863 genomes reveal the origin and domestication of chicken

doi:10.1038/s41422-020-0349-y

. 2020 Aug;30(8):693-701.

doi: 10.1038/s41422-020-0349-y. Epub 2020 Jun 25.

863 genomes reveal the origin and domestication of chicken

Ming-Shan Wang^#^{1

2

3}, Mukesh Thakur^#^{1

4}, Min-Sheng Peng^#^{1

2

5}, Yu Jiang^#⁶, Laurent Alain François Frantz^#^{1

7

8}, Ming Li^#⁶, Jin-Jin Zhang^{1

2}, Sheng Wang^{1

2}, Joris Peters^{9

10}, Newton Otieno Otecko^{1

2}, Chatmongkon Suwannapoom¹¹, Xing Guo¹², Zhu-Qing Zheng⁶, Ali Esmailizadeh^{1

13}, Nalini Yasoda Hirimuthugoda^{1

14}, Hidayat Ashari^{15

16}, Sri Suladari¹⁵, Moch Syamsul Arifin Zein¹⁵, Szilvia Kusza¹⁷, Saeed Sohrabi¹³, Hamed Kharrati-Koopaee^{13

18}, Quan-Kuan Shen^{1

2}, Lin Zeng^{1

2}, Min-Min Yang^{1

2}, Ya-Jiang Wu^{1

19}, Xing-Yan Yang^{1

19}, Xue-Mei Lu^{1

2

5}, Xin-Zheng Jia^{20

21}, Qing-Hua Nie²², Susan Joy Lamont²¹, Emiliano Lasagna²³, Simone Ceccobelli²³, Humpita Gamaralalage Thilini Nisanka Gunwardana¹⁴, Thilina Madusanka Senasige¹⁴, Shao-Hong Feng²⁴, Jing-Fang Si²⁵, Hao Zhang²⁵, Jie-Qiong Jin^{1

26}, Ming-Li Li^{1

2}, Yan-Hu Liu^{1

2}, Hong-Man Chen^{1

2}, Cheng Ma^{1

2}, Shan-Shan Dai^{1

2}, Abul Kashem Fazlul Haque Bhuiyan²⁷, Muhammad Sajjad Khan²⁸, Gamamada Liyanage Lalanie Pradeepa Silva²⁹, Thi-Thuy Le³⁰, Okeyo Ally Mwai²⁰, Mohamed Nawaz Mohamed Ibrahim²⁰, Megan Supple³¹, Beth Shapiro^{31

