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

Ming Shan Wang, Jin Jin Zhang, Xing Guo, Ming Li, Rachel Meyer, Hidayat Ashari, Zhu Qing Zheng, Sheng Wang, Min Sheng Peng, Yu Jiang, Mukesh Thakur, Chatmongkon Suwannapoom, Ali Esmailizadeh, Nalini Yasoda Hirimuthugoda, Moch Syamsul Arifin Zein, Szilvia Kusza, Hamed Kharrati-Koopaee, Lin Zeng, Yun Mei Wang, Ting Ting YinMin Min Yang, Ming Li Li, Xue Mei Lu, Emiliano Lasagna, Simone Ceccobelli, Humpita Gamaralalage Thilini Nisanka Gunwardana, Thilina Madusanka Senasig, Shao Hong Feng, Hao Zhang, Abul Kashem Fazlul Haque Bhuiyan, Muhammad Sajjad Khan, Gamamada Liyanage Lalanie Pradeepa Silva, Le Thi Thuy, Okeyo A. Mwai, Mohamed Nawaz Mohamed Ibrahim, Guojie Zhang, Kai Xing Qu, Olivier Hanotte, Beth Shapiro, Mirte Bosse, Dong Dong Wu*, Jian Lin Han, Ya Ping Zhang

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

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.

Original languageEnglish
Article number118
JournalBMC Biology
Volume19
Issue number1
DOIs
Publication statusPublished - 16 Jun 2021

Keywords

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

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