A genome-wide scan to detect signatures of recent selection in Australian Merino sheep

Document Type : Original Research Article (Regular Paper)

Authors

1 Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, 76169-133, Iran.

2 Young Researchers Society, Shahid Bahonar University of Kerman, Kerman, Iran.

3 Honorary Associate, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

4 State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.

5 Animal Genetic and Breeding Unit, University of New England, Armidale, NSW 2351, Australia.

6 School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

7 Cooperative Research Centre for Sheep Industry Innovation, Armidale, NSW 2351, Australia.

Abstract

Domestication and selection are processes that conserve the pattern of genetic diversities between and within populations. Identification of genomic regions that are targets of selection for phenotypic traits is one of the main aims of research in animal genetics. An approach for identifying divergently selected regions of the genome is to compare FST values among loci to estimate the genetic variability between and within populations. In this study, a whole genome scan using the 50K Illumina Ovine SNP chip was performed in seventeen flocks of Australian Merino sheep (8 CRC flocks and 9 SG flocks). Population differentiation using FST in these flocks revealed seven genomic regions. These areas were located on chromosomes 2 (two region), 3, 6, 7, 16 and 26 (Wintheta> 0.15). In this study, a number of candidate genes associated with reproductive and growth traits were identified. Study of the reported QTLs in these regions of the ovine and bovine genomes also showed that they associated with important traits such as reproduction, carcass yield, growth and wool traits. Further validation studies of these regions can be used to identify the candidate genes for economically important traits in sheep breeds. The results also provided intuitions for further understanding of the genetic diversities among the Merino flocks.

