TY - JOUR

T1 - Large-scale genomic analysis reveals the genetic cost of chicken domestication

AU - Wang, Ming-Shan

AU - Zhang, Jin-Jin

AU - Guo, Xing

AU - Li, Ming

AU - Meyer, Rachel

AU - Ashari, Hidayat

AU - Zheng, Zhu-Qing

AU - Wang, Sheng

AU - Peng, Min-Sheng

AU - Jiang, Yu

AU - Thakur, Mukesh

AU - Suwannapoom, Chatmongkon

AU - Esmailizadeh, Ali

AU - Hirimuthugoda, Nalini Yasoda

AU - Zein, Moch Syamsul Arifin

AU - Kusza, Szilvia

AU - Kharrati-Koopaee, Hamed

AU - Zeng, Lin

AU - Wang, Yun-Mei

AU - Yin, Ting-Ting

AU - Yang, Min-Min

AU - Li, Ming-Li

AU - Lu, Xue-Mei

AU - Lasagna, Emiliano

AU - Ceccobelli, Simone

AU - Gunwardana, Humpita Gamaralalage Thilini Nisanka

AU - Senasig, Thilina Madusanka

AU - Feng, Shao-Hong

AU - Zhang, Hao

AU - Bhuiyan, Abul Kashem Fazlul Haque

AU - Khan, Muhammad Sajjad

AU - Silva, Gamamada Liyanage Lalanie Pradeepa

AU - Thuy, Le Thi

AU - Mwai, Okeyo A.

AU - Ibrahim, Mohamed Nawaz Mohamed

AU - Zhang, Guojie

AU - Qu, Kai-Xing

AU - Hanotte, Olivier

AU - Shapiro, Beth

AU - Bosse, Mirte

AU - Wu, Dong-Dong

AU - Han, Jian-Lin

AU - Zhang, Ya-Ping

N1 - Funding Information: We thank Laurent A. F. Frantz and Greger Larson for their valuable comments on this study. We thank Jing-Fang Si for his help with the SMC++ analysis. We also thank Shao-Bin Xu and Xiu-Zhen Yang from the High-Performance Computing Center at Kunming Institute of Zoology, CAS, for their support on the computational analyses. Funding Information: This work was supported by the National Natural Science Foundation of China (31771415, 31801054, U1902204, 31822048, and 31771405), the Strategic Priority Research Program of the Chinese Academy of Sciences (CAS, XDA2004010301), and the West Light Foundation of CAS (Y902401081). C.S. also thanks to the support of the Unit of Excellence 2021 on Biodiversity and Natural Resources Management, University of Phayao, Thailand. The Youth Innovation Promotion Association of CAS also provided support to M.-S.W. Animal Branch of the Germplasm Bank of Wild Species of CAS (the large research infrastructure funding) also supported this project. The Chinese Government’s contribution to CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources in Beijing (2021-YWF-ZX-02) is appreciated. K.-X.Q was supported by the Young and Middle-aged Academic Technology Leader Backup Talent Cultivation Program in Yunnan Province (2018HB045). This publication has been prepared within the framework of the UNEP/GEF project “Development and application of decision-support tools to conserve and sustainably use genetic diversity in indigenous livestock and wild relatives” and it contributes to the CGIAR Research Program on Livestock. Publisher Copyright: © 2021, The Author(s).

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

KW - Bottleneck

KW - Deleterious mutation

KW - Domestic chicken

KW - Domestication

KW - Genetic load

U2 - 10.1186/s12915-021-01052-x

DO - 10.1186/s12915-021-01052-x

M3 - Journal article

C2 - 34130700

AN - SCOPUS:85108111361

VL - 19

JO - B M C Biology

JF - B M C Biology

SN - 1741-7007

M1 - 118

ER -