., Allen, M.S., Matisoo-Smith, E., Walter, R., 2018. Ancient DNA evidence for the introduction and dispersal of dogs (Canis familiaris) in New Zealand. J. Pac. Archaeol. 9, 1-10

Greig, K., Boocock, J., Prost, S., Horsburgh, K.A., Jacomb, C., Walter, R., Matisoo-Smith, E., 2015. Complete mitochondrial genomes of New Zealand's first dogs. PLoS One 10, e0138536

Greig, K., Gosling, A., Collins, C.J., Boocock, J., McDonald, K., Addison, D.J., Allen, M.S., David, B., Gibbs, M., Higham, C.F.W., et al., 2018. Complex history of dog (Canis familiaris) origins and translocations in the Pacific revealed by ancient mitogenomes. Sci. Rep. 8, 1-9

Groenen, M.A.M., Archibald, A.L., Uenishi, H., Tuggle, C.K., Takeuchi, Y., Rothschild, M.F., Rogel-Gaillard, C., Park, C., Milan, D., Megens, H.J., et al., 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393-398

Hofmanova, Z., Kreutzer, S., Hellenthal, G., Sell, C., Diekmann, Y., Diez-Del-Molino, D., van Dorp, L., Lopez, S., Kousathanas, A., Link, V., et al., 2016. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl. Acad. Sci. U. S. A. 113, 6886-6891

Jin, L., Zhang, M., Ma, J., Zhang, J., Zhou, C., Liu, Y., Wang, T., Jiang, A.A., Chen, L., Wang, J., et al., 2012. Mitochondrial DNA evidence indicates the local origin of domestic pigs in the upstream region of the Yangtze River. PLoS One 7, e51649

Konishi, T., Matsukuma, S., Fuji, H., Nakamura, D., Satou, N., Okano, K., 2019. Principal component analysis applied directly to sequence matrix. Sci. Rep. 9, 19297

Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X:Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549

Larson, G., Albarella, U., Dobney, K., Rowley-Conwy, P., Schibler, J., Tresset, A., Vigne, J.D., Edwards, C.J., Schlumbaum, A., Dinu, A., et al., 2007. Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc. Natl. Acad. Sci. U. S. A. 104, 15276-15281

Larson, G., Dobney, K., Albarella, U., Fang, M., Matisoo-Smith, E., Robins, J., Lowden, S., Finlayson, H., Brand, T., Willerslev, E., et al., 2005. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307, 1618-1621

Larson, G., Fuller, D.Q., 2014. The evolution of animal domestication. Annu. Rev. Ecol. Evol. S. 45, 115-136

Larson, G., Liu, R., Zhao, X., Yuan, J., Fuller, D., Barton, L., Dobney, K., Fan, Q., Gu, Z., Liu, X.H., et al., 2010. Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc. Natl. Acad. Sci. U. S. A. 107, 7686-7691

Larson, G., Piperno, D.R., Allaby, R.G., Purugganan, M.D., Andersson, L., Arroyo-Kalin, M., Barton, L., Climer Vigueira, C., Denham, T., Dobney, K., et al., 2014. Current perspectives and the future of domestication studies. Proc. Natl. Acad. Sci. U. S. A. 111, 6139-6146

Leigh, J.W., Bryant, D., 2015. POPART:Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110-1116

Li, H., Durbin, R., 2010. Fast and accurate long-read alignment with burrowswheeler transform. Bioinformatics 26, 589-595

Li, K.Y., Li, K.T., Yang, C.H., Hwang, M.H., Chang, S.W., Lin, S.M., Wu, H.J., Basilio, E.B., Vega, R.S.A., Laude, R.P., et al., 2017. Insular East Asia pig dispersal and vicariance inferred from Asian wild boar genetic evidence. J. Anim. Sci., 95, 1451-1466

Librado, P., Rozas, J., 2009. DnaSP v5:a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452

Liu, L., Chen, X., 2012. The Archaeology of China:from the Late Paleolithic to the Early Bronze Age. Cambridge:Cambridge University Press

Long, T., Leipe, C., Jin, G., Wagner, M., Guo, R., Schroder, O., Tarasov, P.E., 2018. The early history of wheat in China from C14 dating and Bayesian chronological modelling. Nat. Plants 4, 272-279

Luo, Y., 2015. The development of Chinese domestic pigs in the early stage (in Chinese). China Cultural Heritage 4, 40-45.(In Chinese)

Meyer, M., Kircher, M., 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor protocols 2010, pdb prot5448

Nie, Z.S., Hong, L., Ma, B.Q., 2008. Fossil fauna in the late stage of late Pleistocene in the Hetao basin, Innermongolia. Quat. Sci. 28:14-25.(In Chinese with English Abstract)

Ottoni, C., Flink, L.G., Evin, A., Georg, C., De Cupere, B., Van Neer, W., Bartosiewicz, L., Linderholm, A., Barnett, R., Peters, J., et al., 2013. Pig domestication and human-mediated dispersal in western Eurasia revealed through ancient DNA and geometric morphometrics. Mol. Biol. Evol. 30, 824-832

