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Genome-Wide Analysis Reveals Selection for Important Traits In Genome-wide analysis reveals selection for important traits in domestic horse breeds Jessica L Petersen, James R Mickelson, Aaron K Rendahl, Stephanie J Valberg, Lisa S Andersson, Jeanette Axelsson, Ernie Bailey, Danika Bannasch, Matthew M Binns, Alexandre S Borges, et al. To cite this version: Jessica L Petersen, James R Mickelson, Aaron K Rendahl, Stephanie J Valberg, Lisa S Andersson, et al.. Genome-wide analysis reveals selection for important traits in domestic horse breeds. PLoS Genetics, Public Library of Science, 2013, 9, online (1), Non paginé. 10.1371/journal.pgen.1003211. hal-01000690 HAL Id: hal-01000690 https://hal.archives-ouvertes.fr/hal-01000690 Submitted on 29 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Genome-Wide Analysis Reveals Selection for Important Traits in Domestic Horse Breeds Jessica L. Petersen1*, James R. Mickelson1, Aaron K. Rendahl2, Stephanie J. Valberg1, Lisa S. Andersson3, Jeanette Axelsson3, Ernie Bailey4, Danika Bannasch5, Matthew M. Binns6, Alexandre S. Borges7, Pieter Brama8, Artur da Caˆmara Machado9, Stefano Capomaccio10, Katia Cappelli10, E. Gus Cothran11, Ottmar Distl12, Laura Fox-Clipsham13, Kathryn T. Graves4,Ge´rard Gue´rin14, Bianca Haase15, Telhisa Hasegawa16, Karin Hemmann17, Emmeline W. Hill18, Tosso Leeb19, Gabriella Lindgren3, Hannes Lohi17, Maria Susana Lopes9, Beatrice A. McGivney18, Sofia Mikko3, Nicholas Orr20,M. Cecilia T. Penedo5, Richard J. Piercy21, Marja Raekallio17, Stefan Rieder22, Knut H. Røed23, June Swinburne13,24, Teruaki Tozaki25, Mark Vaudin13, Claire M. Wade15, Molly E. McCue1 1 College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota, United States of America, 2 School of Statistics, University of Minnesota, Minneapolis, Minnesota, United States of America, 3 Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden, 4 Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America, 5 School of Veterinary Medicine, University of California Davis, Davis, California, United States of America, 6 Equine Analysis, Midway, Kentucky, United States of America, 7 Department of Veterinary Clinical Science, University Estadual Paulista, Botucatu, Brazil, 8 School of Veterinary Medicine, University College Dublin, Dublin, Ireland, 9 Department of Agriculture, University of the Azores, Angra do Heroı´smo, Portugal, 10 Faculty of Veterinary Medicine, University of Perugia, Perugia, Italy, 11 College of Veterinary Medicine and Biomedical Science, Texas A&M University, College Station, Texas, United States of America, 12 Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover, Hannover, Germany, 13 Animal Health Trust, Lanwades Park, Newmarket, Suffolk, United Kingdom, 14 Animal Genetics and Integrative Biology Unit, French National Institute for Agricultural Research, Jouy en Josas, France, 15 Faculty of Veterinary Science, University of Sydney, New South Wales, Australia, 16 Nihon Bioresource College, Koga, Ibaraki, Japan, 17 Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland, 18 College of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Dublin, Ireland, 19 Institute of Genetics, University of Bern, Bern, Switzerland, 20 Breakthrough Breast Cancer Research Centre, Institute of Cancer Research, London, United Kingdom, 21 Comparative Neuromuscular Diseases Laboratory, Royal Veterinary College, London, United Kingdom, 22 Swiss National Stud Farm SNSTF, Agroscope Liebefeld- Posieux Research Station, Avenches, Switzerland, 23 Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, Oslo, Norway, 24 Animal DNA Diagnostics, Cambridge, United Kingdom, 25 Department of Molecular Genetics, Laboratory of Racing Chemistry, Utsunomiya, Tochigi, Japan Abstract Intense selective pressures applied over short evolutionary time have resulted in homogeneity within, but substantial variation among, horse breeds. Utilizing this population structure, 744 individuals from 33 breeds, and a 54,000 SNP genotyping array, breed-specific targets of selection were identified using an FST-based statistic calculated in 500-kb windows across the genome. A 5.5-Mb region of ECA18, in which the myostatin (MSTN) gene was centered, contained the highest signature of selection in both the Paint and Quarter Horse. Gene sequencing and histological