Ecdysone coordinates plastic growth with robust pattern in the developing wing

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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).

The following data sets were generated

(2020) Dataset for Nogueira Alves et al: Ecdysone coordinates plastic growth with robust pattern in the developing wing.
figshare.

https://doi.org/10.26180/13393676

Article and author information

Author details

André Nogueira Alves

School of Biological Sciences, Monash University, Melbourne, Australia

Competing interests
The authors declare that no competing interests exist.
Marisa Matheus Oliveira

Instituto Gulbenkian de Ciência, Oeiras, Portugal

Competing interests
The authors declare that no competing interests exist.
Takashi Koyama

Instituto Gulbenkian de Ciência, Oeiras, Portugal

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4203-114X
Alexander Shingleton

Department of Biological Sciences, University of Illinois at Chicago, Chicago, United States

For correspondence
ashingle@uic.edu

Competing interests
The authors declare that no competing interests exist.
Christen K Mirth

School of Biological Sciences, Monash University, Melbourne, Australia

For correspondence
christen.mirth@monash.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9765-4021

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.

Copyright

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.