Genome-wide analysis identifies 12 loci influencing human reproductive behavior

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Abstract

The genetic architecture of human reproductive behavior – age at first birth (AFB) and number of children ever born (NEB) – has a strong relationship with fitness, human development, infertility and risk of neuropsychiatric disorders. However, very few genetic loci have been identified and the underlying mechanisms of AFB and NEB are poorly understood. We report the largest genome-wide association study to date of both sexes including 251,151 individuals for AFB and 343,072 for NEB. We identified 12 independent loci that are significantly associated with AFB and/or NEB in a SNP-based genome-wide association study, and four additional loci in a gene-based effort. These loci harbor genes that are likely to play a role – either directly or by affecting non-local gene expression – in human reproduction and infertility, thereby increasing our understanding of these complex traits.

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Most cited references 53

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Why do people postpone parenthood? Reasons and social policy incentives.

Melinda Mills, Ronald Rindfuss, Peter McDonald … (2011)

Never before have parents in most Western societies had their first children as late as in recent decades. What are the central reasons for postponement? What is known about the link between the delay of childbearing and social policy incentives to counter these trends? This review engages in a systematic analysis of existing evidence to extract the maximum amount of knowledge about the reasons for birth postponement and the effectiveness of social policy incentives. The review followed the PRISMA procedure, with literature searches conducted in relevant demographic, social science and medical science databases (SocINDEX, Econlit, PopLine, Medline) and located via other sources. The search focused on subjects related to childbearing behaviour, postponement and family policies. National, international and individual-level data sources were also used to present summary statistics. There is clear empirical evidence of the postponement of the first child. Central reasons are the rise of effective contraception, increases in women's education and labour market participation, value changes, gender equity, partnership changes, housing conditions, economic uncertainty and the absence of supportive family policies. Evidence shows that some social policies can be effective in countering postponement. The postponement of first births has implications on the ability of women to conceive and parents to produce additional offspring. Massive postponement is attributed to the clash between the optimal biological period for women to have children with obtaining additional education and building a career. A growing body of literature shows that female employment and childrearing can be combined when the reduction in work-family conflict is facilitated by policy intervention.

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Parent-of-origin specific allelic associations among 106 genomic loci for age at menarche

John RB Perry, Felix Day, Cathy E Elks … (2014)

Age at menarche is a marker of timing of puberty in females. It varies widely between individuals, is a heritable trait and is associated with risks for obesity, type 2 diabetes, cardiovascular disease, breast cancer and all-cause mortality 1 . Studies of rare human disorders of puberty and animal models point to a complex hypothalamic-pituitary-hormonal regulation 2,3 , but the mechanisms that determine pubertal timing and underlie its links to disease risk remain unclear. Here, using genome-wide and custom-genotyping arrays in up to 182,416 women of European descent from 57 studies, we found robust evidence (P<5×10−8) for 123 signals at 106 genomic loci associated with age at menarche. Many loci were associated with other pubertal traits in both sexes, and there was substantial overlap with genes implicated in body mass index and various diseases, including rare disorders of puberty. Menarche signals were enriched in imprinted regions, with three loci (DLK1/WDR25, MKRN3/MAGEL2 and KCNK9) demonstrating parent-of-origin specific associations concordant with known parental expression patterns. Pathway analyses implicated nuclear hormone receptors, particularly retinoic acid and gamma-aminobutyric acid-B2 receptor signaling, among novel mechanisms that regulate pubertal timing in humans. Our findings suggest a genetic architecture involving at least hundreds of common variants in the coordinated timing of the pubertal transition.

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VEGAS2: Software for More Flexible Gene-Based Testing.

Aniket Mishra, Stuart MacGregor (2015)

Gene-based tests such as versatile gene-based association study (VEGAS) are commonly used following per-single nucleotide polymorphism (SNP) GWAS (genome-wide association studies) analysis. Two limitations of VEGAS were that the HapMap2 reference set was used to model the correlation between SNPs and only autosomal genes were considered. HapMap2 has now been superseded by the 1,000 Genomes reference set, and whereas early GWASs frequently ignored the X chromosome, it is now commonly included. Here we have developed VEGAS2, an extension that uses 1,000 Genomes data to model SNP correlations across the autosomes and chromosome X. VEGAS2 allows greater flexibility when defining gene boundaries. VEGAS2 offers both a user-friendly, web-based front end and a command line Linux version. The online version of VEGAS2 can be accessed through https://vegas2.qimrberghofer.edu.au/. The command line version can be downloaded from https://vegas2.qimrberghofer.edu.au/zVEGAS2offline.tgz. The command line version is developed in Perl, R and shell scripting languages; source code is available for further development.

