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Uncovering the genetic architecture of broad antisocial behavior through a genome-wide association study meta-analysis

Molecular Psychiatry volume 27, pages 4453–4463 (2022)Cite this article

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Abstract

Despite the substantial heritability of antisocial behavior (ASB), specific genetic variants robustly associated with the trait have not been identified. The present study by the Broad Antisocial Behavior Consortium (BroadABC) meta-analyzed data from 28 discovery samples (N = 85,359) and five independent replication samples (N = 8058) with genotypic data and broad measures of ASB. We identified the first significant genetic associations with broad ASB, involving common intronic variants in the forkhead box protein P2 (FOXP2) gene (lead SNP rs12536335, p = 6.32 × 10−10). Furthermore, we observed intronic variation in Foxp2 and one of its targets (Cntnap2) distinguishing a mouse model of pathological aggression (BALB/cJ strain) from controls (BALB/cByJ strain). Polygenic risk score (PRS) analyses in independent samples revealed that the genetic risk for ASB was associated with several antisocial outcomes across the lifespan, including diagnosis of conduct disorder, official criminal convictions, and trajectories of antisocial development. We found substantial genetic correlations of ASB with mental health (depression rg = 0.63, insomnia rg = 0.47), physical health (overweight rg = 0.19, waist-to-hip ratio rg = 0.32), smoking (rg = 0.54), cognitive ability (intelligence rg = −0.40), educational attainment (years of schooling rg = −0.46) and reproductive traits (age at first birth rg = −0.58, father’s age at death rg = −0.54). Our findings provide a starting point toward identifying critical biosocial risk mechanisms for the development of ASB.

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Fig. 1: SNP-based results from the GWAS meta-analysis (N = 85,359) on broad antisocial behavior.
Fig. 2: Bar charts illustrating the proportion of variance (incremental R2, or ΔR2) explained by the PRSs.
Fig. 3: Significant genetic correlations of ASB with previously published results of other traits and diseases, computed using cross-trait LD score regression in LDHub, Bonferroni-corrected p value: 0.00068 (bars represent 95% confidence intervals).

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Acknowledgements

GM-V was supported by a Doctoral Research Scholarship from the FRQSC. MB, IO-M, and J-PG are supported by the Canada Research Chair Program. KR is supported by a Sir Henry Wellcome Postdoctoral Fellowship. ADB and DD were supported by grants from the Lundbeck Foundation (R102-A9118, R155-2014-1724 and R248-2017-2003), the EU FP7 Program (Grant No. 602805, “Aggressotype”) and H2020 Program (Grant No. 667302, “CoCA”), NIMH (1U01MH109514-01. JL, AM, and KR acknowledge the following funders: Academy of Finland, the Signe and Ane Gyllenberg foundation, Juho Vainio foundation, Yrjö Jahnsson foundation, Jalmari and Rauha Ahokas foundation, Sigrid Juselius Foundation and The Finnish Society of Sciences and Letters. DD is supported by NIH R01 AA015416 (Finnish Twin Study), P50 AA022537 (Alcohol Research Center), R25 AA027402 (VCU GREAT), R34 AA027347 (Personalized Risk Assessment), R01 AA028064 (Parental Marital Discord, PI: JS), and U10 AA008401 (COGA) from the National Institute on Alcohol Abuse and Alcoholism (NIAAA), and by R01 DA050721 (Externalizing Consortium) from the National Institute on Drug Abuse (NIDA). BF, MK, and NRM were also supported by funding from the European Community’s Horizon 2020 Programme (H2020/2014–2020) under grant agreements no. 728018 (Eat2beNICE) and no. 847879 (PRIME). They also received relevant funding from the Netherlands Organization for Scientific Research (NWO) for the Dutch National Science Agenda NeurolabNL project (grant 400-17-602). HMS and MRM are members of the Medical Research Council (MRC) Integrative Epidemiology Unit at the University of Bristol (MC_UU_00011/7). This work is also supported by the NIHR Biomedical Research Centre at University Hospitals Bristol NHS Foundation Trust and the University of Bristol. AW has been supported by funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 602768 for the ACTION consortium. JK has been supported by the Academy of Finland Academy professorship program (grants 265240 and 263278). LC-C was supported by a QIMR Berghofer Research Fellowship. JJM was supported by a QIMR Berghofer International PhD Scholarship. ML was funded by an NHMRC Boosting Dementia Leadership Fellowship (APP1140441). SEM and NGM were funded by NHMRC investigator grants (APP1172917 and APP1172990). PJ has been supported by Academy of Finland (Grants no. 319403, 284385 and 274521) and the Stiftelsen för Åbo Akademi Foundation. MK was supported by a personal Rubicon grant (no. 45219212) from the Dutch Research Council. Additional acknowledgements for each study cohort are described in Supplementary Table 1. We acknowledge the work of all members of the Spit for Science Working Group. Spit for Science Director: Danielle M. Dick. Registry management: Kimberly Pedersen, Zoe Neale, Nathaniel Thomas. Data cleaning and management: Amy E. Adkins, Nathaniel Thomas, Zoe Neale, Kimberly Pedersen, Thomas Bannard and Seung B. Cho. Data collection: Amy E. Adkins, Peter Barr, Holly Byers, Erin C. Berenz, Erin Caraway, Seung B. Cho, James S. Clifford, Megan Cooke, Elizabeth Do, Alexis C. Edwards, Neeru Goyal, Laura M. Hack, Lisa J. Halberstadt, Sage Hawn, Sally Kuo, Emily Lasko, Jennifer Lend, Mackenzie Lind, Elizabeth Long, Alexandra Martelli, Jacquelyn L. Meyers, Kerry Mitchell, Ashlee Moore, Arden Moscati, Aashir Nasim, Zoe Neale, Jill Opalesky, Cassie Overstreet, A. Christian Pais, Kimberly Pedersen, Tarah Raldiris, Jessica Salvatore, Jeanne Savage, Rebecca Smith, David Sosnowski, Jinni Su, Nathaniel Thomas, Chloe Walker, Marcie Walsh, Teresa Willoughby, Madison Woodroof and Jia Yan. Genotypical data processing and cleaning: Cuie Sun, Brandon Wormley, Brien Riley, Fazil Aliev, Roseann Peterson and Bradley T. Webb.

