Bichir external gills arise via heterochronic shift that accelerates hyoid arch development
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.
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Author details
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
- Tanya T Whitfield, University of Sheffield, United Kingdom
Version history
- Received: November 9, 2018
- Accepted: March 15, 2019
- Accepted Manuscript published: March 26, 2019 (version 1)
- 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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