Whole-genome resequencing reveals molecular imprints of anthropogenic and natural selection in wild and domesticated sheep

De-Yin Zhang; Xiao-Xue Zhang; Fa-Di Li; Lv-Feng Yuan; Xiao-Long Li; Yu-Kun Zhang; Yuan Zhao; Li-Ming Zhao; Jiang-Hui Wang; Dan Xu; Jiang-Bo Cheng; Xiao-Bin Yang; Wen-Xin Li; Chang-Chun Lin; Bu-Bo Zhou; Wei-Min Wang

doi:10.24272/j.issn.2095-8137.2022.124

Volume 43 Issue 5

Sep. 2022

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2022 > 43(5): 695-705

De-Yin Zhang, Xiao-Xue Zhang, Fa-Di Li, Lv-Feng Yuan, Xiao-Long Li, Yu-Kun Zhang, Yuan Zhao, Li-Ming Zhao, Jiang-Hui Wang, Dan Xu, Jiang-Bo Cheng, Xiao-Bin Yang, Wen-Xin Li, Chang-Chun Lin, Bu-Bo Zhou, Wei-Min Wang. Whole-genome resequencing reveals molecular imprints of anthropogenic and natural selection in wild and domesticated sheep. Zoological Research, 2022, 43(5): 695-705. doi: 10.24272/j.issn.2095-8137.2022.124

Citation:

De-Yin Zhang, Xiao-Xue Zhang, Fa-Di Li, Lv-Feng Yuan, Xiao-Long Li, Yu-Kun Zhang, Yuan Zhao, Li-Ming Zhao, Jiang-Hui Wang, Dan Xu, Jiang-Bo Cheng, Xiao-Bin Yang, Wen-Xin Li, Chang-Chun Lin, Bu-Bo Zhou, Wei-Min Wang. Whole-genome resequencing reveals molecular imprints of anthropogenic and natural selection in wild and domesticated sheep. Zoological Research, 2022, 43(5): 695-705. doi: 10.24272/j.issn.2095-8137.2022.124

Citation:

De-Yin Zhang, Xiao-Xue Zhang, Fa-Di Li, Lv-Feng Yuan, Xiao-Long Li, Yu-Kun Zhang, Yuan Zhao, Li-Ming Zhao, Jiang-Hui Wang, Dan Xu, Jiang-Bo Cheng, Xiao-Bin Yang, Wen-Xin Li, Chang-Chun Lin, Bu-Bo Zhou, Wei-Min Wang. Whole-genome resequencing reveals molecular imprints of anthropogenic and natural selection in wild and domesticated sheep. Zoological Research, 2022, 43(5): 695-705. doi: 10.24272/j.issn.2095-8137.2022.124

PDF( 10145 KB)

Whole-genome resequencing reveals molecular imprints of anthropogenic and natural selection in wild and domesticated sheep

doi: 10.24272/j.issn.2095-8137.2022.124

1.
State Key Laboratory of Grassland Agro-Ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, Gansu 730020, China
2.
College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, Gansu 730070, China
3.
Engineering Laboratory of Sheep Breeding and Reproduction Biotechnology in Gansu Province, Minqin, Gansu 733300, China
4.
Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu 730046, China

Funds: This work was supported by the National Key R&D Program of China (2021YFD1300901), National Natural Science Foundation of China (31960653), West Light Foundation of the Chinese Academy of Sciences, and National Joint Research on Improved Breeds of Livestock and Poultry (19210365)

More Information

Corresponding author: E-mail: wangwm@gsau.edu.cn
Received Date: 2022-05-23
Accepted Date: 2022-07-05

