Bichir external gills arise via heterochronic shift that accelerates hyoid arch development
- Charles University in Prague, Czech Republic
- 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
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.
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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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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The evolutionary introduction of asymmetric cell division (ACD) into the developmental program facilitates the formation of a new cell type, contributing to developmental diversity and, eventually, species diversification. The micromere of the sea urchin embryo may serve as one of those examples: an ACD at the 16-cell stage forms micromeres unique to echinoids among echinoderms. We previously reported that a polarity factor, activator of G-protein signaling (AGS), plays a crucial role in micromere formation. However, AGS and its associated ACD factors are present in all echinoderms and across most metazoans. This raises the question of what evolutionary modifications of AGS protein or its surrounding molecular environment contributed to the evolutionary acquisition of micromeres only in echinoids. In this study, we learned that the GoLoco motifs at the AGS C-terminus play critical roles in regulating micromere formation in sea urchin embryos. Further, other echinoderms’ AGS or chimeric AGS that contain the C-terminus of AGS orthologs from various organisms showed varied localization and function in micromere formation. In contrast, the sea star or the pencil urchin orthologs of other ACD factors were consistently localized at the vegetal cortex in the sea urchin embryo, suggesting that AGS may be a unique variable factor that facilitates ACD diversity among echinoderms. Consistently, sea urchin AGS appears to facilitate micromere-like cell formation and accelerate the enrichment timing of the germline factor Vasa during early embryogenesis of the pencil urchin, an ancestral type of sea urchin. Based on these observations, we propose that the molecular evolution of a single polarity factor facilitates ACD diversity while preserving the core ACD machinery among echinoderms and beyond during evolution.
