Abstract
Understanding how evolutionary factors related to climate adaptation and human selection have influenced the genetic architecture of domesticated animals is of great interest in biology. In the current study, by using 304 whole genomes from different geographical regions (including Europe, north Africa, Southwest Asia, east Asia, west Africa, south Asia, east Africa, Australia and Turkey), We evaluate global sheep population dynamics in terms of genetic variation and population structure. We further conducted comparative population analysis to study the genetic underpinnings of climate adaption to local environments and also morphological traits. In order to identify genomic signals under selection, we applied fixation index (FST) and also nucleotide diversity (θπ) statistical measurements. Our results revealed several candidate genes on different chromosomes under selection for local climate adaptation (e.g. HOXC12, HOXC13, IRF1, FGD2 and GNAQ), body size (PDGFA, HMGA2, PDE3A) and also morphological related traits (RXFP2). The discovered candidate genes may offer newel insights into genetic underpinning of regional adaptation and commercially significant features in local sheep.
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Data availability
The merged VCF file is available from the corresponding author upon reasonable request. The other data generated in this study have been presented as supplementary information with this manuscript. The fastq files used in this research work were acquired from the public sequence database.
References
Abdoli, R., Mirhoseini, S.Z., Ghavi Hossein-Zadeh, N., Zamani, P., Moradi, M. H., Ferdosi, M. H., Sargolzaei, M., Gondro, C. (2023). Runs of homozygosity and cross-generational inbreeding of Iranian fat-tailed sheep. Heredity, https://doi.org/10.1038/s41437-023-00611-y
Ahbara, A. M., Musa, H. H., et al. (2022). Natural adaptation and human selection of northeast African sheep genomes. Genomics, 114, 110448. https://doi.org/10.1016/j.ygeno.2022.110448
Aldersey, J. E., Sonstegard, T. S., Williams, J. L., Bottema, C. D. K. (2020). Understanding the effects of the bovine POLLED variants. Animal Genetics, 51(2), 166-176.https://doi.org/10.1111/age.12915
Alexander, D. H., Novembre, J., Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655–1664.https://doi.org/10.1101/gr.094052.109
Aljubouri, T. R. S., Al-Shuhaib, M. B. S., Javadmanesh, A. (2020). HMGA2 gene polymorphisms and their effects on main growth traits indices in Awassi and Karakul sheep. Agriculture and Natural Resources, 587–594. https://doi.org/10.34044/j.anres.2020.54.6.03
Al-Mamun, H. A., A Clark, S., Kwan, P. et al. (2015). Genome-wide linkage disequilibrium and genetic diversity in five populations of Australian domestic sheep. Genetics Selection Evolution, 47, 90.https://doi.org/10.1186/s12711-015-0169-6
Almasi, M., Zamani, P., Mirhoseini, S. Z., Moradi, M. H. (2021). Genome-wide association study for postweaning weight traits in Lori-Bakhtiari sheep. Tropical Animal Health and Production, 14, 163.https://doi.org/10.1007/s11250-021-02595-5
Anderssona, L., Purugganan, M. (2022). Molecular genetic variation of animals and plants under domestication. Proceedings of the National Academy of Sciences, 119, e2122150119.https://doi.org/10.1073/pnas.2122150119
Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. 1-1. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Asadollahpour Nanaei, H., Dehghani Qanatqestani, M., Esmailizadeh, A. (2020). Whole-genome resequencing reveals selection signatures associated with milk production traits in African Kenana dairy zebu cattle. Genomics, 112(1), 880-885. https://doi.org/https://doi.org/10.1016/j.ygeno.2019.06.002
Asadollahpour Nanaei, H., Kharrati-Koopaee, H., Esmailizadeh, A. (2022). Genetic diversity and signatures of selection for heat tolerance and immune response in Iranian native chickens. BMC Genomics, 23, 224 https://doi.org/https://doi.org/10.1186/s12864-022-08434-7
Asadollahpour Nanaei, H., Cai, Y., Alshawi, A., Wen, J., Hussain, T., Fu, W. W., Xu, N. Y., Essa, A., Lenstra J. A., Wang, X., Jiang, Y. (2023). Genomic analysis of indigenous goats in Southwest Asia reveals evidence of ancient adaptive introgression related to desert climate. Zoological Research. 18, 20-29.https://doi.org/10.24272/j.issn.2095-8137.2022.242
