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

Wang M.-S., Zhang J.-J., Guo X., Li M., Meyer R., Ashari H., Zheng Z.-Q., Wang S., Peng M.-S., Jiang Y., Thakur M., Suwannapoom C., Esmailizadeh A., Hirimuthugoda N.Y., Zein M.S.A., Kusza S., Kharrati-Koopaee H., Zeng L., Wang Y.-M., Yin T.-T., Yang M.-M., Li M.-L., Lu X.-M., Lasagna E., Ceccobelli S., Gunwardana H.G.T.N., Senasig T.M., Feng S.-H., Zhang H., Bhuiyan A.K.F.H., Khan M.S., Silva G.L.L.P., Thuy L.T., Mwai O.A., Ibrahim M.N.M., Zhang G., Qu K.-X., Hanotte O., Shapiro B., Bosse M., Wu D.-D., Han J.-L., Zhang Y.-P.

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


Abstract

Background: Species 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. Results: We 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. Conclusion: This 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. © 2021, The Author(s).

Bottleneck; Deleterious mutation; Domestic chicken; Domestication; Genetic load


Journal

BMC Biology

Publisher: BioMed Central Ltd

Volume 19, Issue 1, Art No 118, Page – , Page Count


Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85108111361&doi=10.1186%2fs12915-021-01052-x&partnerID=40&md5=3f212b0576186f74855c26448bcf41c5

doi: 10.1186/s12915-021-01052-x

Issn: 17417007

Type: All Open Access, Gold, Green


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