Large-scale genomic analysis reveals the genetic cost of chicken domestication

BMC Biology

Abul Kashem Fazlul Haque Bhuiyan¹  Jian-Lin Han²  Olivier Hanotte³  Yun-Mei Wang⁴  Muhammad Sajjad Khan⁵  Xing Guo⁶  Hamed Kharrati-Koopaee⁷  Gamamada Liyanage Lalanie Pradeepa Silva⁸  Rachel Meyer⁹  Emiliano Lasagna^1,10  Simone Ceccobelli^1,10  Thilina Madusanka Senasig^1,11  Humpita Gamaralalage Thilini Nisanka Gunwardana^1,11  Beth Shapiro^1,12  Szilvia Kusza^1,13  Zhu-Qing Zheng^1,14  Ming Li^1,15  Yu Jiang^1,15  Hao Zhang^1,16  Okeyo A. Mwai^1,17  Mohamed Nawaz Mohamed Ibrahim^1,17  Moch Syamsul Arifin Zein^1,18  Hidayat Ashari^1,19  Le Thi Thuy^2,20  Chatmongkon Suwannapoom^2,21  Shao-Hong Feng^2,22  Guojie Zhang^2,23  Ali Esmailizadeh^2,24  Nalini Yasoda Hirimuthugoda^2,25  Sheng Wang^2,26  Lin Zeng^2,26  Ting-Ting Yin^2,26  Jin-Jin Zhang^2,26  Min-Min Yang^2,26  Min-Sheng Peng^2,26  Ming-Li Li^2,26  Dong-Dong Wu^2,27  Xue-Mei Lu^2,27  Ya-Ping Zhang^2,28  Ming-Shan Wang^2,29  Mukesh Thakur^3,30  Mirte Bosse^3,31  Kai-Xing Qu^3,32 

[1] Bangladesh Agricultural University, 2202, Mymensingh, Bangladesh;CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), 100193, Beijing, China;Livestock Genetics Program, International Livestock Research Institute (ILRI), 00100, Nairobi, Kenya;Cells, Organisms and Molecular Genetics, School of Life Sciences, University of Nottingham, NG7 2RD, Nottingham, UK;Livestock Genetics Program, International Livestock Research Institute (ILRI), P.O. Box 5689, Addis Ababa, Ethiopia;Center for Neurobiology and Brain Restoration, Skolkovo Institute of Science and Technology, 143026, Moscow, Russia;Cholistan University of Veterinary and Animal Sciences, Bahawalpur, Pakistan;College of Animal Science and Technology, Anhui Agricultural University, 230036, Hefei, China;Department of Animal Science, Shahid Bahonar University of Kerman, P.O. Box 76169133, Kerman, Iran;Institute of Biotechnology, School of Agriculture, Shiraz University, P.O. Box 1585, Shiraz, Iran;Department of Animal Science, University of Peradeniya, 20400, Peradeniya, Sri Lanka;Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 95064, Santa Cruz, CA, USA;Dipartimento di Scienze Agrarie, Alimentarie Ambientali, University of Perugia, 06123, Perugia, Italy;Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka;Howard Hughes Medical Institute, University of California Santa Cruz, 95064, Santa Cruz, CA, USA;Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 95064, Santa Cruz, CA, USA;Institute of Animal Husbandry, Biotechnology and Nature Conservation, University of Debrecen, H-4032, Debrecen, Hungary;Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, The Cooperative Innovation Center for Sustainable Pig Production, Ministry of Education, Huazhong Agricultural University, 430070, Wuhan, China;Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, 712100, Yangling, China;Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, Ministry of Agriculture of China, 100193, Beijing, China;Livestock Genetics Program, International Livestock Research Institute (ILRI), 00100, Nairobi, Kenya;Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Science (LIPI), Cibinong, 16911, Bogor, Indonesia;Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Science (LIPI), Cibinong, 16911, Bogor, Indonesia;CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), 100193, Beijing, China;National Institute of Animal Husbandry, Hanoi, Vietnam;School of Agriculture and Natural Resources, University of Phayao, 56000, Phayao, Thailand;Unit of Excellence on Biodiversity and Natural Resources Management, University of Phayao, 56000, Phayao, Thailand;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;BGI-Shenzhen, Beishan Industrial Zone, 518083, Shenzhen, China;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650204, Kunming, China;China National Genebank, BGI-Shenzhen, 518083, Shenzhen, China;Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-1870, Copenhagen, Denmark;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Department of Animal Science, Shahid Bahonar University of Kerman, P.O. Box 76169133, Kerman, Iran;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Kunming College of Life Science, University of Chinese Academy of Sciences, 650204, Kunming, China;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Kunming College of Life Science, University of Chinese Academy of Sciences, 650204, Kunming, China;Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650204, Kunming, China;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Kunming College of Life Science, University of Chinese Academy of Sciences, 650204, Kunming, China;Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650204, Kunming, China;State Key Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, 650091, Kunming, China;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Kunming College of Life Science, University of Chinese Academy of Sciences, 650204, Kunming, China;Howard Hughes Medical Institute, University of California Santa Cruz, 95064, Santa Cruz, CA, USA;Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 95064, Santa Cruz, CA, USA;State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China;Zoological Survey of India, New Alipore, 700053, Kolkata, West Bengal, India;Wageningen University & Research - Animal Breeding and Genomics, 6708 PB, Wageningen, The Netherlands;Yunnan Academy of Grassland and Animal Science, 650212, Kunming, China;

关键词: Domestication;    Bottleneck;    Genetic load;    Deleterious mutation;    Domestic chicken;   

DOI  :  10.1186/s12915-021-01052-x

来源: Springer

【 摘 要 】

BackgroundSpecies domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of domesticated species evolve and how expensive the genetic cost underlying domestication is remain poorly understood. Here, we investigated the demographic history and genetic load of chicken domestication.ResultsWe analyzed a dataset comprising over 800 whole genomes from both indigenous chickens and wild jungle fowls. We show that despite having a higher genetic diversity than their wild counterparts (average π, 0.00326 vs. 0.00316), the red jungle fowls, the present-day domestic chickens experienced a dramatic population size decline during their early domestication. Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the “cost of domestication” hypothesis. Particularly, we find that 62.4% of deleterious SNPs in domestic chickens are maintained in heterozygous states and masked as recessive alleles, challenging the power of modern breeding programs to effectively eliminate these genetic loads. Finally, we suggest that positive selection decreases the incidence but increases the frequency of deleterious SNPs in domestic chicken genomes.ConclusionThis study reveals a new landscape of demographic history and genomic changes associated with chicken domestication and provides insight into the evolutionary genomic profiles of domesticated animals managed under modern human selection.

【 授权许可】

CC BY