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Narrow-sense heritability estimation of complex traits using identity-by-descent information

View ORCID ProfileLuke M. Evans, Rasool Tahmasbi, Matthew Jones, View ORCID ProfileScott I. Vrieze, Gonçalo R. Abecasis, Sayantan Das, Doug W. Bjelland, Teresa R. deCandia, - Haplotype Reference Consortium, Gonçalo Abecasis, David Altshuler, Carl A Anderson, Andrea Angius, Jeffrey C Barrett, Sonja Berndt, Michael Boehnke, Dorrett Boomsma, Kari Branham, Gerome Breen, Chad M Brummett, Fabio Busonero, Harry Campbell, Peter Campbell, Andrew Chan, Sai Chen, Emily Chew, Massimiliano Cocca, Francis S Collins, Laura J Corbin, Francesco Cucca, Petr Danecek, Sayantan Das, Paul I W de Bakker, George Dedoussis, Annelot Dekker, Olivier Delaneau, Marcus Dorr, Richard Durbin, Aliki-Eleni Farmaki, Luigi Ferrucci, Lukas Forer, Ross M Fraser, Timothy Frayling, Christian Fuchsberger, Stacey Gabriel, Ilaria Gandin, Paolo Gasparini, Christopher E Gillies, Arthur Gilly, Leif Groop, Tabitha Harrison, Andrew Hattersley, Oddgeir L Holmen, Kristian Hveem, William Iacono, Amit Joshi, Hyun Min Kang, Hamed Khalili, Charles Kooperberg, Seppo Koskinen, Matthias Kretzler, Warren Kretzschmar, Alan Kwong, James C Lee, Shawn Levy, Yang Luo, Anubha Mahajan, Jonathan Marchini, Steven McCarroll, Mark I McCarthy, Shane McCarthy, Matt McGue, Melvin McInnis, Thomas Meitinger, David Melzer, Massimo Mezzavilla, Josine L Min, Karen L Mohlke, Richard M Myers, Matthias Nauck, Deborah Nickerson, Aarno Palotie, Carlos Pato, Michele Pato, Ulrike Peters, Nicola Pirastu, Wouter Van Rheenen, J Brent Richards, Samuli Ripatti, Cinzia Sala, Veikko Salomaa, Matthew G Sampson, David Schlessinger, Robert E Schoen, Sebastian Schoenherr, Laura J Scott, Kevin Sharp, Carlo Sidore, P Eline Slagboom, Kerrin Small, George Davey Smith, Nicole Soranzo, Timothy Spector, Dwight Stambolian, Anand Swaroop, Morris A Swertz, Alexander Teumer, Nicholas Timpson, Daniela Toniolo, Michela Traglia, Marcus Tuke, Jaakko Tuomilehto, Leonard H Van den Berg, Cornelia M van Duijn, Jan Veldink, John B Vincent, Uwe Volker, Scott Vrieze, Klaudia Walter, Cisca Wijmenga, Cristen Willer, James F Wilson, Andrew R Wood, Eleftheria Zeggini, He Zhang, Jian Yang, Michael E. Goddard, Peter M. Visscher, Matthew C. Keller
doi: https://doi.org/10.1101/164848
Luke M. Evans
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
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  • ORCID record for Luke M. Evans
  • For correspondence: luke.m.evans@colorado.edu matthew.c.keller@gmail.com
Rasool Tahmasbi
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
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Matthew Jones
2Department of Psychology and Neuroscience, University of Colorado, Boulder, CO, 80309
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Scott I. Vrieze
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
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Gonçalo R. Abecasis
3Center for Statistical Genetics, Department of Biostatistics, University of Michigan, Ann Arbor, MI 48109
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Sayantan Das
3Center for Statistical Genetics, Department of Biostatistics, University of Michigan, Ann Arbor, MI 48109
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Doug W. Bjelland
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
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Teresa R. deCandia
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
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Gonçalo Abecasis
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Jian Yang
