Ecdysone coordinates plastic growth with robust pattern in the developing wing
- Monash University, Australia
- Instituto Gulbenkian de Ciência, Portugal
- University of Illinois at Chicago, United States
Abstract
Animals develop in unpredictable, variable environments. In response to environmental change some aspects of development adjust to generate plastic phenotypes. Other aspects of development, however, are buffered against environmental change to produce robust phenotypes. How organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we demonstrate that the steroid hormone ecdysone coordinates both plasticity of organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster. Using fed and starved larvae that lack prothoracic glands, which synthesise ecdysone, we show that nutrition regulates growth both via ecdysone and via an ecdysone-independent mechanism, while nutrition regulates patterning only via ecdysone. We then demonstrate that growth shows a graded response to ecdysone concentration, while patterning shows a threshold response. Collectively, these data support a model where nutritionally-regulated ecdysone fluctuations confer plasticity by regulating disc growth in response to basal ecdysone levels, and confers robustness by initiating patterning only once ecdysone peaks exceeds a threshold concentration. This could represent a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change.
Data availability
All data and R scripts for analysis have been deposited on Figshare (DOI: 10.26180/13393676).
Article and author information
Author details
Funding
Australian Research Council (FT170100259)
- Christen K Mirth
National Science Foundation (IOS-0919855)
- Alexander Shingleton
National Science Foundation (IOS-1557638)
- Alexander Shingleton
National Science Foundation (IOS-1952385)
- Alexander Shingleton
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Lynn M. Riddiford
Version history
- Preprint posted: December 16, 2020 (view preprint)
- Received: July 30, 2021
- Accepted: March 7, 2022
- Accepted Manuscript published: March 9, 2022 (version 1)
- Version of Record published: March 24, 2022 (version 2)
Copyright
© 2022, Nogueira Alves 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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Ecdysone coordinates plastic growth with robust pattern in the developing wing
eLife 11:e72666.
https://doi.org/10.7554/eLife.72666
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