Ashraf, S., Nazemi, A., AghaKouchak, A. (2021). Anthropogenic drought dominates groundwater depletion in Iran. Scientific Reports, 11, 9135. https://doi.org/https://doi.org/10.1038/s41598-021-88522-y
Belhadj Slimen, I., Najar, T., Ghram, A., Abdrrabba, M. (2016). Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. Journal of Animal Physiology and Animal Nutrition, 100, 401-412. https://doi.org/https://doi.org/10.1111/jpn.12379
Berg, P., Moseley, C., Haerter, J. O. (2013). Strong increase in convective precipitation in response to higher temperatures. Nature Geoscience, 6, 181–185. https://doi.org/https://doi.org/10.1038/ngeo1731
Bertolini, F., Servin, B., et al. (2018). Signatures of selection and environmental adaptation across the goat genome. Genetics Selection Evolution, 50, 57. https://doi.org/https://doi.org/10.1186/s12711-018-0421-y
Bolger, A. M., Lohse, M., Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–20. https://doi.org/https://doi.org/10.1093/bioinformatics/btu170
Bouwman, A., Daetwyler, H. D., et al. (2018). Meta-analysis of genome-wide association studies for cattle stature identifies common genes that regulate body size in mammals. Nature Genetics, 50, 362–367.https://doi.org/10.1038/s41588-018-0056-5
Cao, Y. H., Xu, S. S., et al. (2020). Historical Introgression from Wild Relatives Enhanced Climatic Adaptation and Resistance to Pneumonia in Sheep. Molecular Biology and Evolution, 38, 838–855.https://doi.org/10.1093/molbev/msaa236
Carabaño, M. J., Ramón, M., Menéndez-Buxadera, A., Molina, A., Díaz C. (2019). Selecting for heat tolerance. Animal Frontiers, 9 (1), 62–68.https://doi.org/10.1093/af/vfy033
Ceballos, F., Joshi, P., Clark, D. et al. (2018). Runs of homozygosity: windows into population history and trait architecture. Nature Reviews Genetics, 19, 220–234.https://doi.org/10.1038/nrg.2017.109
Chen, H., Patterson, N., Reich, D. (2010). Population differentiation as a test for selective sweeps. Genome Research, 20, 393–402.https://doi.org/10.1101/gr.100545.109
Chen, ZH., Xu, YX., Xie, XL. et al. (2021). Whole-genome sequence analysis unveils different origins of European and Asiatic mouflon and domestication-related genes in sheep. Communications Biology, 4, 1307.https://doi.org/10.1038/s42003-021-02817-4
Chung, J., Zhang, X., et al. (2018). High mobility group A2 (HMGA2) deficiency in pigs leads to dwarfism, abnormal fetal resource allocation, and cryptorchidism. Proceedings of the National Academy of Sciences, 115(21), 5420–5425.https://doi.org/10.1073/pnas.172163011
Creech, T. G., Epps, C. W., et al. (2020). Genetic and Environmental Indicators of Climate Change Vulnerability for Desert Bighorn Sheep. Frontiers in Ecology and Evolution, 8, https://doi.org/10.3389/fevo.2020.00279
Davies, C. J., Fan, Z., et al. (2022). Development and characterization of type I interferon receptor knockout sheep: A model for viral immunology and reproductive signaling. Frontiers in Genetics, 14, 13:986316.https://doi.org/10.3389/fgene.2022.986316
Du, F. X., Clutter, A. C., Lohuis, M. M. (2007). Characterizing linkage disequilibrium in pig populations. International Journal of Biological Sciences, 3(3), 166-78.https://doi.org/10.7150/ijbs.3.166
Fariello, M. I., Servin, B., Tosser-Klopp, G., Rupp, R., Moreno, C. International sheep genomics consortium, et al. (2014). Selection signatures in worldwide sheep populations. PLoS ONE, 9(8): 103813. https://doi.org/10.1371/journal.pone.0103813
Feng, H., Zhang, Y. B., Gui, J. F., Lemon, S. M., Yamane, D. (2021). Interferon regulatory factor 1 (IRF1) and anti-pathogen innate immune responses. PLoS Pathogens, 17(1): e1009220https://doi.org/10.1371/journal.ppat.1009220
Gao, L., Emond, M. J., et al. (2016). Whole-exome sequencing identifies rare variants in atp8b4 as a risk factor for systemic sclerosis. Arthritis Rheumatol, 68, 191-200.https://doi.org/10.1002/art.39449
Gray, M. M., Granka, J. M., Bustamante, C. D., Sutter, N. B., Boyko, A. R., Zhu, L., Ostrander, E. A., Wayne, R. K. (2009). Linkage disequilibrium and demographic history of wild and domestic canids. Genetics, 181(4), 1493-505.