Keywords

Main Subjects


  • Abdi, H., 2007. Bonferroni and Sidak corrections for multiple comparisons. Encyclopedia of Measurement and Statistics 24, 103-107.
  • Akey, J.M., 2009. Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Research 19, 711-722.
  • Akey, J.M., Zhang, G., Zhang, K., Jin, L., Shriver, M.D., 2002. Interrogating a high-density SNP map for signatures of natural selection. Genome Research 12, 1805-1814.
  • Amaral, A.J., Ferretti, L., Megens, H.J., Crooijmans, R.P.M.A., Nie, H., Ramos-Onsins, S.E., Perez-Enciso, M., Schook, L.B., Groenen, M.A.M., 2011. Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PLoS One 6, 14782.
  • Arranz, J.J., Gutiérrez-Gil, B., 2012. Detection of QTL Underlying Milk Traits in Sheep: An Update. 6th Ed. University of Leon, Spain.
  • Asadi Fozi, M., Van der Werf, J.H.J., Swan, A.A., 2005. The importance of accounting for maternal genetic effects in Australian fine-wool Merino breeding. Australian Journal of Agricultural Research 56, 789-796.
  • Ashwell, M.S., Heyen, D.W., Weller, J.I., Ron, M., Sonstegard, T.S., Van Tassell, C.P., Lewin, H.A., 2005. Detection of quantitative trait loci influencing conformation traits and calving ease in Holstein-Friesian cattle. Journal of Dairy Science 88, 4111-4119.
  • Bai, J.Z., Mon, Y., Krissansen, G.W., 2006. Kinectin participates in microtubule-dependent hormone secretion in pancreatic islet beta-cells. Cell Biology International 30, 885-894.
  • Brickell, J.S., Bourne, N., Cheng, Z., Wathes, D.C., 2007. Influence of plasma IGF-1 concentrations and body weight at 6 months on age at first calving in dairy heifers on commercial farms. Reproduction in Domestic Animals 2, 118-129.
  • Cavanagh, C.R., Jonas, E., Hobbs, M., Thomson, P.C., Tammen, I., Raadsma, H.W., 2010. Mapping Quantitative Trait Loci (QTL) in sheep. III. QTL for carcass composition traits derived from CT scans and aligned with a meta-assembly for sheep and cattle carcass QTL. Genetics Selection Evolution 42, 1-14.
  • Chen, H.Y., Zhang, Q., Yin, C.C., Wang, C.K., Gong, W.J., Mei. G., 2006. Detection of quantitative trait loci affecting milk production traits on bovine chromosome 6 in a Chinese Holstein population by the daughter design. Journal of Dairy Science 89, 782-790.
  • Chessa, B., Pereira, F., Arnaud, F., Amorim, A., Goyache, F., Mainland, I., Kao, R.R., Pemberton, J.M., Beraldi, D., Stear, M.J., 2009. Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532-536.
  • DeChiara, T.M., Efstratia, A., Robertson, E.J., 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345, 78-80.
  • Diamond, J., 2002. Evolution, consequences and future of plant and animal domestication. Nature 418, 700-707.
  • Dodds, K.G., McEwan, J.C., 1997. Calculating exact probabilities of allele frequency differences in divergent selection lines. Proceedings of the 12th Conference of the Association for the Advancement of Animal Breeding and Genetics. University of New England, Armidale, New South Wales.
  • Duncan, E.J., Dodds, K.G., Henry, H.M., Thompson, M.P., Phua, S.H., 2007. Cloning, mapping and association studies of the ovine ABCG2 gene with facial eczema disease in sheep. Animal Genetics 38, 126-131.
  • Echternkamp, S.E., Roberts, J., Lunstra, D.D., Wise, T., Spicer, L.J., 2004. Ovarian follicular development in cattle selected for twin ovulations and births. Journal of Animal Science 82, 459-471.
  • Esmailizadeh, A.K., 2015. Detection of chromosomal segments underlying scrotal circumference in ram lambs and age at onset of puberty in ewe lambs. Animal Production Science 55, 1018-1024.
  • Fisher, R.A., 1925. Statistical Methods for Research Worker. Biological Monographs and Manuals. 12th Ed. Gonville and Caius College, Cambridge, Britain.
