Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche
John R. B. Perry (),
Felix Day,
Cathy E. Elks,
Patrick Sulem,
Deborah J. Thompson,
Teresa Ferreira,
Chunyan He,
Daniel I. Chasman,
Tõnu Esko,
Gudmar Thorleifsson,
Eva Albrecht,
Wei Q. Ang,
Tanguy Corre,
Diana L. Cousminer,
Bjarke Feenstra,
Nora Franceschini,
Andrea Ganna,
Andrew D. Johnson,
Sanela Kjellqvist,
Kathryn L. Lunetta,
George McMahon,
Ilja M. Nolte,
Lavinia Paternoster,
Eleonora Porcu,
Albert V. Smith,
Lisette Stolk,
Alexander Teumer,
Natalia Tšernikova,
Emmi Tikkanen,
Sheila Ulivi,
Erin K. Wagner,
Najaf Amin,
Laura J. Bierut,
Enda M. Byrne,
Jouke-Jan Hottenga,
Daniel L. Koller,
Massimo Mangino,
Tune H. Pers,
Laura M. Yerges-Armstrong,
Jing Hua Zhao,
Irene L. Andrulis,
Hoda Anton-Culver,
Femke Atsma,
Stefania Bandinelli,
Matthias W. Beckmann,
Javier Benitez,
Carl Blomqvist,
Stig E. Bojesen,
Manjeet K. Bolla,
Bernardo Bonanni,
Hiltrud Brauch,
Hermann Brenner,
Julie E. Buring,
Jenny Chang-Claude,
Stephen Chanock,
Jinhui Chen,
Georgia Chenevix-Trench,
J. Margriet Collée,
Fergus J. Couch,
David Couper,
Andrea D. Coviello,
Angela Cox,
Kamila Czene,
Adamo Pio D’adamo,
George Davey Smith,
Immaculata De Vivo,
Ellen W. Demerath,
Joe Dennis,
Peter Devilee,
Aida K. Dieffenbach,
Alison M. Dunning,
Gudny Eiriksdottir,
Johan G. Eriksson,
Peter A. Fasching,
Luigi Ferrucci,
Dieter Flesch-Janys,
Henrik Flyger,
Tatiana Foroud,
Lude Franke,
Melissa E. Garcia,
Montserrat García-Closas,
Frank Geller,
Eco E. J. de Geus,
Graham G. Giles,
Daniel F. Gudbjartsson,
Vilmundur Gudnason,
Pascal Guénel,
Suiqun Guo,
Per Hall,
Ute Hamann,
Robin Haring,
Catharina A. Hartman,
Andrew C. Heath,
Albert Hofman,
Maartje J. Hooning,
John L. Hopper,
Frank B. Hu,
David J. Hunter,
David Karasik,
Douglas P. Kiel,
Julia A. Knight,
Veli-Matti Kosma,
Zoltan Kutalik,
Sandra Lai,
Diether Lambrechts,
Annika Lindblom,
Reedik Mägi,
Patrik K. Magnusson,
Arto Mannermaa,
Nicholas G. Martin,
Gisli Masson,
Patrick F. McArdle,
Wendy L. McArdle,
Mads Melbye,
Kyriaki Michailidou,
Evelin Mihailov,
Lili Milani,
Roger L. Milne,
Heli Nevanlinna,
Patrick Neven,
Ellen A. Nohr,
Albertine J. Oldehinkel,
Ben A. Oostra,
Aarno Palotie,
Munro Peacock,
Nancy L. Pedersen,
Paolo Peterlongo,
Julian Peto,
Paul D. P. Pharoah,
Dirkje S. Postma,
Anneli Pouta,
Katri Pylkäs,
Paolo Radice,
Susan Ring,
Fernando Rivadeneira,
Antonietta Robino,
Lynda M. Rose,
Anja Rudolph,
Veikko Salomaa,
Serena Sanna,
David Schlessinger,
Marjanka K. Schmidt,
Mellissa C. Southey,
Ulla Sovio,
Meir J. Stampfer,
Doris Stöckl,
Anna M. Storniolo,
Nicholas J. Timpson,
Jonathan Tyrer,
Jenny A. Visser,
Peter Vollenweider,
Henry Völzke,
Gerard Waeber,
Melanie Waldenberger,
Henri Wallaschofski,
Qin Wang,
Gonneke Willemsen,
Robert Winqvist,
Bruce H. R. Wolffenbuttel,
Margaret J. Wright,
Dorret I. Boomsma,
Michael J. Econs,
Kay-Tee Khaw,
Ruth J. F. Loos,
Mark I. McCarthy,
Grant W. Montgomery,
John P. Rice,
Elizabeth A. Streeten,
Unnur Thorsteinsdottir,
Cornelia M. van Duijn,
Behrooz Z. Alizadeh,
Sven Bergmann,
Eric Boerwinkle,
Heather A. Boyd,
Laura Crisponi,
Paolo Gasparini,
Christian Gieger,
Tamara B. Harris,
Erik Ingelsson,
Marjo-Riitta Järvelin,
Peter Kraft,
Debbie Lawlor,
Andres Metspalu,
Craig E. Pennell,
Paul M. Ridker,
Harold Snieder,
Thorkild I. A. Sørensen,
Tim D. Spector,
David P. Strachan,
André G. Uitterlinden,
Nicholas J. Wareham,
Elisabeth Widen,
Marek Zygmunt,
Anna Murray,
Douglas F. Easton,
Kari Stefansson,
Joanne M. Murabito () and
Ken K. Ong
Additional contact information
John R. B. Perry: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Felix Day: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Cathy E. Elks: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Patrick Sulem: deCODE Genetics, Reykjavik IS-101, Iceland.