4Institute for Molecular Bioscience and the Queensland Brain Institute, University of Queensland, Brisbane, 4072, Queensland, Australia
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Michael E. Goddard
5Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville, Victoria, Australia
6Biosciences Research, Department of Economic Development, Jobs, Transport and Resources, Victoria, Australia
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Peter M. Visscher
4Institute for Molecular Bioscience and the Queensland Brain Institute, University of Queensland, Brisbane, 4072, Queensland, Australia
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Matthew C. Keller
1Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80309
2Department of Psychology and Neuroscience, University of Colorado, Boulder, CO, 80309
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  • For correspondence: luke.m.evans@colorado.edu matthew.c.keller@gmail.com
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ABSTRACT

Heritability is a fundamental parameter in genetics. Traditional estimates based on family or twin studies can be biased due to shared environmental or non-additive genetic variance. Alternatively, those based on genotyped or imputed variants typically underestimate narrow-sense heritability contributed by rare or otherwise poorly-tagged causal variants. Identical-by-descent (IBD) segments of the genome share all variants between pairs of chromosomes except new mutations that have arisen since the last common ancestor. Therefore, relating phenotypic similarity to degree of IBD sharing among classically unrelated individuals is an appealing approach to estimating the near full additive genetic variance while avoiding biases that can occur when modeling close relatives. We applied an IBD-based approach (GREML-IBD) to estimate heritability in unrelated individuals using phenotypic simulation with thousands of whole genome sequences across a range of stratification, polygenicity levels, and the minor allele frequencies of causal variants (CVs). IBD-based heritability estimates were unbiased when using unrelated individuals, even for traits with extremely rare CVs, but stratification led to strong biases in IBD-based heritability estimates with poor precision. We used data on two traits in ~120,000 people from the UK Biobank to demonstrate that, depending on the trait and possible confounding environmental effects, GREML-IBD can be applied successfully to very large genetic datasets to infer the contribution of very rare variants lost using other methods. However, we observed apparent biases in this real data that were not predicted from our simulation, suggesting that more work may be required to understand factors that influence IBD-based estimates.

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Narrow-sense heritability estimation of complex traits using identity-by-descent information
Luke M. Evans, Rasool Tahmasbi, Matthew Jones, Scott I. Vrieze, Gonçalo R. Abecasis, Sayantan Das, Doug W. Bjelland, Teresa R. deCandia, - Haplotype Reference Consortium, Gonçalo Abecasis, David Altshuler, Carl A Anderson, Andrea Angius, Jeffrey C Barrett, Sonja Berndt, Michael Boehnke, Dorrett Boomsma, Kari Branham, Gerome Breen, Chad M Brummett, Fabio Busonero, Harry Campbell, Peter Campbell, Andrew Chan, Sai Chen, Emily Chew, Massimiliano Cocca, Francis S Collins, Laura J Corbin, Francesco Cucca, Petr Danecek, Sayantan Das, Paul I W de Bakker, George Dedoussis, Annelot Dekker, Olivier Delaneau, Marcus Dorr, Richard Durbin, Aliki-Eleni Farmaki, Luigi Ferrucci, Lukas Forer, Ross M Fraser, Timothy Frayling, Christian Fuchsberger, Stacey Gabriel, Ilaria Gandin, Paolo Gasparini, Christopher E Gillies, Arthur Gilly, Leif Groop, Tabitha