Genetic evidence of assortative mating in humans

Abstract

In human populations, assortative mating is almost univer­sally positive, with similarities between partners for quantit­ative phenotypes16, common disease risk1,3,710, beha­vi­our6,11, social factors1214 and personality4,5,11. The causes and genetic consequences of assortative mating remain un­re­solved because partner similarity can arise from different mechanisms: phenotypic assortment based on mate choice15,16, partner interaction and convergence in phenotype over time14,17, or social homogamy where individuals pair according to social or environmental background. Here, we present theory and an analytical approach to test for genetic evidence of assortative mating and find a correlation in genetic value among partners for a range of phenotypes. Across three independent samples of 24,662 spousal pairs in total, we infer a correlation at trait-associated loci between partners for height (0.200, 0.004 standard error, SE) that matched the phenotypic correlation (0.201, 0.004 SE), and a correlation at trait-associated loci for BMI (0.143, 0.007 SE) that was significantly lower than the phenotypic value (0.228, 0.004 SE). We extend our analysis to the UK Biobank study (7,780 pairs), finding evidence of a correlation at trait-associated loci for waist-to-hip ratio (0.101, 0.041 SE), systolic blood pressure (0.138, 0.064 SE) and educational attainment (0.654, 0.014 SE). Our results imply that mate choice, combined with widespread pleiotropy among traits, affects the genomic architecture of traits in humans.

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Figure 1: Assortative mating for height and BMI creates a correlation at trait-associated loci among partners.
Figure 2: Genetic evidence for assortative mating across a range of phenotypes in the UK Biobank study.

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Acknowledgements

The University of Queensland group is supported by the Australian National Health and Medical Research Council (NHMRC grants 1078037, 1048853 and 1050218), the Australian Research Council (Discovery Project 160103860) and the National Institute of Health (NIH grants R21ESO25052-01, R01AG042568 and PO1GMO99568). J.Y. is supported by a Charles and Sylvia Viertel Senior Medical Research Fellowship. We thank the participants of the cohort studies, as well as C. Haley and our colleagues at the Program in Complex Trait Genomics, for comments and suggestions. 23andMe cohort thank the research participants and employees of 23andMe. This work was supported by the National Human Genome Research Institute of the NIH (grant number R44HG006981). The UK Biobank research was conducted using the UK Biobank Resource under project 12514. TWINGENE was supported by the Swedish Research Council (M-2005-1112), GenomEUtwin (EU/QLRT-2001-01254; QLG2-CT-2002-01254), NIH DK U01-066134, the Swedish Foundation for Strategic Research, and the Heart and Lung Foundation grant no. 20070481. The Atherosclerosis Risk in Communities Study (ARIC) is a collaborative study supported by National Heart, Lung, and Blood Institute contracts (HHSN268201100005C, HHSN268201100006C, HHSN268201100007C, HHSN268201100008C, HHSN268201100009C, HHSN268201100010C, HHSN268201100011C, and HHSN268201100012C). K.E.N and M.G. are supported by NIDDK R01 DK089256. We thank the staff and participants of the ARIC study for their contributions. Generation and management of GWAS genotype data for the LifeLines Cohort Study is supported by the Netherlands Organization of Scientific Research (grant 175.010.2007.006), the Economic Structure Enhancing Fund of the Dutch government, the Ministry of Economic Affairs, the Ministry of Education, Culture and Science, the Ministry for Health, Welfare and Sports, the Northern Netherlands Collaboration of Provinces, the Province of Groningen, University Medical Center Groningen, the University of Groningen, Dutch Kidney Foundation and Dutch Diabetes Research Foundation. The authors acknowledge the services of the LifeLines Cohort Study, the contributing research centres delivering data to LifeLines, and all the study participants. Minnesota Center for Twin and Family Research (MCTFR) is funded by US Public Health Service grants from the National Institute on Alcohol Abuse and Alcoholism (AA09367, AA11886), National Institute on Drug Abuse (DA05147, DA13240, DA024417, DA036216) and National Institute of Mental Health (MH066140). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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M.R.R., J.Y. and P.M.V. conceived and designed the study. M.R.R., A.K. and M.G. analysed the data. M.R.R. devised and performed the simulations. A.A.E.V., W.J.P., A.A., B.Z., S.M. provided statistical support. 23andMe Inc., The LifeLines cohort, GIANT consortium, G.W.M., N.G.M., M.L., P.L., D.C., J.V.V.O., M.B.M., H.S., W.G.I., P.K.E.M, N.L.P, M.McG. and K.E.N. provided study oversight, sample collection and management. M.R.R. and P.M.V. derived the theory and wrote the manuscript. All collaborators reviewed and approved the final manuscript.

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Correspondence to Matthew R. Robinson or Peter M. Visscher.

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Supplementary Figures 1–9, Supplementary Table 1, Supplementary Note, Supplementary Methods, Supplementary References, Author Lists (PDF 3325 kb)

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Robinson, M., Kleinman, A., Graff, M. et al. Genetic evidence of assortative mating in humans. Nat Hum Behav 1, 0016 (2017). https://doi.org/10.1038/s41562-016-0016

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