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Author and article information

Journal

Journal ID (nlm-journal-id): 9216904

Journal ID (pubmed-jr-id): 2419

Journal ID (nlm-ta): Nat Genet

Journal ID (iso-abbrev): Nat. Genet.

Title: Nature genetics

ISSN (Print): 1061-4036

ISSN (Electronic): 1546-1718

Publication date Nihms-submitted: 23 June 2017

Publication date (Electronic): 31 October 2016

Publication date (Print): December 2016

Publication date PMC-release: 20 November 2017

Volume: 48

Issue: 12

Pages: 1462-1472

Affiliations

[1 ]University of Oxford, Department of Sociology and Nuffield College, United Kingdom

[2 ]Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands

[3 ]Department of Applied Economics, Erasmus School of Economics, Rotterdam, The Netherlands

[4 ]Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands

[5 ]Erasmus University Rotterdam Institute for Behavior and Biology, Rotterdam, The Netherlands

[6 ]Department of Epidemiology, University of Groningen, University Medical Center Groningen, The Netherlands

[7 ]Sociology of Consumption and Households, Wageningen University Research, Wageningen, the Netherlands

[8 ]Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

[9 ]MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh, United Kingdom

[10 ]entre for Global Health Research, Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, Teviot Place, Edinburgh, United Kingdom

[11 ]Brigham and Women's Hospital, Boston MA and Harvard Medical School, Boston MA

[12 ]Department of Cardiology, Division of Heart and Lungs, University Medical Center Utrecht, Utrecht, The Netherlands

[13 ]Laboratory of Experimental Cardiology, Division of Heart and Lungs, University Medical Center Utrecht, Utrecht, The Netherlands

[14 ]MRC Epidemiology Unit, Institute of Metabolic Science, University of Cambridge, Cambridge, UK

[15 ]School of Engineering and Natural Sciences, University of Iceland, Reykjavik 101, Iceland

[16 ]Novo Nordisk Foundation Centre for Basic Metabolic Research, Section of Metabolic Genetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

[17 ]Steno Diabetes Center, Denmark

[18 ]COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark

[19 ]Institute of Genetic Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health, Neuherberg, Germany

[20 ]University of Maryland School of Medicine, Division of Endocrinology, Diabetes and Nutrition

[21 ]Department of Medicine and Genetic, Institute for Aging Research and the Diabetes Research Center, Albert Einstein College of Medicine, Bronx, NY, USA

[22 ]Department of Natural Science, University of Haifa, Haifa, Israel

[23 ]Department of Health, National Institute for Health and Welfare, Helsinki, Finland

[24 ]University of Helsinki, Institute for Molecular Medicine (FIMM), Helsinki, Finland

[25 ]Institute of Genetic Medicine, Newcastle University

[26 ]Queensland Brain Institute, The University of Queensland, Brisbane, Australia

[27 ]Department of Genetic, Institute for Aging Research and the Diabetes Research Center, Albert Einstein College of Medicine, Bronx, NY, USA

[28 ]Institute of Epidemiology and Social Medicine, University of Münster, Germany

[29 ]Departments of Systems and Computational Biology, Pathology and Neuroscience, Albert Einstein College of Medicine, Bronx, NY, USA

[30 ]Lübeck Interdisciplinary Platform for Genome Analytics, Institutes of Neurogenetics & Integrative and Experimental Genomics, University of Lübeck, Germany

[31 ]Department of Epidemiology, University of Michigan, Ann Arbor, MI, USA

[32 ]deCODE Genetics/Amgen Inc., Reykjavik, Iceland

[33 ]Department of Genetics, Genomics Coordination Center, University of Groningen, University Medical Center Groningen, The Netherlands

[34 ]Department of Internal Medicine, Erasmus Medical Center, The Netherlands

[35 ]Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne

[36 ]Division of Genetics and Cell Biology, San Raffaele Research Institute, Milano, Italy

[37 ]Population, Policy and Practice, UCL Institute of Child Health, London, UK

[38 ]Centre for Environmental and Preventive Medicine, Wolfson Institute of Preventative Medicine, Queen Mary University of London; London, UK

[39 ]Department of Nutrition, Harvard T.H. Chan School of Public Health

[40 ]Department of Medicine, Brigham and Women's Hospital and Harvard Medical School