  • Gibbs, R.A., Taylor, J.F., Van Tassell, C.P., Barendse, W., Eversole, K.A., Gill, C.A., Green, R.D., Hamernik, D.L., Kappes, S.M., Lien, S., 2009. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324, 528-532.
  • Gu, X., Feng, C., Ma, L., Song, C., Wang, Y., Da, Y., 2011. Genome-wide association study of body weight in chicken F2 resource population. PLoS One 6, 1-10.
  • Hancock, A.M., Anna, D.R., 2008. Detecting the genetic signature of natural selection in human populations: Models, Methods, and Data. Annual Review of Anthropology 37, 197-217.
  • Hawlader, A., Al-Mamun, P.K., Clark, S., Ferdosi, M.H., Tellamand, R., Gondro, C., 2015. Genome-wide association study of body weight in Australian Merino sheep reveals an orthologous region on OAR6 to human and bovine genomic regions affecting height and weight. Genetic Selection Evolution 14, 47-66.
  • Hayes, B.J., Chamberlain, A.J., MacEachern, S., Savin, K., McPartlan, H., MacLeod, I., Sethuraman, L., Goddard, M.E., 2009. A genome map of divergent artificial selection between Bos taurus dairy cattle and Bos taurus beef cattle. Animal Genetics 40, 176-184.
  • Hibar, D.P., Stein, J.L., Renteria, M.E., Arias-Vasquez, A., Desrivières, S., Jahanshad, N., Toro, R., Wittfeld, K., Abramovic, L., Andersson, M., Aribisala, B.S., Armstrong, N.J., 2015. Common genetic variants influence human subcortical brain structures. Nature 520, 224-229.
  • Hiendleder, S., Thomsen, H., Reinsch, N., Bennewitz, J., Leythe-Horn, B., Looft, C., Xu, N., Medjugorac, I., Russ, I., Kuhn, C., Bro, G.A., 2003. Mapping of QTL for Body Conformation and Behavior in Cattle. Journal of Heredity 94, 496-506.
  • Hubbard, T.J.P.,  Aken, B.L.,  Ayling, S.,  Ballester, B.,  Beal, K.,  Bragin, E.,  Brent, S.,  Chen, Y.,  Clapham, P.,  Clarke, L.,  Coates, G.,  Fairley, S.,  Fitzgerald, S.,  Fernandez-Banet, J.,  Gordon, L.,  Graf, S.,  Haider, S.,  Hammond, M.,  Holland, R.,  Howe, K.,  Jenkinson, A.,  Johnson, N.,  Kahari, A.,  Keefe, D.,  Keenan, S.,  Kinsella, R.,  Kokocinski, F.,  Kulesha, E.,  Lawson, D.,  Longden, I.,  Megy, K., Meidl, P., Overduin, B., Parker, A., Pritchard, B., Rios, D., 2009. Ensemble BioMart: Ensemble online genome data base BioMart Tool. Nucleic Acids Research 37, 690-697.
  • Jin, C.F., Chen, Y.J., Yang, Z.Q., Shi, K., Chen, C.K., 2015. A genome-wide association study of growth trait-related single nucleotide polymorphisms in Chinese Yancheng chickens. Genetic Molecular Research 14, 15783-15792.
  • Lee, T., Cho, S., Seok, K., Chang, J., Kim, H., Yoon, D., 2013. Genetic variants and signatures of selective sweep of Hanwoo population (Korean native cattle). BMB Reports 46, 346-351.
  • Karamichou, E., Richardson, R.I., Nute, G.R., Gibson, K.P., Bishop, S.C., 2006. Genetic analyses and quantitative trait loci detection, using a partial genome scan, for intramuscular fatty acid composition in Scottish Blackface sheep. Journal of Animal Science 84, 3228-3238.
  • Kathryn, M., John, C., Neil, J., 2014. Signatures of selection in sheep bred for resistance or susceptibility to gastrointestinal nematodes. BMC Genomics 15, 1-13.
  • Kijas, J.W., Townley, D., Dalrymple, B.P., Heaton, M.P., Maddox, J.F., McGrath, A., Wilson, P., Ingersoll, R.G., McCulloch, R., McWilliam, S., 2009. A genome wide survey of SNP variation reveals the genetic structure of sheep breeds. PloS One 4, 46-68.
  • Kijas, J.W., Lenstra, J.A., Hayes, B., Boitard, S., Porto Neto, L.R., Cristobal, M.S., Servin, B., McCulloch, R., Whan, V., Gietzen, K., Paiva, S., Barendse, W., Ciani, E., Raadsma, H., McEwan, J., Kim, Y., 2006. Allele frequency distribution under recurrent selective sweeps. Genetics 172, 1967-1978.
  • MacEachern, S., Hayes, B., McEwan, J., Goddard, M., 2009. An examination of positive selection and changing effective population size in Angus and Holstein cattle populations (Bos taurus) using a high density SNP genotyping platform and the contribution of ancient polymorphism to genomic diversity in Domestic cattle. BMC Genomics 10, 1-19.
