Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network
- University of Cologne, Germany
- The Natural History Museum, United Kingdom
- University of Illinois at Chicago, United States
Abstract
Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways. Drosophila and the beetle Tribolium share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp Nasonia and bug Oncopeltus rely more strongly on BMP signalling. Here, we show that in the cricket Gryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like in Drosophila, a direct patterning role for the ventral half of the embryo. In addition, Toll polarizes BMP signalling, although this does not involve the conserved BMP inhibitor Sog/Chordin. Finally, Toll activation relies on ovarian patterning mechanisms with striking similarity to Drosophila. Our data suggest two surprising hypotheses: 1) that Toll's patterning function in Gryllus and Drosophila is the result of convergent evolution or 2) a Drosophila-like system arose early in insect evolution, and was extensively altered in multiple independent lineages.
Data availability
Raw reads from our sequencing are available from the NCBI SRA under accession PRJNA492804The Gryllus transcriptome is available from 10.6084/m9.figshare.14211062
Article and author information
Author details
Nathan James Kenny
Funding
University of Cologne (Postdoc grant)
- Matthias Pechmann
Deutsche Forschungsgemeinschaft (CRC 680)
- Yen-Ta Chen
Deutsche Forschungsgemeinschaft (CRC 680)
- Thomas Buchta
Deutsche Forschungsgemeinschaft (CRC 680)
- Thomas Buchta
Deutsche Forschungsgemeinschaft (CRC 680)
- Orhan Özüak
Deutsche Forschungsgemeinschaft (CRC 680)
- Jeremy A Lynch
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Patricia J Wittkopp, University of Michigan, United States
Version history
- Received: March 15, 2021
- Accepted: March 24, 2021
- Accepted Manuscript published: March 30, 2021 (version 1)
- Version of Record published: April 16, 2021 (version 2)
Copyright
© 2021, Pechmann 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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Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network
eLife 10:e68287.
https://doi.org/10.7554/eLife.68287
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