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Authors and Affiliations

  1. Center for Neurogenomics and Cognitive Research, Department of Complex Trait Genetics, Vrije Universiteit Amsterdam, De Boelelaan 1105, 1081 HV, Amsterdam, The Netherlands

    Jorim J. Tielbeek, Emil Uffelmann, Philip R. Jansen, Jeanne E. Savage & Danielle Posthuma

  2. Department of Psychology and Neuroscience, Trinity College of Arts and Sciences, Duke University, 2020 West Main Street, Durham, NC, 27705, USA

    Benjamin S. Williams, Karen Sugden, Terrie E. Moffitt & Avshalom Caspi

  3. Psychiatric Genetics, Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, Brisbane, QLD, 4006, Australia

    Lucía Colodro-Conde, Jose J. Morosoli & Sarah E. Medland

  4. Research Unit on Children’s Psychosocial Maladjustment, École de psychologie, Université Laval, 2523 Allée des Bibliothèques, Quebec City, QC, G1V 0A6, Canada

    Éloi Gagnon, Ginette Dionne, Geneviève Morneau-Vaillancourt & Michel Boivin

  5. Psychiatric and Neurodevelopmental Genetics Unit, Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA

    Travis T. Mallard

  6. Carolina Population Center, University of North Carolina at Chapel Hill, 123 Franklin St, Chapel Hill, NC, 27516, USA

    Brandt E. Levitt

  7. Department of Psychology, Faculty of Arts, Psychology, and Theology, Åbo Akademi University, Tuomiokirkontori 3, FI-20500, Turku, Finland

    Ada Johansson & Patrick Jern

  8. MRC Integrative Epidemiology Unit, University of Bristol, Oakfield Road, Bristol, BS8 2BN, UK

    Hannah M. Sallis & Marcus R. Munafò

  9. Center for Psychiatric Epidemiology and Psychopathology, Department of Psychiatry, Lausanne University Hospital and University of Lausanne, Route de Cery 25, CH-1008, Prilly, Vaud, Switzerland

    Giorgio Pistis, Enrique Castelao & Martin Preisig

  10. Department of Psychology, University of Minnesota, 75 E. River Road, Minneapolis, MN, 55455, USA

    Gretchen R. B. Saunders, Scott Vrieze, Matt McGue & William G. Iacono

  11. Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, DeCrespigny Park, Denmark Hill, London, SE5 8AF, UK

    Andrea G. Allegrini, Kaili Rimfeld & Robert Plomin

  12. Department of Psychiatry and Psychotherapy, Medical University of Vienna, Waehringer Guertel 18-20, 1090, Vienna, Austria

    Bettina Konte, Annette M. Hartmann, Dan Rujescu & Ina Giegling

  13. Department of Human Genetics, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Geert Groteplein 10, 6500 HB, Nijmegen, The Netherlands

    Marieke Klein & Nina Roth Mota

  14. Department of Psychiatry, Robert Wood Johnson Medical School, Rutgers University, Piscataway, NJ, USA

    Jessica E. Salvatore

  15. Department of Epidemiology, University of Groningen, University Medical Center Groningen, Hanzeplein 1, 9700 RB, Groningen, The Netherlands