Jiang-hong, W., Wen-guang, Z., Jin-quan, L., Jun Y., Yan-jun Z. (2009). Hoxc13 expression pattern in cashmere goat skin during hair follicle development. Agricultural Sciences in China, 8, 491-496.https://doi.org/10.1016/S1671-2927(08)60237-0
Kaiser, S., Hennessy, M. B., Sachser, N. (2015). Domestication affects the structure, development and stability of biobehavioural profiles. Frontiers in Zoology, (Suppl 1), S19. https://doi.org/10.1186/1742-9994-12-S1-S19
Kaniewski, D., Van Campo, E., Weiss, H. (2012). Drought is a recurring challenge in the Middle East. Proceedings of the National Academy of Sciences, 109, 3862−3867.
Kardos, M., Luikart, G., Bunch, R., Dewey, S., Edwards, W., McWilliam, S., Stephenson, J., Allendorf, F. W., Hogg, J. T., Kijas, J. (2015). Whole-genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep. Molecular Ecology, 24(22):5616-32.https://doi.org/10.1111/mec.13415.
Kawęcka, A., Pasternak, M., Miksza-Cybulska, A., Puchała, M. (2022). Native sheep breeds in poland—importance and outcomes of genetic resources protection programmes. Animals, 12(12), 1510;https://doi.org/10.3390/ani12121510
Lawson, D. J., Hellenthal, G., Myers, S., Falush, D. (2012). Inference of population structure using dense haplotype data. Plos Genetics, 8, e1002453.https://doi.org/10.1371/journal.pgen.1002453
Li, H., Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 15, 1754–60.https://doi.org/10.1093/bioinformatics/btp324
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. (2009a). The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078–2079.https://doi.org/10.1093/bioinformatics/btp352
Li, Q., Lu, Z., Jin, M., Fei, X., Quan, K., Liu, Y., Ma, L., Chu, M., Wang, H., Wei, C. (2020a). Verification and analysis of sheep tail type-associated PDGF-D gene polymorphisms. Animals (Basel), 6, 89.https://doi.org/10.3390/ani10010089
Li, X., Yang, J., Shen, M. et al. (2020b). Whole-genome resequencing of wild and domestic sheep identifies genes associated with morphological and agronomic traits. Nature Communications, 11, 2815https://doi.org/10.1038/s41467-020-16485-1
Li, R., Gong, M., et al. (2023). A sheep pangenome reveals the spectrum of structural variations and their effects on tail phenotypes. Genome Research, 33(3), 463–77.https://doi.org/10.1101/gr.277372.122
Lin, Z. Chen, Q., Shi, L., et al. (2012). Loss-of-function mutations in HOXC13 cause pure hair and nail ectodermal dysplasia. The American Journal of Human Genetics, 2, 91(5):906-11.https://doi.org/10.1016/j.ajhg.2012.08.029
Lv F. H. et al. (2021). Whole-genome resequencing of worldwide wild and domestic sheep elucidates genetic diversity, introgression, and agronomically important loci. Molecular Biology and Evolution. 39(2),msab353.
Man, Y., Hai, L., Run, Z., Ziping, H., Naiqi, N., Lixian, W., Longchao Z. (2022). Association analysis of polymorphism of MYH3 and MYH13 genes with meat quality traits in Beijing Black pigs. China Animal Husbandry and Veterinary Medicine, 49(9), 3428-3437.https://doi.org/10.16431/j.cnki.1671-7236.2022.09.017
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S. (2010). The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297–303.https://doi.org/10.1101/gr.107524.110
Meng, F., Lin, Y., Yang, M., Li, M., Yang, G., Hao, P., Li, L. (2018). JAZF1 Inhibits Adipose Tissue Macrophages and Adipose Tissue Inflammation in Diet-Induced Diabetic Mice. BioMed Research International, 22, 4507659.https://doi.org/10.1155/2018/4507659
Moosanezhad Khabisi, M., Asadi Foozi, M., Lv, F. H., Esmailizadeh A. (2021). Genome-wide DNA arrays profiling unravels the genetic structure of Iranian sheep and pattern of admixture with worldwide coarse-wool sheep breeds. Genomics, 113, 3501-3511.https://doi.org/10.1016/j.ygeno.2021.07.019
Nosrati, M., Asadollahpour Nanaei, H., Javanmard, A., Esmailizadeh, A. (2021a). The pattern of runs of homozygosity and genomic inbreeding in world-wide sheep populations. Genomics. 113(3), 1407-1415.https://doi.org/10.1016/j.ygeno.2021.03.005
Nosrati, M., Asadollahpour Nanaei., H, Esmailizadeh, A. (2021b). Estimation of runs of homozygosity reveals moderate autozygosity in Northern European sheep breeds. Journal of Livestock Science and Technologies, 9(2), 31-40.