  • Maltecca, C., Weigel, K.A., Khatib, H., Cowan, M., Bagnato, A., 2008. Whole-genome scan for quantitative trait loci associated with birth weight, gestation length and passive immune transfer in a Holstein x Jersey crossbred population. Animal Genetics 40, 27-34.
  • Marshall, K., Mugambi, J.M., Nagda, S., Sonstegard, T.S., Tassell, C.P., Baker, R.L., Gibson, J.P., 2013. Quantitative trait loci for resistance to Haemonchus contortus artificial challenge in red Maasai and Dorper sheep of East Africa. Animal Genetics 44, 285-295.
  • McClure, M.C., Morsci, N.S., Schnabel, R.D., Kim, J.W., Yao, P., Rolf, M.M., McKay, S.D., Gregg, S.J., Chapple, R.H., Northcutt, S.L., Taylor, J.F., 2010. A genome scan for quantitative trait loci influencing carcass, post-natal growth and reproductive traits in commercial Angus cattle. Animal Genetics 41, 597-607.
  • Mohammadabadi, M.R., Sattayimokhtari, R., 2013 Estimation of (co) variance components of ewe productivity traits in Kermani sheep. Slovak Journal of Animal Science 46, 45-51.
  • Mohammadabadi, M.R., Torabi, A., Tahmourespoor, M., Baghizadeh, A., Esmailizadeh Koshkoie, A., Mohammadi, A., 2010a. Analysis of bovine growth hormone gene polymorphism of local and Holstein cattle breeds in Kerman province of Iran using polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP). African Journal of Biotechnology 9, 6848-6852.
  • Mohammadabadi, M.R., Nikbakhti, M., Mirzaee, H.R., Shandi, M.A., Saghi, D.A., Romanov, M.N., Moiseyeva, I.G., 2010b. Genetic variability in three native Iranian chicken populations of the Khorasan province based on microsatellite markers. Russian Journal of Genetics 46, 572-576.
  • Moradi, M.H., Nejati-Javaremi, A., Moradi-Shahrbabak, M., Dodds, K.G., McEwan, J.C., 2012. Genomic scan of selective sweeps in thin and fat tail sheep breeds for identifying of candidate regions associated with fat deposition. BMC Genetics 13, 1-15.
  • Nielsen, R., 2005. Molecular signature of natural selection. Annual Review of Genetics 39, 197-218.
  • Notter, D.R., 2008. Genetic aspects of reproduction in sheep. Reproduction in Domestic Animals  43, 122-128.
  • Patton, J., Kenny, D.A., McNamara, S., Mee, J.F., O’Mara, F.P., Diskin, M.G., Murphy, J.J., 2007. Relationships among milk production, energy balance, plasma analysts, and reproduction in Holstein-Friesian cows. Journal of Dairy Science 90, 649-658.
  • Ponz, R., Moreno, C., Allain, D., Elsen, J.M., Lantier, F., Lantier, I., Brunel, J.C., Perez-Enciso, M., 2001. Assessement of genetic variation explained by markers for wool traits in sheep via a segment mapping approach. Mammalian Genome 12, 569-572.
  • Pollot, G.E., Greeff, J.C., 2004. Genotype x environment interactions and genetic parameters for fecal egg count and production traits of Merino sheep. Journal of Animal Science 82, 2840-2851.
  • Porto-Neto, L.R., Lee, S.H., Lee, H.K., Gondro, C., 2013. Detection of signatures of selection using FST. Methods Molecular Biology 1019, 423-436.
  • Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics 81, 559-575.
  • Qanbari, S., Pimentel, E.C.G., Tetens, J., Thaller, G., Lichtner, P., Sharifi, A.R., Simianer, H., 2010. A genome-wide scan for signatures of recent selection in Holstein cattle. Animal Genetics 41, 377-389.
  • Qanbari, S., Gianola, D., Hayes, B., Schenkel, F., Miller, S., Moore, S., Thaller, G., Simianer, H., 2011. Application of site and haplotype frequency based approaches for detecting selection signatures in cattle. BMC Genomics 12, 1-12.
  • R Development Core Team, 2011. R: A language and environment for statistical computing. Vienna, Austria: the R foundation for statistical computing. Available at: https://www.R-project.org [Verified 22 January 2015].