[41 ]Department of Epidemiology, Harvard T.H. Chan School of Public Health

[42 ]Institute of Genetic and Biomedic Research, National Research Council, Cagliari, Italy

[43 ]Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK

[44 ]Department of Psychology, University of Edinburgh, Edinburgh, UK

[45 ]German Socio- Economic Panel Study (SOEP) & Health Economics Research Centre, University of Oxford

[46 ]23andMe, Inc

[47 ]Estonian Genome Center, University of Tartu, Tartu, Estonia

[48 ]Broad Institute of the Massachusetts Institute of Technology and Harvard University, Cambridge, USA

[49 ]Centre for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

[50 ]The Generation R Study Group, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands

[51 ]Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands

[52 ]Center for Economic and Social Research, University of Southern California, Los Angeles, California, USA

[53 ]Department of Medical, Surgical and Health Sciences, University of Trieste, 34100 Trieste, Italy

[54 ]Research Unit of Molecular Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health, Neuherberg, Germany

[55 ]Institute of Epidemiology II, Helmholtz Zentrum München—German Research Center for Environmental Health, Neuherberg, Germany

[56 ]Cardiovascular and Metabolic Conditions Section, Division of Research, Kaiser Permanente Northern California, Oakland, USA

[57 ]Institute for Translational Genomics and Population Sciences, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA

[58 ]Department of Epidemiology, Indiana University Richard M. Fairbanks School of Public Health

[59 ]Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria

[60 ]Institute of Medical Informatics, Statistics and Documentation, Medical University of Graz, Austria

[61 ]William Harvey Research Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, UK

[62 ]Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria

[63 ]Centre for Vision Research, Department of Ophthalmology and The Westmead Institute for Medical Research, NSW Australia

[64 ]Institute of Medical Epidemiology, Biostatistics and Informatics, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany

[65 ]Department of Biostatistics, Harvard T.H. Chan School of Public Health

[66 ]Department of Neurosciences, KU Leuven, Leuven 3000, Belgium

[67 ]Department of Microbiology and Immunology, KU Leuven, Leuven 3000, Belgium

[68 ]Translational Immunology Laboratory, VIB, Leuven 3000, Belgium

[69 ]Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland

[70 ]Helsinki Collegium for Advanced Studies, University of Helsinki, Helsinki, Finland

[71 ]Folkhälsan Research Centre, Helsinki, Finland

[72 ]Department of Clinical Epidemiology, Leiden University Medical Center, Leiden, the Netherlands

[73 ]Psychiatric Genetics, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston Brisbane 4006, Australia

[74 ]Center for Lifespan Psychology, Max Planck Institute for Human Development, Germany & Dept of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, Germany

[75 ]Minnesota Center for Twin and Family Research, Department of Psychology, University of Minnesota, Minneapolis, USA

[76 ]Department of Biological Psychology, VU University Amsterdam, Amsterdam, The Netherlands

[77 ]EMGO+ Institute for Health and Care Research, Amsterdam, The Netherlands

[78 ]School of Social and Community Medicine University of Bristol, Bristol, UK

[79 ]Complex Trait Genetics, VU University, Amsterdam, The Netherlands

[80 ]Department of Psychology, University of Minnesota, Minneapolis, USA

[81 ]Department of Obstetrics, Gynecology and Reproductive Biology, Brigham and Women's Hospital and Harvard Medical School

[82 ]Laboratory of Neurogenetics, National Institute on Aging, NIH, Bethesda, Maryland

[83 ]Institute of Genetics and Biophysics "A. Buzzati-Traverso", CNR, Naples - Italy

[84 ]Department of Nutrition and Dietetics, School of Health Science and Education, Harokopio University, Athens, Greece

[85 ]Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche,c/o Cittadella Universitaria di Monserrato, Monserrato, Cagliari, Italy

[86 ]Dipartimento di Scienze Biomediche, Università di Sassari, Sassari, Italy

[87 ]Department of Genomics of Common Disease, School of Public Health, Imperial College London, London, UK

[88 ]Wellcome Trust Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford, UK

[89 ]Oxford Centre for Diabetes, Endocrinology, and Metabolism, Radcliffe Department of Medicine, University of Oxford, Oxford, UK

[90 ]Rush University Medical Center, Chicago, USA

[91 ]Connors Center for Women's Health and Gender Biology. Brigham and Women's Hospital and Harvard Medical School