Deborah J. Thompson: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
Teresa Ferreira: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.
Chunyan He: Indiana University Richard M Fairbanks School of Public Health
Daniel I. Chasman: Brigham and Women’s Hospital
Tõnu Esko: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Gudmar Thorleifsson: deCODE Genetics, Reykjavik IS-101, Iceland.
Eva Albrecht: Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, D-85764 Neuherberg, Germany.
Wei Q. Ang: School of Women’s and Infants’ Health, The University of Western Australia, WA-6009, Australia.
Tanguy Corre: University of Lausanne, CH-1005 Lausanne, Switzerland.
Diana L. Cousminer: Institute for Molecular Medicine Finland (FIMM), University of Helsinki, FI-00014, Finland.
Bjarke Feenstra: Statens Serum Institut, DK-2300 Copenhagen, Denmark.
Nora Franceschini: University of North Carolina
Andrea Ganna: Karolinska Institutet, 17177 Stockholm, Sweden.
Andrew D. Johnson: NHLBI’s and Boston University’s Framingham Heart Study
Sanela Kjellqvist: Science for Life Laboratory, Karolinska Institutet, Stockholm, Box 1031, 17121 Solna, Sweden.
Kathryn L. Lunetta: NHLBI’s and Boston University’s Framingham Heart Study
George McMahon: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Ilja M. Nolte: University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands.
Lavinia Paternoster: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Eleonora Porcu: Institute of Genetics and Biomedical Research, National Research Council, Cagliari, 09042 Sardinia, Italy.
Albert V. Smith: Icelandic Heart Association, IS-201 Kopavogur, Iceland.
Lisette Stolk: Erasmus MC, 3015 GE Rotterdam, the Netherlands.
Alexander Teumer: Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald, D-17475 Greifswald, Germany.
Natalia Tšernikova: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Emmi Tikkanen: Institute for Molecular Medicine Finland (FIMM), University of Helsinki, FI-00014, Finland.
Sheila Ulivi: Institute for Maternal and Child Health - IRCCS “Burlo Garofolo”, 34137 Trieste, Italy.
Erin K. Wagner: Indiana University Richard M Fairbanks School of Public Health
Najaf Amin: Erasmus MC, 3015 GE, Rotterdam, the Netherlands.
Laura J. Bierut: Washington University
Enda M. Byrne: The University of Queensland, Queensland Brain Institute, St Lucia, Queensland 4072, Australia.
Jouke-Jan Hottenga: VU University Amsterdam, van der Boechorststraat 1, 1081 BT, Amsterdam, The Netherlands.
Daniel L. Koller: Indiana University School of Medicine
Massimo Mangino: King’s College London, London SE1 7EH, UK.
Tune H. Pers: Boston Children’s Hospital
Laura M. Yerges-Armstrong: Program in Personalized and Genomic Medicine, Diabetes and Nutrition, University of Maryland School of Medicine
Jing Hua Zhao: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Irene L. Andrulis: Ontario Cancer Genetics Network, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario M5G 1X5, Canada.
Hoda Anton-Culver: University of California Irvine
Femke Atsma: Sanquin Research, 6525 GA Nijmegen, The Netherlands.
Stefania Bandinelli: Tuscany Regional Health Agency, Florence, Italy, University of Florence, 50134 Florence, Italy.
Matthias W. Beckmann: University Breast Center Franconia, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, D-91054 Erlangen, Germany.
Javier Benitez: Human Genetics Group, Human Cancer Genetics Program, Spanish National Cancer Research Centre (CNIO), E-28029 Madrid, Spain.
Carl Blomqvist: University of Helsinki and Helsinki University Central Hospital, FI-00100 Helsinki, Finland.
