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Mega-analysis of 31,396 individuals from 6 countries uncovers strong gene-environment interaction for human fertility

Felix C. Tropf, Renske M. Verweij, Peter J. van der Most, Gert Stulp, Andrew Bakshi, Daniel A. Briley, Matthew Robinson, Anastasia Numan, Tõnu Esko, Andres Metspalu, Sarah E. Medland, Nicholas G. Martin, Harold Snieder, S. Hong Lee, Melinda C. Mills
doi: https://doi.org/10.1101/049163
Felix C. Tropf
1Department of Sociology/ Nuffield College, University of Oxford, Oxford OX1 3UQ, UK
2Department of Sociology/Interuniversity Center for Social Science Theory and Methodology, University of Groningen, Groningen 9712 TG, The Netherlands
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  • For correspondence: fctropf@gmail.com
Renske M. Verweij
2Department of Sociology/Interuniversity Center for Social Science Theory and Methodology, University of Groningen, Groningen 9712 TG, The Netherlands
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Peter J. van der Most
3Department of Epidemiology, University of Groningen, University Medical Center Groningen, Groningen 9700 RB, Netherlands.
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Gert Stulp
4Department of Population Health, London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
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Andrew Bakshi
5The University of Queensland, Queensland Brain Institute, Brisbane, QLD 4072, Australia
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Daniel A. Briley
6Department of Psychology, University of Illinois at Urbana-Champaign, Champaign 61820-9998, USA
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Matthew Robinson
5The University of Queensland, Queensland Brain Institute, Brisbane, QLD 4072, Australia
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Anastasia Numan
7Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, PO Box 281, Stockholm SE-171 77, Sweden
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Tõnu Esko
8Estonian Genome Center, University of Tartu, Tartu, Estonia, 51010, 140 Cambridge 02142, MA, USA
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Andres Metspalu
8Estonian Genome Center, University of Tartu, Tartu, Estonia, 51010, 140 Cambridge 02142, MA, USA
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Sarah E. Medland
10Quantitative Genetics Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, QLD 4029, Australia
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Nicholas G. Martin
10Quantitative Genetics Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, QLD 4029, Australia
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Harold Snieder
3Department of Epidemiology, University of Groningen, University Medical Center Groningen, Groningen 9700 RB, Netherlands.
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S. Hong Lee
5The University of Queensland, Queensland Brain Institute, Brisbane, QLD 4072, Australia
11School of Environmental and Rural Science, The University of New England, Armidale NSW 2351, Australia
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Melinda C. Mills
1Department of Sociology/ Nuffield College, University of Oxford, Oxford OX1 3UQ, UK
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Abstract

Family and twin studies suggest that up to 50% of individual differences in human fertility within a population might be heritable. However, it remains unclear whether the genes associated with fertility outcomes such as number of children ever born (NEB) or age at first birth (AFB) are the same across geographical and historical environments. By not taking this into account, previous genetic studies implicitly assumed that the genetic effects are constant across time and space. We conduct a mega-analysis applying whole genome methods on 31,396 unrelated men and women from six Western countries. Across all individuals and environments, common single-nucleotide polymorphisms (SNPs) explained only ~4% of the variance in NEB and AFB. We then extend these models to test whether genetic effects are shared across different environments or unique to them. For individuals belonging to the same population and demographic cohort (born before or after the 20th century fertility decline), SNP-based heritability was almost five times higher at 22% for NEB and 19% for AFB. We also found no evidence suggesting that genetic effects on fertility are shared across time and space. Our findings imply that the environment strongly modifies genetic effects on the tempo and quantum of fertility, that currently ongoing natural selection is heterogeneous across environments, and that gene-environment interactions may partly account for missing heritability in fertility. Future research needs to combine efforts from genetic research and from the social sciences to better understand human fertility.

Authors Summary Fertility behavior – such as age at first birth and number of children – varies strongly across historical time and geographical space. Yet, family and twin studies, which suggest that up to 50% of individual differences in fertility are heritable, implicitly assume that the genes important for fertility are the same across both time and space. Using molecular genetic data (SNPs) from over 30,000 unrelated individuals from six different countries, we show that different genes influence fertility in different time periods and different countries, and that the genetic effects consistently related to fertility are presumably small. The fact that genetic effects on fertility appear not to be universal could have tremendous implications for research in the area of reproductive medicine, social science and evolutionary biology alike.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 18, 2016.
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Mega-analysis of 31,396 individuals from 6 countries uncovers strong gene-environment interaction for human fertility
Felix C. Tropf, Renske M. Verweij, Peter J. van der Most, Gert Stulp, Andrew Bakshi, Daniel A. Briley, Matthew Robinson, Anastasia Numan, Tõnu Esko, Andres Metspalu, Sarah E. Medland, Nicholas G. Martin, Harold Snieder, S. Hong Lee, Melinda C. Mills
bioRxiv 049163; doi: https://doi.org/10.1101/049163
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Mega-analysis of 31,396 individuals from 6 countries uncovers strong gene-environment interaction for human fertility
Felix C. Tropf, Renske M. Verweij, Peter J. van der Most, Gert Stulp, Andrew Bakshi, Daniel A. Briley, Matthew Robinson, Anastasia Numan, Tõnu Esko, Andres Metspalu, Sarah E. Medland, Nicholas G. Martin, Harold Snieder, S. Hong Lee, Melinda C. Mills
bioRxiv 049163; doi: https://doi.org/10.1101/049163

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