Oliveira H. R., McEwan J. C., Jakobsen, J., Blichfeldt, T., Meuwissen, T., Pickering, N., Clarke, S. M., Brito, L. F. (2020). Genetic connectedness between Norwegian white sheep and New Zealand composite sheep populations with similar development history. Frontiers in Genetics, 11. https://doi.org/10.3389/fgene.2020.00371
Onzima, R. B., Upadhyay, M. R., Doekes, H. P., Brito, L. F., Bosse, M., Kanis, E., Groenen, M. A. M., Crooijmans, R. (2018). Genome-wide characterization of selection signatures and runs of homozygosity in Ugandan goat breeds. Frontiers in Genetics, 9, 318. https://doi.org/10.3389/fgene.2018.00318
Osei-Amponsah, R., Chauhan, S. S., Leury, B. J., Cheng, L., Cullen, B., Clarke, I. J., Dunshea, F. R. (2019). Genetic Selection for thermotolerance in Ruminants. Animals (Basel). 11, 948.
Pan, Z. Li, S., Liu, Q., Wang, Z., et al. (2018). Whole-genome sequences of 89 Chinese sheep suggest role of RXFP2 in the development of unique horn phenotype as response to semi-feralization. Gigascience. 7, 1–15.https://doi.org/10.1093/gigascience/giy019
Patterson, N., Price, A. L., Reich, D. (2006). Population structure and eigenanalysis. PLoS Genetics, 2(12), e190.https://doi.org/10.1371/journal.pgen.0020190
Perini, F., Cendron, F., Wu, Z., Sevane, N., Li, Z., Huang, C., Smith, J., Lasagna, E., Cassandro, M., Penasa, M. Genomics of Dwarfism in Italian Local Chicken Breeds. Genes, 14, 633 (2023).https://doi.org/10.3390/genes14030633
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A., Bender, D., Maller, J., Sklar, P., de Bakker, P. I., Daly, M. J., Sham, P. C. (2007). PLINK: a tool set for whole genome association and population-based linkage analyses. The American Journal of Human Genetics, 81, 559–575.https://doi.org/10.1086/519795
Purfield, D. C., McParland, S., Wall, E., Berry, D. P. (2017). The distribution of runs of homozygosity and selection signatures in six commercial meat sheep breeds. PLoS ONE. 12(5), e0176780.https://doi.org/10.1371/journal.pone.0176780
Quinn, G., O’Toole, E., Dennis, C., Batta, K. (2022). BG08: A new variant in HOXC13 associated with a severe phenotype of pure hair and nail ectodermal dysplasia, British Journal of Dermatology, 187(S1), 93.https://doi.org/10.1111/bjd.21324
Ron M, Kliger D, Feldmesser E, Seroussi E, Ezra E, Weller JL. (2001). Multiple quantitative trait locus analysis of bovine chromosome 6 in the Israeli Holstein population by a daughter design. Genetics, 159, 727–35.https://doi.org/10.1093/genetics/159.2.727
Ruiz-Larrañaga, O. Asadollahpour Nanaei, H., et al. (2020). Genetic structure of Iranian indigenous sheep breeds: insights for conservation. Tropical Animal Health and Production, 52, 2283–2290.https://doi.org/10.1007/s11250-020-02252-3
Sander, G. R., Powell B. C. (2004). Structure and expression of the ovine Hoxc-13 gene. Gene, 8;327(1):107-16.https://doi.org/10.1016/j.gene.2003.11.006.
Savolainen, O., Lascoux, M., Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics, 14, 807–820.https://doi.org/10.1038/nrg3522.
Slatkin, M. (2008). Linkage disequilibrium--understanding the evolutionary past and mapping the medical future. Nature Reviews Genetics, 9(6), 477-85.
Song, C., Gu, X., Feng, C., Wang, Y., Gao, Y., Hu, X., Li, N. (2011). Evaluation of SNPs in the chicken HMGA2 gene as markers for body weight gain. Animal Genetics, 42, 333–336.https://doi.org/10.1111/j.1365-2052.2010.02141.x
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 1, 30(9),1312-1313.https://doi.org/10.1093/bioinformatics/btu033
Taye, M. Lee, W., Caetano-Anolles, K., et al. (2017). Whole genome detection of signature of positive selection in African cattle reveals selection for thermotolerance. Animal Science Journal, 88, 1889-1901.