Harrison, Andrew Hattersley, Oddgeir L Holmen, Kristian Hveem, William Iacono, Amit Joshi, Hyun Min Kang, Hamed Khalili, Charles Kooperberg, Seppo Koskinen, Matthias Kretzler, Warren Kretzschmar, Alan Kwong, James C Lee, Shawn Levy, Yang Luo, Anubha Mahajan, Jonathan Marchini, Steven McCarroll, Mark I McCarthy, Shane McCarthy, Matt McGue, Melvin McInnis, Thomas Meitinger, David Melzer, Massimo Mezzavilla, Josine L Min, Karen L Mohlke, Richard M Myers, Matthias Nauck, Deborah Nickerson, Aarno Palotie, Carlos Pato, Michele Pato, Ulrike Peters, Nicola Pirastu, Wouter Van Rheenen, J Brent Richards, Samuli Ripatti, Cinzia Sala, Veikko Salomaa, Matthew G Sampson, David Schlessinger, Robert E Schoen, Sebastian Schoenherr, Laura J Scott, Kevin Sharp, Carlo Sidore, P Eline Slagboom, Kerrin Small, George Davey Smith, Nicole Soranzo, Timothy Spector, Dwight Stambolian, Anand Swaroop, Morris A Swertz, Alexander Teumer, Nicholas Timpson, Daniela Toniolo, Michela Traglia, Marcus Tuke, Jaakko Tuomilehto, Leonard H Van den Berg, Cornelia M van Duijn, Jan Veldink, John B Vincent, Uwe Volker, Scott Vrieze, Klaudia Walter, Cisca Wijmenga, Cristen Willer, James F Wilson, Andrew R Wood, Eleftheria Zeggini, He Zhang, Jian Yang, Michael E. Goddard, Peter M. Visscher, Matthew C. Keller
bioRxiv 164848; doi: https://doi.org/10.1101/164848
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Narrow-sense heritability estimation of complex traits using identity-by-descent information
Luke M. Evans, Rasool Tahmasbi, Matthew Jones, Scott I. Vrieze, Gonçalo R. Abecasis, Sayantan Das, Doug W. Bjelland, Teresa R. deCandia, - Haplotype Reference Consortium, Gonçalo Abecasis, David Altshuler, Carl A Anderson, Andrea Angius, Jeffrey C Barrett, Sonja Berndt, Michael Boehnke, Dorrett Boomsma, Kari Branham, Gerome Breen, Chad M Brummett, Fabio Busonero, Harry Campbell, Peter Campbell, Andrew Chan, Sai Chen, Emily Chew, Massimiliano Cocca, Francis S Collins, Laura J Corbin, Francesco Cucca, Petr Danecek, Sayantan Das, Paul I W de Bakker, George Dedoussis, Annelot Dekker, Olivier Delaneau, Marcus Dorr, Richard Durbin, Aliki-Eleni Farmaki, Luigi Ferrucci, Lukas Forer, Ross M Fraser, Timothy Frayling, Christian Fuchsberger, Stacey Gabriel, Ilaria Gandin, Paolo Gasparini, Christopher E Gillies, Arthur Gilly, Leif Groop, Tabitha Harrison, Andrew Hattersley, Oddgeir L Holmen, Kristian Hveem, William Iacono, Amit Joshi, Hyun Min Kang, Hamed Khalili, Charles Kooperberg, Seppo Koskinen, Matthias Kretzler, Warren Kretzschmar, Alan Kwong, James C Lee, Shawn Levy, Yang Luo, Anubha Mahajan, Jonathan Marchini, Steven McCarroll, Mark I McCarthy, Shane McCarthy, Matt McGue, Melvin McInnis, Thomas Meitinger, David Melzer, Massimo Mezzavilla, Josine L Min, Karen L Mohlke, Richard M Myers, Matthias Nauck, Deborah Nickerson, Aarno Palotie, Carlos Pato, Michele Pato, Ulrike Peters, Nicola Pirastu, Wouter Van Rheenen, J Brent Richards, Samuli Ripatti, Cinzia Sala, Veikko Salomaa, Matthew G Sampson, David Schlessinger, Robert E Schoen, Sebastian Schoenherr, Laura J Scott, Kevin Sharp, Carlo Sidore, P Eline Slagboom, Kerrin Small, George Davey Smith, Nicole Soranzo, Timothy Spector, Dwight Stambolian, Anand Swaroop, Morris A Swertz, Alexander Teumer, Nicholas Timpson, Daniela Toniolo, Michela Traglia, Marcus Tuke, Jaakko Tuomilehto, Leonard H Van den Berg, Cornelia M van Duijn, Jan Veldink, John B Vincent, Uwe Volker, Scott Vrieze, Klaudia Walter, Cisca Wijmenga, Cristen Willer, James F Wilson, Andrew R Wood, Eleftheria Zeggini, He Zhang, Jian Yang, Michael E. Goddard, Peter M. Visscher, Matthew C. Keller
bioRxiv 164848; doi: https://doi.org/10.1101/164848

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