Published Online: 2022-07-06

Publish Date: 2022-09-18

Abstract

Abstract

The abundance of domesticated sheep varieties and phenotypes is largely the result of long-term natural and artificial selection. However, there is limited information regarding the genetic mechanisms underlying phenotypic variation induced by the domestication and improvement of sheep. In this study, to explore genomic diversity and selective regions at the genome level, we sequenced the genomes of 100 sheep across 10 breeds and combined these results with publicly available genomic data from 225 individuals, including improved breeds, Chinese indigenous breeds, African indigenous breeds, and their Asian mouflon ancestor. Based on population structure, the domesticated sheep formed a monophyletic group, while the Chinese indigenous sheep showed a clear geographical distribution trend. Comparative genomic analysis of domestication identified several selective signatures, including IFI44 and IFI44L genes and PANK2 and RNF24 genes, associated with immune response and visual function. Population genomic analysis of improvement demonstrated that candidate genes of selected regions were mainly associated with pigmentation, energy metabolism, and growth development. Furthermore, the IFI44 and IFI44L genes showed a common selection signature in the genomes of 30 domesticated sheep breeds. The IFI44 c. 54413058 C>G mutation was selected for genotyping and population genetic validation. Results showed that the IFI44 polymorphism was significantly associated with partial immune traits. Our findings identified the population genetic basis of domesticated sheep at the whole-genome level, providing theoretical insights into the molecular mechanism underlying breed characteristics and phenotypic changes during sheep domestication and improvement.
- Sheep,
- Whole-genome resequencing,
- Selection signature analysis,
- Immunity,
- IFI44 gene

FullText(HTML)

References(48)

