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

Authors

Ming Shan Wang, Kunming Institute of Zoology Chinese Academy of Sciences
Jin Jin Zhang, Kunming Institute of Zoology Chinese Academy of SciencesFollow
Xing Guo, Anhui Agricultural University
Ming Li, Northwest A&F University
Rachel Meyer, University of California, Santa Cruz
Hidayat Ashari, Museum Zoologicum Bogoriense
Zhu Qing Zheng, Huazhong Agricultural UniversityFollow
Sheng Wang, Kunming Institute of Zoology Chinese Academy of Sciences
Min Sheng Peng, Kunming Institute of Zoology Chinese Academy of Sciences
Yu Jiang, Northwest A&F University
Mukesh Thakur, Kunming Institute of Zoology Chinese Academy of Sciences
Chatmongkon Suwannapoom, University of Phayao
Ali Esmailizadeh, Kunming Institute of Zoology Chinese Academy of Sciences
Nalini Yasoda Hirimuthugoda, Kunming Institute of Zoology Chinese Academy of Sciences
Moch Syamsul Arifin Zein, Museum Zoologicum BogorienseFollow
Szilvia Kusza, Debreceni Egyetem
Hamed Kharrati-Koopaee, Shahid Bahonar University of Kerman
Lin Zeng, Kunming Institute of Zoology Chinese Academy of SciencesFollow
Yun Mei Wang, Skolkovo Institute of Science and Technology
Ting Ting Yin, Kunming Institute of Zoology Chinese Academy of Sciences
Min Min Yang, Kunming Institute of Zoology Chinese Academy of SciencesFollow
Ming Li Li, Kunming Institute of Zoology Chinese Academy of Sciences
Xue Mei Lu, Kunming Institute of Zoology Chinese Academy of Sciences
Emiliano Lasagna, Università degli Studi di Perugia
Simone Ceccobelli, Università degli Studi di Perugia
Humpita Gamaralalage Thilini Nisanka Gunwardana, Faculty of Agriculture University of Ruhuna
Thilina Madusanka Senasig, Faculty of Agriculture University of Ruhuna
Shao Hong Feng, Kunming Institute of Zoology Chinese Academy of SciencesFollow
Hao Zhang, China Agricultural University
Abul Kashem Fazlul Haque Bhuiyan, Bangladesh Agricultural University
Muhammad Sajjad Khan, University of Veterinary and Animal Sciences, Lahore
Gamamada Liyanage Lalanie Pradeepa Silva, University of Peradeniya
Le Thi Thuy, National Institute of Animal Husbandry Hanoi

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.

Publication Title

BMC Biology

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