32}, Olivier Hanotte^{33

34}, Guojie Zhang^{1

5

35

36}, Greger Larson⁷, Jian-Lin Han^{37

38}, Dong-Dong Wu^{39

40

41}, Ya-Ping Zhang^{42

43

44

45}

Affiliations

¹ State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
² Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China.
³ Department of Ecology and Evolutionary Biology, Howard Hughes Medical Institute, University of California, Santa Cruz, Santa Cruz, CA, USA.
⁴ Zoological Survey of India, New Alipore, Kolkata, West Bengal, India.
⁵ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China.
⁶ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, China.
⁷ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
⁸ School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.
⁹ ArchaeoBioCenter and Department of Veterinary Sciences, Institute of Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, LMU Munich, Munich, Germany.
¹⁰ SNSB, Bavarian State Collection of Anthropology and Palaeoanatomy, Munich, Germany.
¹¹ School of Agriculture and Natural Resources, University of Phayao, Phayao, Thailand.
¹² College of Animal Science and Technology, Anhui Agricultural University, Hefei, Anhui, China.
¹³ Department of Animal Science, Shahid Bahonar University of Kerman, Kerman, Iran.
¹⁴ Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka.
¹⁵ Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Science (LIPI), Cibinong, Indonesia.
¹⁶ CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China.
¹⁷ Institute of Animal Husbandry, Biotechnology and Nature Conservation, University of Debrecen, Debrecen, Hungary.
¹⁸ Institute of Biotechnology, School of Agriculture, Shiraz University, Shiraz, Iran.
¹⁹ State Key Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming, Yunnan, China.
²⁰ Livestock Genetics Program, International Livestock Research Institute (ILRI), Nairobi, Kenya.
²¹ Department of Animal Science, Iowa State University, Ames, IA, USA.
²² College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.
²³ Dipartimento di Scienze Agrarie, Alimentarie Ambientali, University of Perugia, Perugia, Italy.
²⁴ BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Guangdong, China.
²⁵ Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture of China, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, Beijing, China.
²⁶ Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (CAS-SEABRI), Yezin, Myanmar.
²⁷ Bangladesh Agricultural University, Mymennsingh, Bangladesh.
²⁸ University of Agriculture Faisalabad, Faisalabad, Pakistan.
²⁹ Department of Animal Science, University of Peradeniya, Peradeniya, Sri Lanka.
³⁰ National Institute of Animal Husbandry, Hanoi, Vietnam.
³¹ Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, USA.
³² Howard Hughes Medical Institute, University of California, Santa Cruz, Santa Cruz, CA, USA.
³³ Cells, Organisms and Molecular Genetics, School of Life Sciences, University of Nottingham, Nottingham, UK.
³⁴ Livestock Genetics Program, International Livestock Research Institute (ILRI), Addis Ababa, Ethiopia.
³⁵ Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark.
³⁶ China National Genebank, BGI-Shenzhen, Shenzhen, Guangdong, China.
³⁷ CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China. h.jianlin@cgiar.org.
³⁸ Livestock Genetics Program, International Livestock Research Institute (ILRI), Nairobi, Kenya. h.jianlin@cgiar.org.
³⁹ State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴⁰ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴¹ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴² State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴³ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴⁴ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴⁵ State Key Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.

^# Contributed equally.

PMID: 32581344
PMCID: PMC7395088
DOI: 10.1038/s41422-020-0349-y

863 genomes reveal the origin and domestication of chicken

Ming-Shan Wang et al. Cell Res. 2020 Aug.

. 2020 Aug;30(8):693-701.

doi: 10.1038/s41422-020-0349-y. Epub 2020 Jun 25.

Authors

Affiliations

¹ State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
² Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China.
³ Department of Ecology and Evolutionary Biology, Howard Hughes Medical Institute, University of California, Santa Cruz, Santa Cruz, CA, USA.
⁴ Zoological Survey of India, New Alipore, Kolkata, West Bengal, India.
⁵ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China.
⁶ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, China.
⁷ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
⁸ School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.
⁹ ArchaeoBioCenter and Department of Veterinary Sciences, Institute of Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, LMU Munich, Munich, Germany.
¹⁰ SNSB, Bavarian State Collection of Anthropology and Palaeoanatomy, Munich, Germany.
¹¹ School of Agriculture and Natural Resources, University of Phayao, Phayao, Thailand.
¹² College of Animal Science and Technology, Anhui Agricultural University, Hefei, Anhui, China.
¹³ Department of Animal Science, Shahid Bahonar University of Kerman, Kerman, Iran.
¹⁴ Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka.
¹⁵ Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Science (LIPI), Cibinong, Indonesia.
¹⁶ CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China.
¹⁷ Institute of Animal Husbandry, Biotechnology and Nature Conservation, University of Debrecen, Debrecen, Hungary.
¹⁸ Institute of Biotechnology, School of Agriculture, Shiraz University, Shiraz, Iran.
¹⁹ State Key Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming, Yunnan, China.
²⁰ Livestock Genetics Program, International Livestock Research Institute (ILRI), Nairobi, Kenya.
²¹ Department of Animal Science, Iowa State University, Ames, IA, USA.
²² College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.
²³ Dipartimento di Scienze Agrarie, Alimentarie Ambientali, University of Perugia, Perugia, Italy.
²⁴ BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Guangdong, China.
²⁵ Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture of China, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, Beijing, China.
²⁶ Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (CAS-SEABRI), Yezin, Myanmar.
²⁷ Bangladesh Agricultural University, Mymennsingh, Bangladesh.
²⁸ University of Agriculture Faisalabad, Faisalabad, Pakistan.
²⁹ Department of Animal Science, University of Peradeniya, Peradeniya, Sri Lanka.
³⁰ National Institute of Animal Husbandry, Hanoi, Vietnam.
³¹ Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, USA.
³² Howard Hughes Medical Institute, University of California, Santa Cruz, Santa Cruz, CA, USA.
³³ Cells, Organisms and Molecular Genetics, School of Life Sciences, University of Nottingham, Nottingham, UK.
³⁴ Livestock Genetics Program, International Livestock Research Institute (ILRI), Addis Ababa, Ethiopia.
³⁵ Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark.
³⁶ China National Genebank, BGI-Shenzhen, Shenzhen, Guangdong, China.
³⁷ CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China. h.jianlin@cgiar.org.
³⁸ Livestock Genetics Program, International Livestock Research Institute (ILRI), Nairobi, Kenya. h.jianlin@cgiar.org.
³⁹ State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴⁰ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴¹ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China. wudongdong@mail.kiz.ac.cn.
⁴² State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴³ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴⁴ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.
⁴⁵ State Key Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming, Yunnan, China. zhangyp@mail.kiz.ac.cn.