[92 ]Institute for Maternal and Child Health-IRCCS “Burlo Garofolo” – Trieste, Italy

[93 ]Department of Medical Genetics, University of Lausanne, Lausanne, Switzerland

[94 ]Swiss Institute of Bioinformatics, Lausanne, Switzerland

[95 ]Department of Medicine, University of Leipzig, Leipzig, Germany

[96 ]Department of Public Health, University of Helsinki, Helsinki, Finland

[97 ]King’s British Heart Foundation Centre, King’s College London, UK

[98 ]Department of Public Health and Primary Care, University of Cambridge, UK

[99 ]University of Lille, CNRS, Institut Pasteur of Lille, UMR 8199 - EGID, F-59000 Lille, France

[100 ]Centre for Neurogenetics and Statistical Genomics, University of Queensland, Australia

[101 ]MRC Epidemiology Unit, Institute of Metabolic Science, University of Cambridge, Cambridge, UK

[102 ]The Data Coordinating Center, New York State Psychiatric Institute

[103 ]Institute of Molecular Genetics, National Research Council of Italy, Pavia

[104 ]Integrative Epidemiology Unit, University of Bristol, Bristol, UK

[105 ]Princess Al-Jawhara Al-Brahim Centre of Excellence in Research of Hereditary Disorders (PACER-HD), King Abdulaziz University, Jeddah, Saudi Arabia

[106 ]National Institute for Health and Welfare, Department of Chronic Disease Prevention, Helsinki, Finland

[107 ]Department of General Practice and Primary Health Care, University of Helsinki, Finland

[108 ]Unit of General Practice, Helsinki University Central Hospital, Finland

[109 ]Vasa Central Hospital, Vasa, Finland

[110 ]Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, MI

[111 ]Medical Genetics, IRCCS-Burlo Garofolo and University of Trieste, Trieste, Italy

[112 ]Department of Experimental Genetics, Sidra, Doha, Qatar

[113 ]Department of Psychiatry, University Medicine Greifswald, Greifswald, Germany

[114 ]German Cancer Research Center, Division of Cancer Epidemiology, Heidelberg, Germany

[115 ]Econometric Institute, Erasmus School of Economics, Erasmus University Rotterdam, Rotterdam, The Netherlands

[116 ]Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Bethesda, Maryland

[117 ]Genetic Epidemiology, QIMR Berghofer Medical Research Institute, Brisbane, Australia

[118 ]Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA

[119 ]Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald, Germany

[120 ]School of Medicine and Public Health, University of Newcastle, Newcastle, Australia

[121 ]Hunter Medical Research Institute, Newcastle, Australia

[122 ]Centre for Population Health Research, Sansom Institute of Health Research and School of Health Sciences, University of South Australia, Adelaide,Australia

[123 ]South Australian Health and Medical Research Institute, Adelaide, Australia

[124 ]Department of Obstetrics and Gynecology, Institute of Public Health, Sahlgrenska Academy, Sahgrenska University Hospital, Gothenburg, Sweden

[125 ]Department of Genetics and Bioinformatics, Area of Health Data and Digitalisation, Institute of Public Health, Oslo, Norway

[126 ]Department of Economics, Stockholm School of Economics,Box Stockholm, Sweden

[127 ]Department of Clinical Physiology, University of Tampere and Tampere University Hospital, Tampere, Finland

[128 ]National Institute for Health and Welfare, Diabetes Prevention Unit, Helsinki, Finland

[129 ]Children's Hospital, Helsinki University Central Hospital and University of Helsinki,Helsinki, Finland

[130 ]Department of Obstetrics and Gynecology, MRC Oulu, Oulu University Hospital and University of Oulu, Oulu, Finland

[131 ]Institute of Cardiovascular Sciences, University of Manchester

[132 ]Department of Public Health, Faculty of Medicine, University of Split, Croatia

[133 ]National Institute for Health and Welfare, Health Monitoring Unit, Helsinki, Finland

[134 ]IFB Adiposity Diseases, University of Leipzig, Leipzig, Germany

[135 ]Division of Genetic Epidemiology, Medical university of Innsbruck, Innsbruck, Austria

[136 ]Institute of Social and Preventive Medicine, Lausanne University Hospital (CHUV), Lausanne, Switzerland

[137 ]Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom

[138 ]Department of Clinical Chemistry, Fimlab Laboratories, and School of Medicine, University of Tampere, Tampere, Finland

[139 ]LifeLines Cohort Study, Groningen, The Netherlands

[140 ]The National Institute for Health Research Oxford Biomedical Research Centre (F.K.)