Stig E. Bojesen: Copenhagen General Population Study, Herlev Hospital, Copenhagen University Hospital, University of Copenhagen, DK-2100 Copenhagen, Denmark.
Manjeet K. Bolla: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
Bernardo Bonanni: Istituto Europeo di Oncologia (IEO), 20139 Milan, Italy.
Hiltrud Brauch: DrMargarete Fischer-Bosch-Institute of Clinical Pharmacology, D-70376 Stuttgart, Germany.
Hermann Brenner: German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany.
Julie E. Buring: Brigham and Women’s Hospital
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Stephen Chanock: National Cancer Institute
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Georgia Chenevix-Trench: QIMR Berghofer Medical Research Institute
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Fergus J. Couch: Mayo Clinic
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Andrea D. Coviello: Boston University School of Medicine, Sections of Preventive Medicine and Endocrinology
Angela Cox: Sheffield Cancer Research Centre, University of Sheffield, Sheffield S10 2RX, UK.
Kamila Czene: Karolinska Institutet, 17177 Stockholm, Sweden.
Adamo Pio D’adamo: Institute for Maternal and Child Health - IRCCS “Burlo Garofolo”, 34137 Trieste, Italy.
George Davey Smith: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Immaculata De Vivo: Harvard School of Public Health
Ellen W. Demerath: School of Public Health, University of Minnesota
Joe Dennis: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
Peter Devilee: Leiden University Medical Center, 2300 RC Leiden, The Netherlands.
Aida K. Dieffenbach: German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany.
Alison M. Dunning: Centre for Cancer Genetic Epidemiology, University of Cambridge CB1 8RN, UK.
Gudny Eiriksdottir: Icelandic Heart Association, IS-201 Kopavogur, Iceland.
Johan G. Eriksson: National Institute for Health and Welfare, P.O. Box 30, FI-00271 Helsinki, Finland.
Peter A. Fasching: University Breast Center Franconia, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, D-91054 Erlangen, Germany.
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Melissa E. Garcia: National Insitute on Aging, National Institutes of Health
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Frank Geller: Statens Serum Institut, DK-2300 Copenhagen, Denmark.
Eco E. J. de Geus: VU University Amsterdam, van der Boechorststraat 1, 1081 BT, Amsterdam, The Netherlands.
Graham G. Giles: Cancer Epidemiology Centre, Cancer Council Victoria
Daniel F. Gudbjartsson: deCODE Genetics, Reykjavik IS-101, Iceland.
Vilmundur Gudnason: Icelandic Heart Association, IS-201 Kopavogur, Iceland.
Pascal Guénel: Inserm (National Institute of Health and Medical Research), CESP (Center for Research in Epidemiology and Population Health), U1018, Environmental Epidemiology of Cancer, F-94807 Villejuif, France.
Suiqun Guo: Southern Medical University
Per Hall: Karolinska Institutet, 17177 Stockholm, Sweden.
Ute Hamann: Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum (DKFZ), D-69120 Heidelberg, Germany.
Robin Haring: Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, D-17475 Greifswald, Germany.
Catharina A. Hartman: University of Groningen, University Medical Center Groningen, P.O. Box 72, 9700 AB Groningen, The Netherlands.
Andrew C. Heath: Washington University
Albert Hofman: Erasmus MC, PO Box 2040, 3000 CA Rotterdam, the Netherlands.
Maartje J. Hooning: Erasmus University Medical Center, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands.
John L. Hopper: Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne
Frank B. Hu: Harvard School of Public Health
David J. Hunter: Broad Institute of the Massachusetts Institute of Technology and Harvard University
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Douglas P. Kiel: Hebrew SeniorLife Institute for Aging Research
Julia A. Knight: Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario M5G 1X5, Canada.
Veli-Matti Kosma: School of Medicine, Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland.
Zoltan Kutalik: University of Lausanne, CH-1005 Lausanne, Switzerland.
Sandra Lai: Institute of Genetics and Biomedical Research, National Research Council, Cagliari, 09042 Sardinia, Italy.
Diether Lambrechts: Vesalius Research Center (VRC), VIB, 3000 Leuven, Belgium.
Annika Lindblom: Karolinska Institutet, SE-171 77 Stockholm, Sweden.
Reedik Mägi: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Patrik K. Magnusson: Karolinska Institutet, 17177 Stockholm, Sweden.
Arto Mannermaa: School of Medicine, Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland.
Nicholas G. Martin: QIMR Berghofer Medical Research Institute
Gisli Masson: deCODE Genetics, Reykjavik IS-101, Iceland.
Patrick F. McArdle: Program in Personalized and Genomic Medicine, Diabetes and Nutrition, University of Maryland School of Medicine
Wendy L. McArdle: School of Social and Community Medicine, University of Bristol, Oakfield House, Oakfield Grove, Bristol BS8 2BN, UK.
