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

Affiliation

Cao YH(1)(2), Xu SS(1)(2), Shen M(3)(4), Chen ZH(1)(2), Gao L(3)(4), Lv FH(1)(5), Xie XL(1)(2), Wang XH(3)(4), Yang H(3)(4), Liu CB(3)(4), Zhou P(3)(4), Wan PC(3)(4), Zhang YS(3)(4), Yang JQ(3)(4), Pi WH(3)(4), Hehua E(6), Berry DP(7), Barbato M(8), Esmailizadeh A(9), Nosrati M(10), Salehian-Dehkordi H(1)(2), Dehghani-Qanatqestani M(9), Dotsev AV(11), Deniskova TE(11), Zinovieva NA(11), Brem G(12), Štěpánek O(13), Ciani E(14), Weimann C(15), Erhardt G(15), Mwacharo JM(16), Ahbara A(17), Han JL(18)(19), Hanotte O(17)(20)(21), Miller JM(22), Sim Z(22)(23), Coltman D(22), Kantanen J(24), Bruford MW(25)(26), Lenstra JA(27), Kijas J(28), Li MH(1)(5).
Author information:
(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

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.