[141 ]The Li Ka Shing Centre for Health Information and Discovery, the Big Data Institute (C.M.L.), University of Oxford, Oxford, United Kingdom

[142 ]Division of Public Health Sciences, Wake Forest School of Medicine, Winston-Salem, North Carolina

[143 ]Strangeways Research Laboratory, University of Cambridge, Worts Causeway, Cambridge, UK

[144 ]UKK Institute for Health Promotion, Finland

[145 ]The Danish Aging Research Center, and The Danish twin Registry, Institute of Public Health, University of Southern Denmark, Odense, Denmark

[146 ]MONICA/KORA Myocardial Infarction Registry, Central Hospital of Augsburg, Augsburg, Germany

[147 ]Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia

[148 ]Molecular Bioscience, University of Queensland, Brisbane, Australia

[149 ]Department of Public Health and Primary Care, Leiden University Medical Center, Leiden, the Netherlands

[150 ]Department of BESC, Epidemiology Section, King Faisal Specialist Hospital and Research Centre, Riyadh, Saudi Arabia

[151 ]Research Unit for Gynaecology and Obstetrics, Deparrtment of Clinical Research, University of Southern Denmark

[152 ]Department of Clinical Epidemiology, Aarhus University, Aarhus, Denmark

[153 ]Department of Psychiatry & EMGO Institute for Health and Care Research VU University Medical Center, Amsterdam, The Netherlands

[154 ]National Institute for Health and Welfare, Dept of Health, Helsinki, Finland

[155 ]Medical Genetics Institute; Cedars-Sinai Medical Center, Los Angeles, CA

[156 ]Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku and the Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland

[157 ]Department of Psychiatry, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany

[158 ]Laboratory of Genetics, National Institute on Aging, Baltimore, Maryland, USA

[159 ]Institute of Molecular Biology and Biochemistry, Centre for Molecular Medicine, Medical University of Graz, Austria

[160 ]Departments of Epidemiology and Psychiatry, Columbia University Medical Center NY, USA

[161 ]Alzheimer Scotland Dementia Research Centre, University of Edinburgh, Edinburgh, UK

[162 ]Institute of Medical Informatics, Biometry and Epidemiology, Ludwig Maximilians Universität, Munich, Germany

[163 ]Medical Department, University of Leipzig, Leipzig, Germany

[164 ]Faculty of Medicine, University of Iceland, Reykjavik, Iceland

[165 ]Montpellier Business School, Montpellier, France

[166 ]Department of Medicine, University of Turku, and Division of Medicine, Turku University Hospital, Turku, Finland

[167 ]Institute for Community Medicine, University Medicine Greifswald, Germany

[168 ]Department of Internal Medicine, Internal Medicine, Lausanne University Hospital (CHUV), Lausanne, Switzerland

[169 ]Genetic and Genomic Epidemiology Unit, Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK

[170 ]Department of Psicology, University of Minnesota, USA

[171 ]Center for Economic and Social Research, University of Southern California, Los Angeles, CA, USA

[172 ]National Bureau of Economic Research, Cambridge, MA, USA

[173 ]Department of Economics, New York University, New York, USA

[174 ]Research Institute for Industrial Economics, Stockholm, Sweden

[175 ]Department of Medical Sciences, Molecular Epidemiology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden

Author notes

Correspondence to: Melinda C. Mills ( melinda.mills@ 123456nuffield.ox.ac.uk ), Nicola Barban ( nicola.barban@ 123456sociology.ox.ac.uk ), Harold Snieder ( h.snieder@ 123456umcg.nl ) or Marcel den Hoed ( marcel.den_hoed@ 123456medsci.uu.se )

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These authors contributed equally to this work

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Accession ID: PMC5695684 Pmcid ID: PMC5695684 Pmc-uid ID: 5695684 Manuscript ID: nihpa841435

DOI: 10.1038/ng.3698

PMC ID: 5695684

PubMed ID: 27798627

SO-VID: c685dfdc-9142-4ef1-afa1-ce8cdef8f50e

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Genome-wide analysis identifies 12 loci influencing human reproductive behavior

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Most cited references 53

Why do people postpone parenthood? Reasons and social policy incentives.

Parent-of-origin specific allelic associations among 106 genomic loci for age at menarche

VEGAS2: Software for More Flexible Gene-Based Testing.

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