Transient role of the middle ear as a lower jaw support across mammals

  1. Neal Anthwal
  2. Jane Catherine Fenelon
  3. Stephen D Johnston
  4. Marilyn B Renfree
  5. Abigail S Tucker  Is a corresponding author
  1. King's College London, United Kingdom
  2. University of Melbourne, Australia
  3. University of Queensland, Australia

Abstract

Mammals articulate their jaws using a novel joint between the dentary and squamosal bones. In eutherian mammals, this joint forms in the embryo, supporting feeding and vocalisation from birth. In contrast, marsupials and monotremes exhibit extreme altriciality and are born before the bones of the novel mammalian jaw joint form. These mammals need to rely on other mechanisms to allow them to feed. Here we show that this vital function is carried out by the earlier developing, cartilaginous incus of the middle ear, abutting the cranial base to form a cranio-mandibular articulation. The nature of this articulation varies between monotremes and marsupials, with juvenile monotremes retaining a double articulation, similar to that of the fossil mammaliaform Morganucodon, while marsupials use a versican-rich matrix to stabilise the jaw against the cranial base. These findings provide novel insight into the evolution of mammals and the changing relationship between the jaw and ear.

Data availability

All data generated or analysed during this study are included in the manuscript.

Article and author information

Author details

  1. Neal Anthwal

    Department of Craniofacial Development and Stem Cell Biology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4104-7839
  2. Jane Catherine Fenelon

    School of BioSciences, University of Melbourne, Parkville, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8771-5196
  3. Stephen D Johnston

    School of Agriculture and Food Sciences, University of Queensland, Galton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Marilyn B Renfree

    School of BioSciences, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4589-0436
  5. Abigail S Tucker

    Department of Craniofacial Development and Stem Cell Biology, King's College London, London, United Kingdom
    For correspondence
    abigail.tucker@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8871-6094

Funding

Wellcome (102889/Z/13/Z)

  • Abigail S Tucker

Australian Research Council (Linkage Grant)

  • Stephen D Johnston
  • Marilyn B Renfree

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed under UK Home Office licence and regulations in line with the regulations set out under the United Kingdom Animals (Scientific Procedures) Act 1986 and the European Union Directive 2010/63/EU.

Reviewing Editor

  1. Min Zhu, Chinese Academy of Sciences, China

Publication history

  1. Received: April 14, 2020
  2. Accepted: June 17, 2020
  3. Accepted Manuscript published: June 30, 2020 (version 1)
  4. Version of Record published: July 15, 2020 (version 2)

Copyright

© 2020, Anthwal et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Neal Anthwal
  2. Jane Catherine Fenelon
  3. Stephen D Johnston
  4. Marilyn B Renfree
  5. Abigail S Tucker
(2020)
Transient role of the middle ear as a lower jaw support across mammals
eLife 9:e57860.
https://doi.org/10.7554/eLife.57860

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