^# Contributed equally.

PMID: 32581344
PMCID: PMC7395088
DOI: 10.1038/s41422-020-0349-y

Erratum in

Author Correction: 863 genomes reveal the origin and domestication of chicken.
Wang MS, Thakur M, Peng MS, Jiang Y, Frantz LAF, Li M, Zhang JJ, Wang S, Peters J, Otecko NO, Suwannapoom C, Guo X, Zheng ZQ, Esmailizadeh A, Hirimuthugoda NY, Ashari H, Suladari S, Zein MSA, Kusza S, Sohrabi S, Kharrati-Koopaee H, Shen QK, Zeng L, Yang MM, Wu YJ, Yang XY, Lu XM, Jia XZ, Nie QH, Lamont SJ, Lasagna E, Ceccobelli S, Gunwardana HGTN, Senasige TM, Feng SH, Si JF, Zhang H, Jin JQ, Li ML, Liu YH, Chen HM, Ma C, Dai SS, Bhuiyan AKFH, Khan MS, Silva GLLP, Le TT, Mwai OA, Ibrahim MNM, Supple M, Shapiro B, Hanotte O, Zhang G, Larson G, Han JL, Wu DD, Zhang YP. Wang MS, et al. Cell Res. 2020 Sep;30(9):824-825. doi: 10.1038/s41422-020-0380-z. Cell Res. 2020. PMID: 32690900 Free PMC article.

Abstract

Despite the substantial role that chickens have played in human societies across the world, both the geographic and temporal origins of their domestication remain controversial. To address this issue, we analyzed 863 genomes from a worldwide sampling of chickens and representatives of all four species of wild jungle fowl and each of the five subspecies of red jungle fowl (RJF). Our study suggests that domestic chickens were initially derived from the RJF subspecies Gallus gallus spadiceus whose present-day distribution is predominantly in southwestern China, northern Thailand and Myanmar. Following their domestication, chickens were translocated across Southeast and South Asia where they interbred locally with both RJF subspecies and other jungle fowl species. In addition, our results show that the White Leghorn chicken breed possesses a mosaic of divergent ancestries inherited from other subspecies of RJF. Despite the strong episodic gene flow from geographically divergent lineages of jungle fowls, our analyses show that domestic chickens undergo genetic adaptations that underlie their unique behavioral, morphological and reproductive traits. Our study provides novel insights into the evolutionary history of domestic chickens and a valuable resource to facilitate ongoing genetic and functional investigations of the world's most numerous domestic animal.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

**Fig. 1. Sample distribution and phylogeny of *Gallus* taxa.**
a Map showing the geographic distribution of the sampling localities of all domestic chickens and wild jungle fowls across South Asia, Southeast Asia, and East Asia covered by our study. Map in the left bottom depicts the natural ranges of all jungle fowls (see details in Supplementary information, Fig. S1). b Maximum-likelihood tree depicting the evolutionary relationships among RJF subspecies and other three jungle fowl species. The numbers at the major branches are bootstrap values.

