Historical Introgression from Wild Relatives Enhanced Climatic Adaptation and Resistance to Pneumonia in Sheep

Author:

Cao Yin-Hong12,Xu Song-Song12,Shen Min34,Chen Ze-Hui12,Gao Lei34,Lv Feng-Hua15,Xie Xing-Long12,Wang Xin-Hua34,Yang Hua34,Liu Chang-Bin34,Zhou Ping34,Wan Peng-Cheng34,Zhang Yun-Sheng34,Yang Jing-Quan34,Pi Wen-Hui34,Hehua EEr6,Berry Donagh P7,Barbato Mario8,Esmailizadeh Ali9,Nosrati Maryam10,Salehian-Dehkordi Hosein12,Dehghani-Qanatqestani Mostafa9,Dotsev Arsen V11,Deniskova Tatiana E11,Zinovieva Natalia A11,Brem Gottfried12,Štěpánek Ondřej13,Ciani Elena14,Weimann Christina15,Erhardt Georg15,Mwacharo Joram M16,Ahbara Abulgasim17,Han Jian-Lin1819,Hanotte Olivier172021,Miller Joshua M22,Sim Zijian2223,Coltman David22,Kantanen Juha24,Bruford Michael W2526,Lenstra Johannes A27,Kijas James28,Li Meng-Hua15ORCID

Affiliation:

1. CAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences (CAS), Beijing, China

2. College of Life Sciences, University of Chinese Academy of Sciences (UCAS), Beijing, China

3. Institute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Sciences, Shihezi, China

4. Xinjiang Academy of Agricultural and Reclamation Sciences, State Key Laboratory of Sheep Genetic Improvement and Healthy Breeding, Shihezi, China

5. College of Animal Science and Technology, China Agricultural University, Beijing, China

6. Institute of Animal Science, Ningxia Academy of Agriculture and Forestry Sciences, Hui Autonomous Region, Yinchuan, Ningxia, China

7. Animal and Grassland Research and Innovation Centre, Teagasc, Moorepark, Fermoy, Co. Cork, Ireland

8. Department of Animal Sciences, Food and Nutrition, Università Cattolica del Sacro Cuore, Piacenza, Italy

9. Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

10. Department of Agriculture, Payame Noor University, Tehran, Iran

11. L.K. Ernst Federal Science Center for Animal Husbandry, Moscow Region, Podolsk, Russian Federation

12. Institute of Animal Breeding and Genetics, University of Veterinary Medicine, Vienna, Austria

13. Department of Virology, State Veterinary Institute Jihlava, Jihlava, Czech Republic

14. Dipartimento di Bioscienze, Biotecnologie e Biofarmaceutica, Università degli Studi di Bari Aldo 24, Moro, Bari, Italy

15. Department of Animal Breeding and Genetics, Justus-Liebig-University Giessen, Giessen, Germany

16. Small Ruminant Genomics, International Center for Agricultural Research in the Dry Areas (ICARDA), Addis Ababa, Ethiopia

17. School of Life Sciences, University of Nottingham, University Park, Nottingham, United Kingdom

18. CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China

19. Livestock Genetics Program, International Livestock Research Institute (ILRI), Nairobi, Kenya

20. Livestock Genetics Program, International Livestock Research Institute (ILRI), Addis Abeba, Ethiopia

21. Center for Tropical Livestock Genetics and Health (CTLGH), The Roslin Institute, University of Edinburgh, Easter Bush, Midlothian, United Kingdom

22. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

23. Fish and Wildlife Enforcement Branch Forensic Unit, Government of Alberta, Edmonton, AB, Canada

24. Production Systems, Natural Resources Institute Finland (Luke), Jokioinen, Finland

25. School of Biosciences, Cardiff University, Cathays Park, Cardiff, United Kingdom

26. Sustainable Places Research Institute, Cardiff University, Cardiff, United Kingdom

27. Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands

28. Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Queensland Bioscience Precinct, St Lucia, Brisbane, QLD, Australia

Abstract

Abstract How animals, particularly livestock, adapt to various climates and environments over short evolutionary time is of fundamental biological interest. Further, understanding the genetic mechanisms of adaptation in indigenous livestock populations is important for designing appropriate breeding programs to cope with the impacts of changing climate. Here, we conducted a comprehensive genomic analysis of diversity, interspecies introgression, and climate-mediated selective signatures in a global sample of sheep and their wild relatives. By examining 600K and 50K genome-wide single nucleotide polymorphism data from 3,447 samples representing 111 domestic sheep populations and 403 samples from all their seven wild relatives (argali, Asiatic mouflon, European mouflon, urial, snow sheep, bighorn, and thinhorn sheep), coupled with 88 whole-genome sequences, we detected clear signals of common introgression from wild relatives into sympatric domestic populations, thereby increasing their genomic diversities. The introgressions provided beneficial genetic variants in native populations, which were significantly associated with local climatic adaptation. We observed common introgression signals of alleles in olfactory-related genes (e.g., ADCY3 and TRPV1) and the PADI gene family including in particular PADI2, which is associated with antibacterial innate immunity. Further analyses of whole-genome sequences showed that the introgressed alleles in a specific region of PADI2 (chr2: 248,302,667–248,306,614) correlate with resistance to pneumonia. We conclude that wild introgression enhanced climatic adaptation and resistance to pneumonia in sheep. This has enabled them to adapt to varying climatic and environmental conditions after domestication.

Funder

National Key Research and Development Program-Key Projects of International Innovation Cooperation between Governments

National Natural Science Foundation of China

External Cooperation Program of Chinese Academy of Sciences

Second Tibetan Plateau Scientific Expedition and Research Program

Taishan Scholars Program of Shandong Province

Russian Ministry of Higher Education and Science

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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