References

[1]	Alberto FJ, Boyer F, Orozco-Terwengel P, Streeter I, Servin B, de Villemereuil P, et al. 2018. Convergent genomic signatures of domestication in sheep and goats. Nature Communications, 9(1): 813. doi: 10.1038/s41467-018-03206-y
[2]	Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19(9): 1655−1664. doi: 10.1101/gr.094052.109
[3]	Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, et al. 2013. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature, 495(7441): 360−364. doi: 10.1038/nature11837
[4]	Axenovich T, Zorkoltseva I, Belonogova N, van Koolwijk LME, Borodin P, Kirichenko A, et al. 2011. Linkage and association analyses of glaucoma related traits in a large pedigree from a Dutch genetically isolated population. Journal of Medical Genetics, 48(12): 802−809. doi: 10.1136/jmedgenet-2011-100436
[5]	Bu DC, Luo HT, Huo PP, Wang ZH, Zhang S, He ZH, et al. 2021. KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Research, 49(W1): W317−W325. doi: 10.1093/nar/gkab447
[6]	Busse DC, Habgood-Coote D, Clare S, Brandt C, Bassano I, Kaforou M, et al. 2020. Interferon-induced protein 44 and interferon-induced protein 44-like restrict replication of respiratory syncytial virus. Journal of Virology, 94(18): e00297−20.
[7]	Cao YH, Xu SS, Shen M, Chen ZH, Gao L, Lv FH, et al. 2021. Historical introgression from wild relatives enhanced climatic adaptation and resistance to pneumonia in sheep. Molecular Biology and Evolution, 38(3): 838−855. doi: 10.1093/molbev/msaa236
[8]	Chen L, Guo WW, Ren LL, Yang MY, Zhao YF, Guo ZY, et al. 2016. A de novo silencer causes elimination of MITF-M expression and profound hearing loss in pigs. BMC Biology, 14: 52. doi: 10.1186/s12915-016-0273-2
[9]	Chen NB, Cai YD, Chen QM, Li R, Wang K, Huang YZ, et al. 2018. Whole-genome resequencing reveals world-wide ancestry and adaptive introgression events of domesticated cattle in East Asia. Nature Communications, 9(1): 2337. doi: 10.1038/s41467-018-04737-0
[10]	Chen ZH, Xu YX, Xie XL, Wang DF, Aguilar-Gómez D, Liu GJ, et al. 2021. Whole-genome sequence analysis unveils different origins of European and Asiatic mouflon and domestication-related genes in sheep. Communications Biology, 4(1): 1307. doi: 10.1038/s42003-021-02817-4
[11]	Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, Mainland I, et al. 2009. Revealing the history of sheep domestication using retrovirus integrations. Science, 324(5926): 532−536. doi: 10.1126/science.1170587
[12]	Daetwyler HD, Capitan A, Pausch H, Stothard P, van Binsbergen R, Brøndum RF, et al. 2014. Whole-genome sequencing of 234 bulls facilitates mapping of monogenic and complex traits in cattle. Nature Genetics, 46(8): 858−865. doi: 10.1038/ng.3034
[13]	Diamond J. 2002. Evolution, consequences and future of plant and animal domestication. Nature, 418(6898): 700−707. doi: 10.1038/nature01019
[14]	Fang X, Gamallat Y, Chen ZH, Mai HR, Zhou P, Sun CB, et al. 2021. Hypomorphic and hypermorphic mouse models of Fsip2 indicate its dosage-dependent roles in sperm tail and acrosome formation. Development, 148(11): dev199216. doi: 10.1242/dev.199216
[15]	Henderson JV, Wathes CM, Nicol CJ, White RP, Lines JA. 2000. Threat assessment by domestic ducklings using visual signals: implications for animal-machine interactions. Applied Animal Behaviour Science, 69(3): 241−253. doi: 10.1016/S0168-1591(00)00132-5
[16]	Hu XJ, Yang J, Xie XL, Lv FH, Cao YH, Li WR, et al. 2019. The genome landscape of tibetan sheep reveals adaptive introgression from argali and the history of early human settlements on the Qinghai-Tibetan Plateau. Molecular Biology and Evolution, 36(2): 283−303. doi: 10.1093/molbev/msy208
[17]	Jiang Y, Xie M, Chen WB, Talbot R, Maddox JF, Faraut T, et al. 2014. The sheep genome illuminates biology of the rumen and lipid metabolism. Science, 344(6188): 1168−1173. doi: 10.1126/science.1252806
[18]	Karlsson EK, Baranowska I, Wade CM, Hillbertz NHCS, Zody MC, Anderson N, et al. 2007. Efficient mapping of mendelian traits in dogs through genome-wide association. Nature Genetics, 39(11): 1321−1328. doi: 10.1038/ng.2007.10
[19]	Kodama Y, Shumway M, Leinonen R. 2012. The sequence read archive: explosive growth of sequencing data. Nucleic Acids Research, 40(D1): D54−D56. doi: 10.1093/nar/gkr854
[20]	Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1754−1760. doi: 10.1093/bioinformatics/btp324
[21]	Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352
[22]	Li MH, Tiirikka T, Kantanen J. 2014. A genome-wide scan study identifies a single nucleotide substitution in ASIP associated with white versus non-white coat-colour variation in sheep (Ovis aries). Heredity, 112(2): 122−131. doi: 10.1038/hdy.2013.83
[23]	Li MZ, Chen L, Tian SL, Lin Y, Tang QZ, Zhou XM, et al. 2017. Comprehensive variation discovery and recovery of missing sequence in the pig genome using multiple de novo assemblies. Genome Research, 27(5): 865−874. doi: 10.1101/gr.207456.116
[24]	Li X, Yang J, Shen M, Xie XL, Liu GJ, Xu YX, et al. 2020. Whole-genome resequencing of wild and domestic sheep identifies genes associated with morphological and agronomic traits. Nature Communications, 11(1): 2815. doi: 10.1038/s41467-020-16485-1