**Fig. 2. Domestic chickens were most likely derived from *G. g. spadiceus*.**
a Maximum-likelihood phylogenetic tree showing that domestic chickens form a monophyletic clade, with *G. g. spadiceus* being the closest wild progenitor. Black dots at nodes indicate ≥ 99% bootstrap support. Domestic chicken and RJF clades are collapsed and colored according to their geographic ranges and subspecies classifications. b PCA showing a closer genetic affinity between domestic chickens and *G. g. spadiceus*. *G. g. bankiva* was removed in this analysis because of its high divergence from other four RJF subspecies. RJF subspecies are denoted within rings.

**Fig. 3. The admixture and splitting of domestic chickens with RJF subspecies.**
a Outgroup-f3 statistics in the form of f3(*G. varius*; domestic chicken, RJF) show that all domestic chickens carry more genetic ancestry from *G. g. spadiceus* (GGS, higher f3 values) than from other four RJF subspecies. The estimated f3 value ± 3 standard errors are plotted. b MSMC plots show the divergence time between chicken and each of RJF subspecies. c MSMC plots show the splitting time between chicken and *G. g. spadiceus*. For clarity, we only present one result of MSMC for each population pair; more pairs were analyzed and shown in Supplementary information, Figs. S30, S31 and S48a. GGB *G. g. bankiva*, GGG *G. g. gallus*, GGM *G. g. murghi*, GGJ *G. g. jabouillei*.

**Fig. 4. Signatures of selection in domestic chickens.**
a Genomic landscape of selection signal in domestic chicken. From inner to outer, circle indicates signature of selection from each statistics: π-ratio (I), LSBL_j(chicken; *G. g. spadiceus*, *G. g. jabouillei*) (II), LSBL_m(chicken; *G. g. spadiceus*, *G. g. murghi*) (III), and chromosome scheme (IV), respectively. b Signals of positive selection on *FRGR1. FRGR1*-located region in chicken genome showed a lower diversity (π-ratio), lower heterozygosity (Hp) and higher differentiation (LSBL) compared with RJFs. Red dashed line indicates Z-transformed score of 3.3 for each statistic, and pink shadow depicts the location of *FGFR1* on the chr22.

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References

1. Lawler, A. Why did the chicken cross the world? Atria Books, New York (2014).
1. Larson G, Fuller DQ. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 2014;45:115–136.
1. Peters J, et al. Questioning new answers regarding Holocene chicken domestication in China. Proc. Natl Acad. Sci. USA. 2015;112:E2415. - PMC - PubMed
1. Tixier-Boichard M, Bed’hom B, Rognon X. Chicken domestication: from archeology to genomics. C. R. Biol. 2011;334:197–204. - PubMed
1. Miao YW, et al. Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity. 2013;110:277–282. - PMC - PubMed

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[1] Lawler, A. Why did the chicken cross the world? Atria Books, New York (2014).

[2] Lawler, A. Why did the chicken cross the world? Atria Books, New York (2014).

[3] Larson G, Fuller DQ. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 2014;45:115–136.

[4] Larson G, Fuller DQ. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 2014;45:115–136.

[5] Peters J, et al. Questioning new answers regarding Holocene chicken domestication in China. Proc. Natl Acad. Sci. USA. 2015;112:E2415. - PMC - PubMed

[6] Peters J, et al. Questioning new answers regarding Holocene chicken domestication in China. Proc. Natl Acad. Sci. USA. 2015;112:E2415. - PMC - PubMed

[7] Tixier-Boichard M, Bed’hom B, Rognon X. Chicken domestication: from archeology to genomics. C. R. Biol. 2011;334:197–204. - PubMed

[8] Tixier-Boichard M, Bed’hom B, Rognon X. Chicken domestication: from archeology to genomics. C. R. Biol. 2011;334:197–204. - PubMed

[9] Miao YW, et al. Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity. 2013;110:277–282. - PMC - PubMed

[10] Miao YW, et al. Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity. 2013;110:277–282. - PMC - PubMed

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863 genomes reveal the origin and domestication of chicken

Affiliations

863 genomes reveal the origin and domestication of chicken

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