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Ancient DNA Reveals China as a Historical Genetic Melting Pot in Tiger Evolution

Xin Sun, Yue-Chen Liu, Mikhail P. Tiunov, Dmitry O. Gimranov, Yan Zhuang, Yu Han, Carlos A. Driscoll, Yu-Hong Pang, Chunmei Li, Yan Pan, Marcela Sandoval Velasco, Shyam Gopalakrishnan, Rui-Zheng Yang, Bao-Guo Li, Kun Jin, Xiao Xu, Olga Uphyrkina, Yan-Yi Huang, Xiao-Hong Wu, M. Thomas P. Gilbert, Stephen J. O’Brien, Nobuyuki Yamaguchi, Shu-Jin Luo
doi: https://doi.org/10.1101/2022.09.14.507899
Xin Sun
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Yue-Chen Liu
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Mikhail P. Tiunov
2Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok 690022, Russia
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Dmitry O. Gimranov
3Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, Yekaterinburg 620144, Russia; Ural Federal University, Yekaterinburg 620002, Russia
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Yan Zhuang
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Yu Han
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Carlos A. Driscoll
4Section of Comparative Behavioral Genomics, National Institute on Alcohol Abuse and Alcoholism, NIH, Rockville, MD 20852, USA
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Yu-Hong Pang
5Beijing Advanced Innovation Center for Genomics (ICG), Biodynamic Optical Imaging Center (BIOPIC), School of Life Sciences, Peking University, Beijing 100871, China
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Chunmei Li
5Beijing Advanced Innovation Center for Genomics (ICG), Biodynamic Optical Imaging Center (BIOPIC), School of Life Sciences, Peking University, Beijing 100871, China
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Yan Pan
6School of Archaeology and Museology, Peking University, Beijing 100871, China
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Marcela Sandoval Velasco
7Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
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Shyam Gopalakrishnan
7Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
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Rui-Zheng Yang
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Bao-Guo Li
8Shaanxi Key Laboratory for Animal Conservation, College of Life Sciences, Northwest University, Xi’an 710069, China
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Kun Jin
9Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing, China
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Xiao Xu
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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Olga Uphyrkina
2Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok 690022, Russia
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Yan-Yi Huang
5Beijing Advanced Innovation Center for Genomics (ICG), Biodynamic Optical Imaging Center (BIOPIC), School of Life Sciences, Peking University, Beijing 100871, China
10College of Chemistry and Molecular Engineering, Beijing National Laboratory for Molecular Sciences, Peking University, Beijing, China
11Institute for Cell Analysis, Shenzhen Bay Laboratory, Guangdong, China
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Xiao-Hong Wu
6School of Archaeology and Museology, Peking University, Beijing 100871, China
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M. Thomas P. Gilbert
7Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
12University Museum, Norwegian University of Science and Technology, Trondheim, Norway
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Stephen J. O’Brien
13Laboratory of Genomic Diversity, ITMO University, St. Petersburg, Russia
14Guy Harvey Oceanographic Center, Halmos College of Arts and Sciences, Nova Southeastern University, Fort Lauderdale, FL 33004, USA
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  • For correspondence: luo.shujin@pku.edu.cn human37564nobby@gmail.com lgdchief@gmail.com
Nobuyuki Yamaguchi
15Institute of Tropical Biodiversity and Sustainable Development, University of Malaysia Terengganu, Kuala Nerus 21030, Kuala Terengganu, Terengganu, Malaysia
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  • For correspondence: luo.shujin@pku.edu.cn human37564nobby@gmail.com lgdchief@gmail.com
Shu-Jin Luo
1The State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
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  • For correspondence: luo.shujin@pku.edu.cn human37564nobby@gmail.com lgdchief@gmail.com
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Abstract

The contrast between the tiger’s (Panthera tigris) 2-3 My age and extant tigers’ coalescence approximately 110,000 years ago suggests an ancient demographic bottleneck. Here we collected over 60 extinct specimens across mainland Asia and generated whole genome sequences from a 10,600-year-old Russian Far East (RFE) specimen (RUSA21, 8ξ coverage), 14 South China tigers (0.1-12ξ), three Caspian tigers (4-8ξ), plus 17 new mitogenomes. RUSA21 clustered within modern Northeast Asian phylogroups and partially derived from an extinct Late Pleistocene lineage. While some 8,000-10,000-year-old RFE mitogenomes are basal to all tigers, one 2,000-year-old specimen resembles present Amur tigers. The Caspian tiger likely dispersed from an ancestral Northeast Asian population and experienced gene flow from southern Bengal tigers. Lastly, genome-wide monophyly supported the South China tiger as a distinct subspecies, albeit with mitochondrial paraphyly, hence resolving its longstanding taxonomic controversy. The distribution of mitochondrial haplogroups corroborated by biogeographical modeling suggested Southwest China was a Late Pleistocene refugium for a relic basal lineage. As suitable habitat returned, Eastern China became a genetic melting pot to foster divergent lineages to merge into South China tigers and other subsequent northern subspecies to develop. Genomic information retrieved from ancient tigers hence sheds light on the species’ full evolutionary history leading to nine modern subspecies and resolves the natural history of surviving tigers.

Competing Interest Statement

The authors have declared no competing interest.

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Ancient DNA Reveals China as a Historical Genetic Melting Pot in Tiger Evolution
Xin Sun, Yue-Chen Liu, Mikhail P. Tiunov, Dmitry O. Gimranov, Yan Zhuang, Yu Han, Carlos A. Driscoll, Yu-Hong Pang, Chunmei Li, Yan Pan, Marcela Sandoval Velasco, Shyam Gopalakrishnan, Rui-Zheng Yang, Bao-Guo Li, Kun Jin, Xiao Xu, Olga Uphyrkina, Yan-Yi Huang, Xiao-Hong Wu, M. Thomas P. Gilbert, Stephen J. O’Brien, Nobuyuki Yamaguchi, Shu-Jin Luo
bioRxiv 2022.09.14.507899; doi: https://doi.org/10.1101/2022.09.14.507899
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Ancient DNA Reveals China as a Historical Genetic Melting Pot in Tiger Evolution
Xin Sun, Yue-Chen Liu, Mikhail P. Tiunov, Dmitry O. Gimranov, Yan Zhuang, Yu Han, Carlos A. Driscoll, Yu-Hong Pang, Chunmei Li, Yan Pan, Marcela Sandoval Velasco, Shyam Gopalakrishnan, Rui-Zheng Yang, Bao-Guo Li, Kun Jin, Xiao Xu, Olga Uphyrkina, Yan-Yi Huang, Xiao-Hong Wu, M. Thomas P. Gilbert, Stephen J. O’Brien, Nobuyuki Yamaguchi, Shu-Jin Luo
bioRxiv 2022.09.14.507899; doi: https://doi.org/10.1101/2022.09.14.507899

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