Bichir external gills arise via heterochronic shift that accelerates hyoid arch development

  1. Jan Stundl
  2. Anna Pospisilova
  3. David Jandzik
  4. Peter Fabian
  5. Barbora Dobiasova
  6. Martin Minarik
  7. Brian D Metscher
  8. Vladimir Soukup  Is a corresponding author
  9. Robert Cerny  Is a corresponding author
  1. Charles University in Prague, Czech Republic
  2. University of Vienna, Austria

Abstract

In most vertebrates, pharyngeal arches form in a stereotypic anterior-to-posterior progression. To gain insight into the mechanisms underlying evolutionary changes in pharyngeal arch development, here we investigate embryos and larvae of bichirs. Bichirs represent the earliest diverged living group of ray-finned fishes, and possess intriguing traits otherwise typical for lobe-finned fishes such as ventral paired lungs and larval external gills. In bichir embryos, we find that the anteroposterior way of formation of cranial segments is modified by the unique acceleration of the entire hyoid arch segment, with earlier and orchestrated development of the endodermal, mesodermal, and neural crest tissues. This major heterochronic shift in the anteroposterior developmental sequence enables early appearance of the external gills that represent key breathing organs of bichir free-living embryos and early larvae. Bichirs thus stay as unique models for understanding developmental mechanisms facilitating increased breathing capacity.

Data availability

All data generated and analysed during this study are included in the manuscript and providing files. All sources are cited in the Methods chapter.

Article and author information

Author details

  1. Jan Stundl

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  2. Anna Pospisilova

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  3. David Jandzik

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  4. Peter Fabian

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  5. Barbora Dobiasova

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Martin Minarik

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6660-0031
  7. Brian D Metscher

    Department of Theoretical Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Vladimir Soukup

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    For correspondence
    vladimir.soukup@natur.cuni.cz
    Competing interests
    The authors declare that no competing interests exist.
  9. Robert Cerny

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    For correspondence
    robert.cerny@natur.cuni.cz
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0022-0199

Funding

Charles University Grant Agency (1448514)

  • Jan Stundl

Charles University Grant Agency (640016)

  • Anna Pospisilova

Charles University Grant Agency (220213)

  • Martin Minarik

Czech Science Foundation (16-23836S)

  • Robert Cerny

Charles University Grant Agency (726516)

  • Martin Minarik

The Charles University grant SVV (260434/2019)

  • Jan Stundl
  • Anna Pospisilova
  • David Jandzik
  • Vladimir Soukup
  • Robert Cerny

The Charles University Research Centre program (204069)

  • Vladimir Soukup

The grant of the Scientific Grant Agency of Slovak Republic VEGA (1/0415/17)

  • David Jandzik

The European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant (751066)

  • David Jandzik

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

Reviewing Editor

  1. Tanya T Whitfield, University of Sheffield, United Kingdom

Version history

  1. Received: November 9, 2018
  2. Accepted: March 15, 2019
  3. Accepted Manuscript published: March 26, 2019 (version 1)
  4. Version of Record published: March 29, 2019 (version 2)

Copyright

© 2019, Stundl 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. Jan Stundl
  2. Anna Pospisilova
  3. David Jandzik
  4. Peter Fabian
  5. Barbora Dobiasova
  6. Martin Minarik
  7. Brian D Metscher
  8. Vladimir Soukup
  9. Robert Cerny
(2019)
Bichir external gills arise via heterochronic shift that accelerates hyoid arch development
eLife 8:e43531.
https://doi.org/10.7554/eLife.43531

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