    Ilja M. Nolte & Harold Snieder

  16. iPSYCH, The Lundbeck Foundation Initiative for Integrative Psychiatric Research, 8000, Aarhus C, Aarhus, Denmark

    Ditte Demontis & Anders D. Børglum

  17. Department of Psychology and Logopedics, University of Helsinki, Haartmaninkatu 3, 00014, Helsinki, Finland

    Anni L. K. Malmberg, Katri Räikkönen & Jari Lahti

  18. Michigan State University, East Lansing, MI, USA

    S. Alexandra Burt

  19. Dunedin Multidisciplinary Health and Development Research Unit, Department of Psychology, Dunedin, New Zealand

    Richie Poulton

  20. Department of Sociology, University of North Carolina at Chapel Hill, CB# 3210, 201 Hamilton Hall, Chapel Hill, NC, 27599, USA

    Kathleen Mullan Harris

  21. University of Exeter Medical School, University of Exeter, Exeter, UK

    Jonathan Mill

  22. The Institute of Metabolism and Systems Research (IMSR), University of Birmingham, Edgbaston, Birmingham, UK

    Joana F. Viana

  23. Genetic Epidemiology, Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, Brisbane, QLD, 4006, Australia

    Brittany L. Mitchell, Michelle K. Lupton & Nicholas G. Martin

  24. Department of Neurology, Technical University of Munich, 22 Ismaninger St., 81675, Munich, Germany

    Till F. M. Andlauer

  25. Research Unit on Children’s Psychosocial Maladjustment, École de criminologie, Université of Montreal, 3150 Rue Jean-Brillant, Montreal, QC, H3T 1N8, Canada

    Isabelle Ouellet-Morin

  26. Research Unit on Children’s Psychosocial Maladjustment, Département de pédiatrie et de psychologie, University of Montreal, 90 Avenue Vincent d’Indy, Montreal, QC, H2V 2S9, Canada

    Richard E. Tremblay

  27. Research Unit on Children’s Psychosocial Maladjustment, CHU Ste-Justine Research Center and Department of Social and Preventive Medicine, University of Montreal, 3175 Chemin de la Côte Ste-Catherine, Montreal, QC, H3T 1C5, Canada

    Sylvana M. Côté

  28. Department of Psychology, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, H4B 1R6, Canada

    Jean-Philippe Gouin

  29. Research Unit on Children’s Psychosocial Maladjustment, Département de psychologie, Université du Québec à Montréal, CP 8888 succursale Centre-ville, Montreal, QC, H3C 3P8, Canada

    Mara R. Brendgen

  30. Research Unit on Children’s Psychosocial Maladjustment, CHU Sainte-Justine Research Center and University of Montreal, 3175 Chemin de la Côte Ste-Catherine, Montreal, QC, H3T 1C5, Canada

    Frank Vitaro

  31. Department of General Practice and Primary Health Care, University of Helsinki, Tukholmankatu 8 B, Helsinki, Finland

    Johan G. Eriksson

  32. Interdisciplinary Center Psychopathology and Emotion Regulation (ICPE), University of Groningen, University Medical Center Groningen, Hanzeplein 1, 9700 RB, Groningen, The Netherlands

    Catharina A. Hartman & Albertine J. Oldehinkel

  33. School of Criminal Justice, University of Cincinnati, 2840 Bearcat Way, Cincinnati, OH, 45221, USA

    Hexuan Liu & J. C. Barnes

  34. Institute for Molecular Medicine Finland (FIMM), HiLIFE, University of Helsinki, PO Box 4, (Yliopistonkatu 3), 00014, Helsinki, Finland

    Alyce Whipp, Eero Vuoksimaa, Teemu Palviainen & Jaakko Kaprio

  35. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Nobels Väg 12A, 171 77, Stockholm, Sweden

    Yi Lu

  36. Department of Psychology and Population Research Center, University of Texas at Austin, 108 E Dean Keeton Stop #A8000, Austin, TX, 78712, USA

    Kathryn Paige Harden

  37. Division of Psychology and Language Sciences, University College London, London, UK

    Essi Viding

  38. School of Applied Sciences, University of Mississippi, John D. Bower School of Population Health, University of Mississippi Medical Center, 84 Dormitory Row West, University, MS, 38677, USA

    Brian B. Boutwell

  39. Department of Psychology, Virginia Commonwealth University, Box 842018, 806W Franklin St, Richmond, VA, 23284, USA

    Fazil Aliev & Danielle M. Dick

  40. Amsterdam UMC, VKC Psyche, Child and Adolescent Psychiatry & Psychosocial Care, Amsterdam, The Netherlands

    Arne Popma & Tinca J. C. Polderman

  41. Department of Psychiatry, SUNY Upstate Medical University, Syracuse, NY, USA

    Stephen V. Faraone

  42. Department of Human Genetics, Donders Institute for Brain, Cognition and Behaivour, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA, Nijmegen, The Netherlands