analysis of gluteal muscle biopsies showed a promoter variant and intronic SNP of MSTN were each significantly associated with higher Type 2B and lower Type 1 muscle fiber proportions in the Quarter Horse, demonstrating a functional consequence of selection at this locus. Signatures of selection on ECA23 in all gaited breeds in the sample led to the identification of a shared, 186-kb haplotype including two doublesex related mab transcription factor genes (DMRT2 and 3). The recent identification of a DMRT3 mutation within this haplotype, which appears necessary for the ability to perform alternative gaits, provides further evidence for selection at this locus. Finally, putative loci for the determination of size were identified in the draft breeds and the Miniature horse on ECA11, as well as when signatures of selection surrounding candidate genes at other loci were examined. This work provides further evidence of the importance of MSTN in racing breeds, provides strong evidence for selection upon gait and size, and illustrates the potential for population-based techniques to find genomic regions driving important phenotypes in the modern horse. Citation: Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS, et al. (2013) Genome-Wide Analysis Reveals Selection for Important Traits in Domestic Horse Breeds. PLoS Genet 9(1): e1003211. doi:10.1371/journal.pgen.1003211 Editor: Joshua M. Akey, University of Washington, United States of America Received August 28, 2012; Accepted November 15, 2012; Published January 17, 2013 Copyright: ß 2013 Petersen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by National Research Initiative Competitive Grants 2008-35205-18766, 2009-55205-05254, and 2012-67015-19432 from the USDA-NIFA; Foundation for the Advancement of the Tennessee Walking Show Horse and Tennessee Walking Horse Foundation; NIH-NAIMS grant 1K08AR055713- 01A2 (MEM salary support) and 2T32AR007612 (JLP salary support); American Quarter Horse Foundation grant ‘‘Selective Breeding Practices in the American Quarter Horse: Impact on Health and Disease 2011-2012’’; Morris Animal Foundation Grant D07EQ-500; The Swedish Research Council FORMAS (Contract 221- 2009-1631 and 2008-617); The Swedish-Norwegian Foundation for Equine Research (Contract H0847211 and H0947256); The Carl Tryggers Stiftelse (Contract CTS 08:29); support to IBB-CBA-UAc¸ (University of the Azores) by FCT and DRCT, and to MSL by FRCT/2011/317/005; Science Foundation Ireland Award (04/Y11/B539) to EWH; Volkswagen Stiftung und Niedersa¨chsisches Ministerium fu¨r Wissenschaft und Kultur, Germany (VWZN2012). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. PLOS Genetics | www.plosgenetics.org 1 January 2013 | Volume 9 | Issue 1 | e1003211 Signatures of Selection in the Horse Competing Interests: Equinome Ltd. (EWH, Director) has been granted a license for commercial use of MSTN data as contained within patent applications: U.S. Provisional Serial Number 61/136553; Irish Patent Application Numbers 2008/0735 and 2010/0151; and Patent Cooperation Treaty number PCT/IE2009/000062. The PCT publication WO2010/029527A published 18 March 2010. Title: ‘‘A method for predicting athletics performance potential’’ and U.S. publication US2011/0262915 published 27 October 2011. Title: ‘‘Method for predicting the athletic performance potential of a subject.’’ EWH, NO, and BAM are named on the applications. MMB works for The Genetic Edge, previously published a paper on the association between SNPs in the MSTN region and best racing distance for elite Thoroughbred horses [46], and uses these markers in commercial tests. LSA and GL are co-applicants on a patent application concerning the commercial utilization of the DMRT3 mutation. These commercial ventures had no influence on the interpretation of the results relating to myostatin or gait presented in the paper. * E-mail: [email protected] Introduction Results Since domestication of the horse approximately 5,000 years ago Overview [1–3], selective breeding has been directed mainly toward the use A total of 744 horses representing 33 breeds (average 22.5 of the horse in agriculture, transportation, and warfare. Within the horses/breed) genotyped with the Equine SNP50 Beadchip past 400 years, the founding of formal breed registries and (Illumina)
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