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Genomic evidence consistent with antagonistic pleiotropy may help explain the evolutionary maintenance of same-sex sexual behaviour in humans

An Author Correction to this article was published on 13 September 2021

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Abstract

Human same-sex sexual behaviour (SSB) is heritable, confers no immediately obvious direct reproductive or survival benefit and can divert mating effort from reproductive opportunities. This presents a Darwinian paradox: why has SSB been maintained despite apparent selection against it? We show that genetic effects associated with SSB may, in individuals who only engage in opposite-sex sexual behaviour (OSB individuals), confer a mating advantage. Using results from a recent genome-wide association study of SSB and a new genome-wide association study on number of opposite-sex sexual partners in 358,426 individuals, we show that, among OSB individuals, genetic effects associated with SSB are associated with having more opposite-sex sexual partners. Computer simulations suggest that such a mating advantage for alleles associated with SSB could help explain how it has been evolutionarily maintained. Caveats include the cultural specificity of our UK and US samples, the societal regulation of sexual behaviour in these populations, the difficulty of measuring mating success and the fact that measured variants capture a minority of the total genetic variation in the traits.

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Fig. 1: Evolutionary simulations.
Fig. 2: Per-chromosome SNP-based heritability.

Data availability

This research was conducted using data from the UK Biobank resource (application number 25995). UK Biobank data can be accessed on request once a research project has been submitted and approved by the UK Biobank committee (https://www.ukbiobank.ac.uk/researchers/). Data from The National Longitudinal Study of Adolescent to Adult Health (Add Health) can also be applied for (see https://www.cpc.unc.edu/projects/addhealth/documentation for details). GWAS summary statistics of the number of opposite sex sexual partners among OSB individuals in UK-Biobank are available at GWAS Catalog (https://www.ebi.ac.uk/gwas/downloads/summary-statistics, study accession IDs: GCST90026480, GCST90026481, and GCST90026482). Source data are provided with this paper.

Code availability

Custom code used for statistical analyses is available from the corresponding author upon request. Source data are provided with this paper.

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Acknowledgements

This research was conducted using the UK Biobank Resource under applications 25995. We thank all cohort participants for making this study possible. A.R.S. received funding from the Eunice Kennedy Shriver National Institute of Child Health and Human Development specifically to investigate the genetics of sexual orientation: R01HD041563 (A.R.S. PI) and R21HD080410 (A.R.S., E.R.M. MPI). E.R.M., G.W.B. and S.G. are also supported by R21HD080410. No other member of the group received funding specifically for this study, but members of our team received salary funding from organizations as well as their own universities. B.P.Z. received funding from The Australian Research Council (FT160100298). A.A. is supported by ZonMw grant 849200011 from The Netherlands Organisation for Health Research and Development. Study-specific acknowledgements: This research uses data from Add Health, a programme project directed by K.M. Harris (PI) and designed by J.R. Udry, P.S. Bearman and K.M. Harris at the University of North Carolina at Chapel Hill, and funded by grant P01-HD031921 from the Eunice Kennedy Shriver National Institute of Child Health and Human Development, with cooperative funding from 23 other federal agencies and foundations. Information on how to obtain the Add Health data files is available on the Add Health website (http://www.cpc.unc.edu/addhealth). This research uses Add Health GWAS data funded by Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) grants R01 HD073342 to K. M. Harris (PI) and R01 HD060726 to K.M. Harris, J.D. Boardman and M.B. McQueen (MPIs). The authors thank A. Ganna and M. Nivard for analysis work, A. Ganna, J. Perry, M. Nivard, B. Neale, R. Wedow and M. Keller for extensive discussion, and B. von Hippel, F. Barlow, F. Sathirapongsasuti, A. Auton and J. McCreight for comments on manuscript drafts. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Contributions

B.P.Z. and K.J.H.V. conceived and designed the study. M.S., A.A. and R.M. analysed the data and produced the figures. B.P.Z., M.S. and K.J.H.V. wrote the manuscript. A.A., R.M., J.N.L., S.G., G.W.B., E.R.M. and A.R.S. provided significant feedback on the analyses and the manuscript.

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Correspondence to Brendan P. Zietsch.

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Peer review information Primary Handling Editors: Charlotte Payne and Stavroula Kousta.

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Supplementary Information

I. Evolutionary simulations. II. Notes on the use of lifetime number of sex partners to index mating advantage. III. Overview of GWAS results for number of opposite-sex sexual partners in heterosexuals; (A) QQ plot, (B) Manhattan plot and (C) list of significant SNPs. IV. Further discussion of evolutionary possibilities regarding SSB. V. Pre-registration and changes to the pre-registered plan. VI. Genomic SEM model used to test potential mediating effects of personality traits. VII. 24 VII. General summary and frequently asked questions. Supplementary references. The Supplementary Information includes Supplementary Figs. 1–7 and Tables 1 and 2.

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Zietsch, B.P., Sidari, M.J., Abdellaoui, A. et al. Genomic evidence consistent with antagonistic pleiotropy may help explain the evolutionary maintenance of same-sex sexual behaviour in humans. Nat Hum Behav 5, 1251–1258 (2021). https://doi.org/10.1038/s41562-021-01168-8

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