    Barbara Franke

  43. Department of Clinical, Educational and Health Psychology, University College London, London, UK

    Jean-Baptiste Pingault

  44. Conway Institute of Biomolecular and Biomedical Sciences, School of Medicine, University College Dublin, Dublin, Ireland

    Jeffrey C. Glennon

  45. Language and Genetics Department, Max Planck Institute for Psycholinguistics, Wundtlaan 1, 6525 XD, Nijmegen, The Netherlands

    Simon E. Fisher

  46. Department of Psychiatry and Behavioral Sciences, State University of New York Health Sciences University, Brooklyn, NY, USA

    Bernice Porjesz, Jacquelyn M. Meyers, Chella Kamarajan & Ashwini Pandey

  47. Department of Psychiatry, University of Connecticut School of Medicine, Farmington, CT, USA

    Victor Hesselbrock

  48. Department of Medical and Molecular Genetics, Indiana University, Indianapolis, IN, USA

    Tatiana Foroud

  49. Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, USA

    Arpana Agrawal, Laura Bierut, John Rice & Kathleen K. Bucholz

  50. Department of Biochemistry and Molecular Biology, Indiana University, Indianapolis, IN, USA

    Howard J. Edenberg

  51. Departments of Medical and Molecular Genetics, Biostatistics, and BioHealth Informatics, Indiana University, Indianapolis, IN, USA

    Yunlong Liu

  52. Department of Psychiatry, Indiana University, Indianapolis, IN, USA

    Martin H. Plawecki

  53. Department of Psychiatry, University of Iowa, Iowa City, IA, USA

    Samuel Kuperman & John R. Kramer

  54. Department of Psychiatry, University of California San Diego Medical School, San Diego, CA, USA

    Marc A. Schuckit

  55. Department of Genetics, Rutgers University, Piscataway, NJ, USA

    Jay Tischfield

  56. Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ, USA

    Ronald Hart

  57. The Children’s Hospital of Philadelphia, University of Pennsylvania, Philadelphia, PA, USA

    Laura Almasy

  58. Departments of Genetics and Genomic Sciences, Neuroscience, and Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Alison Goate

  59. Departments of Neuroscience and Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Paul Slesinger

  60. Department of Pediatrics, Howard University, Washington, DC, USA

    Denise Scott

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  1. Jorim J. Tielbeek
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Consortia

COGA Consortium

  • Bernice Porjesz
  • , Victor Hesselbrock
  • , Tatiana Foroud
  • , Arpana Agrawal
  • , Danielle M. Dick
  • , Howard J. Edenberg
  • , Yunlong Liu
  • , Martin H. Plawecki
  • , Samuel Kuperman
  • , John R. Kramer
  • , Jacquelyn M. Meyers
  • , Chella Kamarajan
  • , Ashwini Pandey
  • , Laura Bierut
  • , John Rice
  • , Kathleen K. Bucholz
  • , Marc A. Schuckit
  • , Jay Tischfield
  • , Ronald Hart
  • , Jessica E. Salvatore
  • , Laura Almasy
  • , Alison Goate
  • , Paul Slesinger
  •  & Denise Scott

Spit for Science Working Group

Contributions

Study concept and design: JJT, TJCP, and DP. Acquisition, analysis, or interpretation of data: EU, BSW, LC-C, EG, TTM, BEL, PRJ, AJ, HMS, GP, GRBS, AGA, KR, BK, MK, AMH, JES, IMN, DD, ALKM, SAB, JES, KS, RP, KMH, SV, MM, WGI, NRM, JM, JFV, BLM, JJM, TFMA, IO-M, RET, SMC, JPG, MRB, GD, FV, and MKL. Drafting of the manuscript: JJT, TJCP, PRJ, BBB, TEM, AC, and DP. Study supervision: TJCP, NGM, EC, KR, JGE, JL, CAH, AJO, HS, HL, MP, AW, EV, PJ, YL, DR, IG, TP, JK, KPH, MRM, GM-V, RP, EV, BBB, FA, DD, AP, SVF, ADB, SEM, BF, MB, JBP, JCG, JCB, SEF, TEM, AC, and DP. All authors critically evaluated and revised the manuscript. JJT had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding author

Correspondence to Jorim J. Tielbeek.

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BF has received educational speaking fees from Medice.

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Tielbeek, J.J., Uffelmann, E., Williams, B.S. et al. Uncovering the genetic architecture of broad antisocial behavior through a genome-wide association study meta-analysis. Mol Psychiatry 27, 4453–4463 (2022). https://doi.org/10.1038/s41380-022-01793-3

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