Mads Melbye: Statens Serum Institut, DK-2300 Copenhagen, Denmark.
Kyriaki Michailidou: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
Evelin Mihailov: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Lili Milani: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Roger L. Milne: Cancer Epidemiology Centre, Cancer Council Victoria
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Patrick Neven: KULeuven (University of Leuven), Multidisciplinary Breast Center, University Hospitals Leuven, 3000 Leuven, Belgium.
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Paolo Radice: Unit of Molecular Bases of Genetic Risk and Genetic Testing, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), 20133 Milan, Italy.
Susan Ring: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Fernando Rivadeneira: Erasmus MC, 3015 GE Rotterdam, the Netherlands.
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Mellissa C. Southey: The University of Melbourne
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Meir J. Stampfer: Harvard School of Public Health
Doris Stöckl: Institute of Epidemiology II, Helmholtz Zentrum München - German Research Center for Environmental Health, D-8576 Neuherberg, Germany.
Anna M. Storniolo: Indiana University School of Medicine
Nicholas J. Timpson: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Jonathan Tyrer: Centre for Cancer Genetic Epidemiology, University of Cambridge CB1 8RN, UK.
Jenny A. Visser: Erasmus MC, 3015 GE Rotterdam, the Netherlands.
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Melanie Waldenberger: Research Unit of Molecular Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, D-8576 Neuherberg, Germany.
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Qin Wang: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
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Michael J. Econs: Indiana University School of Medicine
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Ruth J. F. Loos: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Mark I. McCarthy: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.
Grant W. Montgomery: Queensland Insitute of Medical Research
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Elizabeth A. Streeten: Program in Personalized and Genomic Medicine, Diabetes and Nutrition, University of Maryland School of Medicine
Unnur Thorsteinsdottir: deCODE Genetics, Reykjavik IS-101, Iceland.
Cornelia M. van Duijn: Netherlands Consortium on Health Aging and National Genomics Initiative, 2300 RC Leiden, the Netherlands.
Behrooz Z. Alizadeh: University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands.
Sven Bergmann: University of Lausanne, CH-1005 Lausanne, Switzerland.
Eric Boerwinkle: Human Genetics Center and Divof Epidemiology, University of Houston, P.O. Box 20186, Texas 77025 USA.
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Laura Crisponi: Institute of Genetics and Biomedical Research, National Research Council, Cagliari, 09042 Sardinia, Italy.
Paolo Gasparini: Institute for Maternal and Child Health - IRCCS “Burlo Garofolo”, 34137 Trieste, Italy.
Christian Gieger: Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, D-85764 Neuherberg, Germany.
Tamara B. Harris: National Insitute on Aging, National Institutes of Health
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Marjo-Riitta Järvelin: MRC Health Protection Agency (HPA) Centre for Environment and Health, School of Public Health, Imperial College London, London W2 1PG, UK.
Peter Kraft: Harvard School of Public Health
Debbie Lawlor: MRC Integrative Epidemiology Unit, University of Bristol, Bristol BS8 2BN, UK.
Andres Metspalu: Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia.
Craig E. Pennell: School of Women’s and Infants’ Health, The University of Western Australia, WA-6009, Australia.
Paul M. Ridker: Brigham and Women’s Hospital
Harold Snieder: University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands.
Thorkild I. A. Sørensen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200, Denmark.
Tim D. Spector: King’s College London, London SE1 7EH, UK.
David P. Strachan: St George’s, University of London, Cranmer Terrace, London SW17 0RE, UK.
André G. Uitterlinden: Erasmus MC, 3015 GE Rotterdam, the Netherlands.
Nicholas J. Wareham: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Elisabeth Widen: Institute for Molecular Medicine Finland (FIMM), University of Helsinki, FI-00014, Finland.
Marek Zygmunt: University Medicine Greifswald, D-17475 Greifswald, Germany.
Anna Murray: University of Exeter Medical School, University of Exeter, Exeter EX1 2LU, UK.
Douglas F. Easton: Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge CB1 8RN, UK.
Kari Stefansson: deCODE Genetics, Reykjavik IS-101, Iceland.
Joanne M. Murabito: NHLBI’s and Boston University’s Framingham Heart Study
Ken K. Ong: MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Box 285 Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
Nature, 2014, vol. 514, issue 7520, 92-97
Abstract:
Here 106 genomic loci associated with age at menarche, a marker of puberty timing in females, are identified; these loci show enrichment for genes involved in nuclear hormone receptor function, body mass index, and rare disorders of puberty, and for genes located in imprinted regions, with parent-of-origin specific effects at several loci.
Date: 2014
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DOI: 10.1038/nature13545
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