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.

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.

Metrics

  • 3,055
    views
  • 463
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.57860

Further reading

    1. Cell Biology
    2. Developmental Biology
    Dilara N Anbarci, Jennifer McKey ... Blanche Capel
    Research Article

    The rete ovarii (RO) is an appendage of the ovary that has been given little attention. Although the RO appears in drawings of the ovary in early versions of Gray’s Anatomy, it disappeared from recent textbooks, and is often dismissed as a functionless vestige in the adult ovary. Using PAX8 immunostaining and confocal microscopy, we characterized the fetal development of the RO in the context of the mouse ovary. The RO consists of three distinct regions that persist in adult life, the intraovarian rete (IOR), the extraovarian rete (EOR), and the connecting rete (CR). While the cells of the IOR appear to form solid cords within the ovary, the EOR rapidly develops into a convoluted tubular epithelium ending in a distal dilated tip. Cells of the EOR are ciliated and exhibit cellular trafficking capabilities. The CR, connecting the EOR to the IOR, gradually acquires tubular epithelial characteristics by birth. Using microinjections into the distal dilated tip of the EOR, we found that luminal contents flow toward the ovary. Mass spectrometry revealed that the EOR lumen contains secreted proteins potentially important for ovarian function. We show that the cells of the EOR are closely associated with vasculature and macrophages, and are contacted by neuronal projections, consistent with a role as a sensory appendage of the ovary. The direct proximity of the RO to the ovary and its integration with the extraovarian landscape suggest that it plays an important role in ovary development and homeostasis.

    1. Cell Biology
    2. Developmental Biology
    Yan Zhang, Hua Zhang
    Insight

    Long thought to have little relevance to ovarian physiology, the rete ovarii may have a role in follicular dynamics and reproductive health.