Terhorst, J., Kamm, J. A., Song, Y. S. (2017). Robust and scalable inference of population history from hundreds of unphased whole genomes. Nature Genetics, 49(2), 303-309.https://doi.org/10.1038/ng.3748
Thornton, P., Nelson, G., Mayberry, D., Herrero, M. (2021). Increases in extreme heat stress in domesticated livestock species during the twenty-first century. Global Change Biology, 27, 5762– 5772.https://doi.org/10.1111/gcb.15825
Tyne T. (2012). The sheep book for smallholder. Preston, 320 p.
Vahidi, S. M. F. et al. (2016). Multilocus genotypic data reveal high genetic diversity and low population genetic structure of Iranian indigenous sheep. Animal Genetics, 47(4), 463-470.
Wang, S., Luo, Z., Zhang, Y. et al. (2018). The inconsistent regulation of HOXC13 on different keratins and the regulation mechanism on HOXC13 in cashmere goat (Capra hircus). BMC Genomics, 19, 630.https://doi.org/10.1186/s12864-018-5011-4
Weedon, M. N., Lettre, G., et al. (2007). A common variant of HMGA2 is associated with adult and childhood height in the general population. Nature Genetics, 39(10):1245-50.https://doi.org/10.1038/ng2121
Weir, B. S., Cockerham, C. C. (1984). Estimating F-Statistics for the analysis of population structure. Evolution. 38(6), 1358–1370.
Wiedemar, N., Drögemüller, C. (2015). A 1.8-kb insertion in the 3'-UTR of RXFP2 is associated with polledness in sheep. Animal Genetics, 46(4), 457-61.https://doi.org/10.1111/age.12309
Wu, J., Husile, H., Sun, H., Wang, F., Li, Y., Zhao, C., Zhang, W. (2013). Adaptive evolution of Hoxc13 genes in the origin and diversification of the vertebrate integument. Journal of Experimental Zoology Part B, 320, 412-9.https://doi.org/10.1002/jez.b.22504
Xu, S. S., Gao, L., Shen, M., Lyu, F. (2021). Whole-genome selective scans detect genes associated with important phenotypic traits in sheep (Ovis aries). Frontiers in Genetics, 18, 738879.https://doi.org/10.3389/fgene.2021.738879
Zapata, I., Serpell, J. A., Alvarez, C. E. (2016). Genetic mapping of canine fear and aggression. BMC Genomics, 17, 572.https://doi.org/10.1186/s12864-016-2936-3
Zeder, M. A. (2017a). Domestication as a model system for the extended evolutionary synthesis. Interface Focus. 7, 20160133
Zeder, M. A. (2017b). In Human Dispersal and Species Movement: from Prehistory to the Present (eds Petraglia, M.D., Crassard, R. & Boivin, N.) p. 261 (Cambridge Univ. Press, 2017).
Zhang, X., Alexander, L., Hegerl, G. C., et al. (2011). Indices for monitoring changes in extremes based on daily temperature and precipitation data. WIREs Climate Change, 2: 851-870.https://doi.org/10.1002/wcc.147
Zhang, C., Dong, S. S., Xu, J. Y., He, W. M., Yang, T. L. (2019). PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics, 35(10), 1786–1788.https://doi.org/10.1093/bioinformatics/bty875
Zhang, C. L., Liu, C., Zhang, J., Zheng, L., Chang, Q., Cui, Z., Liu, S. (2022). Analysis on the desert adaptability of indigenous sheep in the southern edge of Taklimakan Desert. Scientific Reports, 18,12(1):12264
Acknowledgements
This study was performed as postdoctoral research at Shahid Bahonar University of Kerman, Kerman, Iran. H.A.N. was supported jointly by Shahid Bahonar University of Kerman and Iran National Science Foundation (INSF; Grant number: 4006174).
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This study was carried out with financial support from the Iran National Science Foundation (INSF; Grant number: 4006174) and Shahid Bahonar University of Kerman, Kerman, Iran.
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M.A.F. and H.A. N. conceived the project and designed the research. H.A.N. analyzed the data and drafted the manuscript. H.A.N, Z.A.G., M.A.F., revised the manuscript. All authors approved the final manuscript.
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Asadollahpour Nanaei, H., Amiri Ghanatsaman, Z., Farahvashi, M.A. et al. High-throughput DNA sequence analysis elucidates novel insight into the genetic basis of adaptation in local sheep. Trop Anim Health Prod 56, 150 (2024). https://doi.org/10.1007/s11250-024-04002-1
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DOI: https://doi.org/10.1007/s11250-024-04002-1