[25]	Liu WJ, Wu H, Wang L, Yang XY, Liu CY, He XJ, et al. 2019a. Homozygous loss-of-function mutations in FSIP2 cause male infertility with asthenoteratospermia. Journal of Genetics and Genomics, 46(1): 53−56. doi: 10.1016/j.jgg.2018.09.006
[26]	Liu XX, Zhang YL, Li YF, Pan JF, Wang DD, Chen WH, et al. 2019b. EPAS1 gain-of-function mutation contributes to high-altitude adaptation in Tibetan horses. Molecular Biology and Evolution, 36(11): 2591−2603. doi: 10.1093/molbev/msz158
[27]	Lv FH, Cao YH, Liu GJ, Luo LY, Lu R, Liu MJ, et al. 2022. Whole-genome resequencing of worldwide wild and domestic sheep elucidates genetic diversity, introgression, and agronomically important loci. Molecular Biology and Evolution, 39(2): msab353. doi: 10.1093/molbev/msab353
[28]	Minvielle F, Bed'hom B, Coville JL, Ito S, Inoue-Murayama M, Gourichon D. 2010. The "silver" Japanese quail and the MITF gene: causal mutation, associated traits and homology with the "blue" chicken plumage. BMC Genetics, 11: 15.
[29]	Parish CR. 2006. The role of heparan sulphate in inflammation. Nature Reviews Immunology, 6(9): 633−643. doi: 10.1038/nri1918
[30]	Peichlcu L. 1992. Topography of ganglion cells in the dog and wolf retina. The Journal of Comparative Neurology, 324(4): 603−620. doi: 10.1002/cne.903240412
[31]	Scher BD. 2000. World Watch List for Domestic Animal Diversity. 3^rd ed. Rome: Food and Agriculture Organization of the United Nations.
[32]	Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Research, 19(2): 327−335. doi: 10.1101/gr.073585.107
[33]	Wang K, Li MY, Hakonarson H. 2010. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 38(16): e164. doi: 10.1093/nar/gkq603
[34]	Wang MS, Thakur M, Peng MS, Jiang Y, Frantz LAF, Li M, et al. 2020. 863 genomes reveal the origin and domestication of chicken. Cell Research, 30(8): 693−701. doi: 10.1038/s41422-020-0349-y
[35]	Wang MS, Zhang RW, Su LY, Li Y, Peng MS, Liu HQ, et al. 2016. Positive selection rather than relaxation of functional constraint drives the evolution of vision during chicken domestication. Cell Research, 26(5): 556−573. doi: 10.1038/cr.2016.44
[36]	Wang WM, Zhang XX, Zhou X, Zhang YZ, La YF, Zhang Y, et al. 2019. Deep genome resequencing reveals artificial and natural selection for visual deterioration, plateau adaptability and high prolificacy in Chinese domestic sheep. Frontiers in Genetics, 10: 300. doi: 10.3389/fgene.2019.00300
[37]	Wei CH, Wang HH, Liu G, Wu MH, Cao JX, Liu Z, et al. 2015. Genome-wide analysis reveals population structure and selection in Chinese indigenous sheep breeds. BMC Genomics, 16(1): 194. doi: 10.1186/s12864-015-1384-9
[38]	Xu JY, Fu YH, Hu Y, Yin LL, Tang ZS, Yin D, et al. 2020. Whole genome variants across 57 pig breeds enable comprehensive identification of genetic signatures that underlie breed features. Journal of Animal Science and Biotechnology, 11(1): 115. doi: 10.1186/s40104-020-00520-8
[39]	Yang J, Li WR, Lv FH, He SG, Tian SL, Peng WF, et al. 2016. Whole-genome sequencing of native sheep provides insights into rapid adaptations to extreme environments. Molecular Biology and Evolution, 33(10): 2576−2592. doi: 10.1093/molbev/msw129
[40]	Yokoyama S. 2002. Molecular evolution of color vision in vertebrates. Gene, 300(1-2): 69−78. doi: 10.1016/S0378-1119(02)00845-4
[41]	Yang J, Lee SH, Goddard ME, Visscher PM. 2011. GCTA: a tool for genome-wide complex trait analysis. The American Journal of Human Genetics, 88(1): 76−82.
[42]	Zeder MA. 2008. Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proceedings of the National Academy of Sciences of the United States of America, 105(33): 11597−11604. doi: 10.1073/pnas.0801317105
[43]	Zhang DL, Huang JL, Sun XD, Chen HG, Huang S, Yang J, et al. 2021a. Targeting local lymphatics to ameliorate heterotopic ossification via FGFR3-BMPR1a pathway. Nature Communications, 12(1): 4391. doi: 10.1038/s41467-021-24643-2
[44]	Zhang DY, Zhang XX, Li FD, Yuan LF, Zhang YK, Li XL, et al. 2021b. Polymorphisms in ovine ME1 and CA1 genes and their association with feed efficiency in Hu sheep. Journal of Animal Breeding and Genetics, 138(5): 589−599. doi: 10.1111/jbg.12541
[45]	Zhang DY, Zhang XX, Li FD, Zhao Y, Li XL, Wang JH, et al. 2022. Expression profiles of the ovine IL18 gene and association of its polymorphism with hematologic parameters in Hu lambs. Frontiers in Veterinary Science, 9: 925928. doi: 10.3389/fvets.2022.925928
[46]	Zhang XY, Weng MJ, Chen ZQ. 2021c. Fibroblast growth factor 9 (FGF9) negatively regulates the early stage of chondrogenic differentiation. PLoS One, 16(2): e0241281. doi: 10.1371/journal.pone.0241281
[47]	Zhao YX, Yang J, Lv FH, Hu XJ, Xie XL, Zhang M, et al. 2017. Genomic reconstruction of the history of native sheep reveals the peopling patterns of nomads and the expansion of early pastoralism in East Asia. Molecular Biology and Evolution, 34(9): 2380−2395. doi: 10.1093/molbev/msx181
[48]	Zhou ZK, Li M, Cheng H, Fan WL, Yuan ZR, Gao Q, et al. 2018. An intercross population study reveals genes associated with body size and plumage color in ducks. Nature Communications, 9(1): 2648. doi: 10.1038/s41467-018-04868-4