  • R Development Core Team, 2014b. Analyses of phylogenetics and evolution. Available at: http://ape-package.ird.fr. [Verified 18 December 2015].
  • Rubin, C.J., Megens, H.J., Barrio, A.M., Maqboolc, K., Sayyabc, S., Schwochowc, D., Wanga, C., Carlborgd, Ö., Jerna, P., Jørgensen, C.B., 2012. Strong signatures of selection in the domestic pig genome. Proceedings of the National Academy of Sciences 109, 19529-19536.
  • Sabeti, P.C., Reich, D.E., Higgins, J.M., Levine, H.Z.P., Richter, D.J., Schaffer, S.F., 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832-837.
  • Safari, E., Fogarty, N.M., Gilmour, A.R., Atkins, K.D., Mortimer, S.I., Swan, A.A., Brien, F.D., Greeff, J.C., van der Werf, J.H.J., 2007. Genetic correlations among and between wool, growth and reproduction traits in Merino sheep. Journal of Animal Breeding and Genetics 124, 65-72.
  • Sorbolini, S., Marras, G., Gaspa, G., Dimauro, C., Cellesi, M., Valentini, A., Macciotta, N., 2015. Detection of selection signatures in Piemontese and Marchigiana cattle, two breeds with similar production aptitudes but different selection histories. Genetics Selection Evolution 47, 1-13.
  • Soufy, B., Mohammadabadi, M.R., Shojaeyan, K., Baghizadeh, A., Ferasaty, S., Askari, N., Dayani, O., 2009. Evaluation of Myostatin gene polymorphism in Sanjabi sheep by PCR-RFLP method. Research Journal of Animal Sciences 19, 81-89. In Farsi.
  • Tyner, C., Barber, G.P., Casper, J., Clawson, H., Diekhans, M., Eisenhart, C., Fischer, C.M., Gibson, D., Gonzalez, J.N., Guruvadoo, L., Haeussler, M., Heitner, S., Hinrichs, A.S., Karolchik, D., Lee, B.T., Lee, C.M., Nejad, P., Raney, B.J., Rosenbloom, K.R., Speir, M.L., Villarreal, C., Vivian, J., Zweig, A.S., Haussler, D., Kuhn, R.M., Kent, W.J., 2016. The UCSC Genome Browser database. Available at: http://genome.ucsc.edu [Verified 29 November 2017].
  • Tran, H., Pankov, R., Tran, S.D., Hampton, B., Burgess, W.H., Yamada, K.M., 2002. Integrin clustering induces Kinectin accumulation. Journal of Cell Science 115, 2031-2040.
  • Walling, G.A., Visscher, P.M., Wilson, A.D., McTeir, B.L., Simm, G., Bishop, S.C., 2004. Mapping of quantitative trait loci for growth and carcass traits in commercial sheep populations. Journal of Animal Science 82, 2234-2245.
  • Weir, B.S., Cardon, L.R., Anderson, A.D., Nielsen, D.M., Hill, W.G., 2005. Measures of human population structure show heterogeneity among genomic regions. Genome Research 15, 1468-1476.
  • Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
  • Wright, S., 1992. Coefficient of inbreeding and relationship. American Naturalist 56, 330-338.
  • Wright, S., 1951. The genetical structure of populations. Annals of Human Genetics 15, 323-354.
  • Vajed Ebrahimi, M.T., Mohammadabadi, M.R., Esmailizadeh, A.K., 2017. Using microsatellite markers to analyze genetic diversity in 14 sheep types in Iran. Archiv Tierzucht (Archive Animal Breeding) 60, 183-189.
  • Velazquez, M.A., Newman, M., Christie, M.F., Cripps, P.J., Crowe, M.A., Smith R.F., Dobson, H., 2005. The usefulness of a single measurement of insulin-like growth factor-1 as a predictor of embryo yield and pregnancy rates in a bovine MOET program. Theriogenology 64, 1977-1994.
  • Yang, S., Xiuling, L., Kui, L., Bin, F., Zhonglin, T., 2014. A genome-wide scan for signatures of selection in Chinese indigenous and commercial pig breeds. BMC Genetics 15, 1-9.
  • Zamani, P., Akhondi, M., Mohammadabadi, M.R., 2015. Associations of inter-simple sequence repeat loci with predicted breeding values of body weight in sheep. Small Ruminant Research 132, 123-127.
  • Zhiliang, H., Fritz, E.R., Reecy, J.M., 2007. Animal QTLdb: a livestock QTL database tool set for positional QTL information mining and beyond. Nucleic Acids Research 35, 604-609.