Developmental constraint through negative pleiotropy in the zygomatic arch Public Deposited

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Creator
  • Morgan, Judith L
    • Other Affiliation: The Jackson Laboratory, Bar Harbor, USA
  • Gatti, Daniel M
    • Other Affiliation: The Jackson Laboratory, Bar Harbor, USA
  • Marcucio, Ralph
    • Other Affiliation: The Orthopaedic Trauma Institute, Department of Orthopaedic Surgery, UCSF School of Medicine, San Francisco, USA
  • Green, Rebecca
    • Other Affiliation: Alberta Children’s Hospital Institute for Child and Maternal Health, University of Calgary, Calgary, Canada; The McCaig Bone and Joint Institute, University of Calgary, Calgary, Canada; Department of Cell Biology and Anatomy, University of Calgary, Calgary, Canada
  • Donahue, Leah R
    • Other Affiliation: The Jackson Laboratory, Bar Harbor, USA
  • Pollard, K. M
    • Other Affiliation: Department of Molecular Medicine, The Scripps Research Institute, La Jolla, USA
  • Mayeux, Jessica M
    • Other Affiliation: Department of Molecular Medicine, The Scripps Research Institute, La Jolla, USA
  • Hallgrímsson, Benedikt
    • Other Affiliation: Alberta Children’s Hospital Institute for Child and Maternal Health, University of Calgary, Calgary, Canada; The McCaig Bone and Joint Institute, University of Calgary, Calgary, Canada; Department of Cell Biology and Anatomy, University of Calgary, Calgary, Canada
  • Roseman, Charles C
    • Other Affiliation: Program in Ecology Evolution and Conservation Biology, University of Illinois, Urbana, USA
  • Hua, Kunjie
    • Affiliation: School of Medicine, Department of Genetics
  • Percival, Christopher J
    • Other Affiliation: Department of Anthropology, Stony Brook University, Stony Brook, USA
  • Pomp, Daniel
    • Affiliation: School of Medicine, Department of Genetics
  • Murray, Stephen A
    • Other Affiliation: The Jackson Laboratory, Bar Harbor, USA
Abstract
  • Abstract Background Previous analysis suggested that the relative contribution of individual bones to regional skull lengths differ between inbred mouse strains. If the negative correlation of adjacent bone lengths is associated with genetic variation in a heterogeneous population, it would be an example of negative pleiotropy, which occurs when a genetic factor leads to opposite effects in two phenotypes. Confirming negative pleiotropy and determining its basis may reveal important information about the maintenance of overall skull integration and developmental constraint on skull morphology. Results We identified negative correlations between the lengths of the frontal and parietal bones in the midline cranial vault as well as the zygomatic bone and zygomatic process of the maxilla, which contribute to the zygomatic arch. Through gene association mapping of a large heterogeneous population of Diversity Outbred (DO) mice, we identified a quantitative trait locus on chromosome 17 driving the antagonistic contribution of these two zygomatic arch bones to total zygomatic arch length. Candidate genes in this region were identified and real-time PCR of the maxillary processes of DO founder strain embryos indicated differences in the RNA expression levels for two of the candidate genes, Camkmt and Six2. Conclusions A genomic region underlying negative pleiotropy of two zygomatic arch bones was identified, which provides a mechanism for antagonism in component bone lengths while constraining overall zygomatic arch length. This type of mechanism may have led to variation in the contribution of individual bones to the zygomatic arch noted across mammals. Given that similar genetic and developmental mechanisms may underlie negative correlations in other parts of the skull, these results provide an important step toward understanding the developmental basis of evolutionary variation and constraint in skull morphology.
Date of publication
Identifier
  • doi:10.1186/s13227-018-0092-3
Resource type
  • Article
Rights statement
  • In Copyright
Rights holder
  • The Author(s)
Language
  • English
Bibliographic citation
  • EvoDevo. 2018 Jan 27;9(1):3
Publisher
  • BioMed Central
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