Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population

Abstract Human craniofacial shape is highly variable yet highly heritable with numerous genetic variants interacting through multiple layers of development. Here, we hypothesize that Mendelian phenotypes represent the extremes of a phenotypic spectrum and, using achondroplasia as an example, we intr...

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Main Authors: Michiel Vanneste, Hanne Hoskens, Seppe Goovaerts, Harold Matthews, Jay Devine, Jose D. Aponte, Joanne Cole, Mark Shriver, Mary L. Marazita, Seth M. Weinberg, Susan Walsh, Stephen Richmond, Ophir D. Klein, Richard A. Spritz, Hilde Peeters, Benedikt Hallgrímsson, Peter Claes
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54839-1
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author Michiel Vanneste
Hanne Hoskens
Seppe Goovaerts
Harold Matthews
Jay Devine
Jose D. Aponte
Joanne Cole
Mark Shriver
Mary L. Marazita
Seth M. Weinberg
Susan Walsh
Stephen Richmond
Ophir D. Klein
Richard A. Spritz
Hilde Peeters
Benedikt Hallgrímsson
Peter Claes
author_facet Michiel Vanneste
Hanne Hoskens
Seppe Goovaerts
Harold Matthews
Jay Devine
Jose D. Aponte
Joanne Cole
Mark Shriver
Mary L. Marazita
Seth M. Weinberg
Susan Walsh
Stephen Richmond
Ophir D. Klein
Richard A. Spritz
Hilde Peeters
Benedikt Hallgrímsson
Peter Claes
author_sort Michiel Vanneste
collection DOAJ
description Abstract Human craniofacial shape is highly variable yet highly heritable with numerous genetic variants interacting through multiple layers of development. Here, we hypothesize that Mendelian phenotypes represent the extremes of a phenotypic spectrum and, using achondroplasia as an example, we introduce a syndrome-informed phenotyping approach to identify genomic loci associated with achondroplasia-like facial variation in the general population. We compare three-dimensional facial scans from 43 individuals with achondroplasia and 8246 controls to calculate achondroplasia-like facial scores. Multivariate GWAS of the control scores reveals a polygenic basis for facial variation along an achondroplasia-specific shape axis, identifying genes primarily involved in skeletal development. Jointly modeling these genes in two independent control samples, both human and mouse, shows craniofacial effects approximating the characteristic achondroplasia phenotype. These findings suggest that both complex and Mendelian genetic variation act on the same developmentally determined axes of facial variation, providing insights into the genetic intersection of complex traits and Mendelian disorders.
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spelling doaj-art-53249a4e52054d56af916527ff5bdc392025-08-20T02:31:19ZengNature PortfolioNature Communications2041-17232024-12-0115111310.1038/s41467-024-54839-1Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general populationMichiel Vanneste0Hanne Hoskens1Seppe Goovaerts2Harold Matthews3Jay Devine4Jose D. Aponte5Joanne Cole6Mark Shriver7Mary L. Marazita8Seth M. Weinberg9Susan Walsh10Stephen Richmond11Ophir D. Klein12Richard A. Spritz13Hilde Peeters14Benedikt Hallgrímsson15Peter Claes16Department of Human Genetics, KU LeuvenDepartment of Cell Biology & Anatomy, Cumming School of Medicine, University of CalgaryDepartment of Human Genetics, KU LeuvenDepartment of Human Genetics, KU LeuvenMedical Imaging Research Center, University Hospitals LeuvenDepartment of Cell Biology & Anatomy, Cumming School of Medicine, University of CalgaryDepartment of Biomedical Informatics, University of Colorado School of MedicineDepartment of Anthropology, Pennsylvania State UniversityCenter for Craniofacial and Dental Genetics, Department of Oral and Craniofacial Sciences, School of Dental Medicine, University of PittsburghCenter for Craniofacial and Dental Genetics, Department of Oral and Craniofacial Sciences, School of Dental Medicine, University of PittsburghDepartment of Biology, Indiana University Purdue University IndianapolisApplied Clinical Research and Public Health, School of Dentistry, Cardiff UniversityDepartment of Pediatrics, Cedars-Sinai Guerin Children’sDepartment of Pediatrics, University of Colorado School of MedicineDepartment of Human Genetics, KU LeuvenDepartment of Cell Biology & Anatomy, Cumming School of Medicine, University of CalgaryDepartment of Human Genetics, KU LeuvenAbstract Human craniofacial shape is highly variable yet highly heritable with numerous genetic variants interacting through multiple layers of development. Here, we hypothesize that Mendelian phenotypes represent the extremes of a phenotypic spectrum and, using achondroplasia as an example, we introduce a syndrome-informed phenotyping approach to identify genomic loci associated with achondroplasia-like facial variation in the general population. We compare three-dimensional facial scans from 43 individuals with achondroplasia and 8246 controls to calculate achondroplasia-like facial scores. Multivariate GWAS of the control scores reveals a polygenic basis for facial variation along an achondroplasia-specific shape axis, identifying genes primarily involved in skeletal development. Jointly modeling these genes in two independent control samples, both human and mouse, shows craniofacial effects approximating the characteristic achondroplasia phenotype. These findings suggest that both complex and Mendelian genetic variation act on the same developmentally determined axes of facial variation, providing insights into the genetic intersection of complex traits and Mendelian disorders.https://doi.org/10.1038/s41467-024-54839-1
spellingShingle Michiel Vanneste
Hanne Hoskens
Seppe Goovaerts
Harold Matthews
Jay Devine
Jose D. Aponte
Joanne Cole
Mark Shriver
Mary L. Marazita
Seth M. Weinberg
Susan Walsh
Stephen Richmond
Ophir D. Klein
Richard A. Spritz
Hilde Peeters
Benedikt Hallgrímsson
Peter Claes
Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
Nature Communications
title Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
title_full Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
title_fullStr Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
title_full_unstemmed Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
title_short Syndrome-informed phenotyping identifies a polygenic background for achondroplasia-like facial variation in the general population
title_sort syndrome informed phenotyping identifies a polygenic background for achondroplasia like facial variation in the general population
url https://doi.org/10.1038/s41467-024-54839-1
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