Peters, J., Driesch, A.V.D., Helmer, D., 2005. The Upper Euphrates-Tigris Basin:Cradle of agro-pastoralism?, in:Vigne, J.D., Peters, J., Helmer, D.(Eds.), The first steps of animal domestication:new archaeozoological approaches. Proceedings of the Ninth International Council of Archeozoology, Oxbow Books, Oxford, pp. 96-123

Price, M., Hongo, H., 2020. The archaeology of Ppig domestication in Eurasia. Archaeol. Res. 28, 557-615

Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., 2014. Tracer V1. 6. Computer Program and Documentation Distributed by the Author, website http://beast.bio.ed.ac.uk/Tracer

Ren, L., Yang, Y., Wang, Q., Zhang, S., Chen, T., Cui, Y., Wang, Z., Liang, G., Dong, G., 2020. The transformation of cropping patterns from Late Neolithic to Early Iron Age (5900-2100 BP) in the Gansu-Qinghai region of northwest China. The Holocene 31, 183-193

Rohland, N., Harney, E., Mallick, S., Nordenfelt, S., Reich, D., 2015. Partial uracil-DNA-glycosylase treatment for screening of ancient DNA. Philos. Trans. R. Soc. B-Biol. Sci. 370, 20130624

Skoglund, P., Northoff, B.H., Shunkov, M.V., Derevianko, A.P., Paabo, S., Krause, J., Jakobsson, M., 2014. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proc. Natl. Acad. Sci. U. S. A. 111, 2229-2234

Thalmann, O., Shapiro, B., Cui, P., Schuenemann, V.J., Sawyer, S.K., Greenfield, D.L., Germonpre, M.B., Sablin, M.V., Lopez-Giraldez, F., Domingo-Roura, X., et al., 2013. Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science 342, 871-874

Wang, C., Chen, Y.S., Han, J.L., Mo, D.L., Li, X.J., Liu, X.H., 2019. Mitochondrial DNA diversity and origin of indigenous pigs in South China and their contribution to western modern pig breeds. J. Integr. Agr. 18, 2338-2350

Wang, C., Lu, H.Y., Zhang, J.P., Gu, Z.Y., He, K.Y., 2014. Prehistoric demographic fluctuations in China inferred from radiocarbon data and their linkage with climate change over the past 50,000 years. Quat. Sci. Rev. 98, 45-59

Wang, J., Zou, H., Chen, L., Long, X., Lan, J., Liu, W., Ma, L., Wang, C., Xu, X., Ren, L., et al., 2017. Convergent and divergent genetic changes in the genome of Chinese and European pigs. Sci. Rep. 7, 8662

White, S., 2011. From globalized pig breeds to capitalist pigs:a study in animals cultures and evolutionary history. Environ. Hist. 16, 94-120

Wu, G.S., Yao, Y.G., Qu, K.X., Ding, Z.L., Li, H., Palanichamy, M.G., Duan, Z.Y., Li, N., Chen, Y.S., Zhang, Y.P., 2007. Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol. 8, R245

Xiang, H., Gao, J., Cai, D., Luo, Y., Yu, B., Liu, L., Liu, R., Zhou, H., Chen, X., Dun, W., et al., 2017. Origin and dispersal of early domestic pigs in northern China. Sci. Rep. 7, 5602

Yang, S.L., Zhang, H., Mao, H.M., Yan, D.W., Lu, S.X., Lian, L.S., Zhao, G.Y., Yan, Y.L., Deng, W.D., Shi, X.W., et al., 2011. The local origin of the Tibetan pig and additional insights into the origin of Asian pigs. Plos One 6, e28215

Zeder, M.A., 2008. Domestication and early agriculture in the Mediterranean Basin:Origins, diffusion, and impact. Proc. Natl. Acad. Sci. U. S. A. 105, 11597-11604

Zeder, M.A., 2011. The origins of agriculture in the Near East. Curr. Anthropol. 52, S221-S235

Zeder, M.A., 2017. Out of the fertile crescent:The dispersal of domestic livestock through Europe and Africa, in:N., B, R., C., M., P (Eds.), Human dispersal and species movement:from prehistory to the present. Cambridge University Press, Cambridge pp. 261-303

Zhang, M., Sun, G., Ren, L., Yuan, H., Dong, G., Zhang, L., Liu, F., Cao, P., Ko, A.M., Yang, M.A., et al., 2020. Ancient DNA evidence from China reveals the expansion of Pacific dogs. Mol. Biol. Evol. 37, 1462-1469

Zheng, H.X., Yan, S., Qin, Z.D., Wang, Y., Tan, J.Z., Li, H., Jin, L., 2011. Major population expansion of East Asians began before Neolithic time:evidence of mtDNA genomes. Plos One 6, e25835

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