Coordination of Wing and Whole-Body Development at Developmental Milestones Ensures Robustness against Environmental and Physiological Perturbations
Marisa M. Oliveira, Alexander W. Shingleton, Christen K. Mirth mail
Published: June 19, 2014DOI: 10.1371/journal.pgen.1004408
Development produces correctly patterned tissues under a wide range of conditions that alter the rate of development in the whole body. We propose two hypotheses through which tissue patterning could be coordinated with whole-body development to generate this robustness. Our first hypothesis states that tissue patterning is tightly coordinated with whole-body development over time. The second hypothesis is that tissue patterning aligns at developmental milestones. To distinguish between our two hypotheses, we developed a staging scheme for the wing imaginal discs of Drosophila larvae using the expression of canonical patterning genes, linking our scheme to three whole-body developmental events: moulting, larval wandering and pupariation. We used our scheme to explore how the progression of pattern changes when developmental time is altered either by changing temperature or by altering the timing of hormone synthesis that drives developmental progression. We found the expression pattern in the wing disc always aligned at moulting and pupariation, indicating that these key developmental events represent milestones. Between these milestones, the progression of pattern showed greater variability in response to changes in temperature and alterations in physiology. Furthermore, our data showed that discs from wandering larvae showed greater variability in patterning stage. Thus for wing disc patterning, wandering does not appear to be a developmental milestone. Our findings reveal that tissue patterning remains robust against environmental and physiological perturbations by aligning at developmental milestones. Furthermore, our work provides an important glimpse into how the development of individual tissues is coordinated with the body as a whole.
Between distantly related species, development converges at common morphological and genetic stages, called developmental milestones, to ensure the establishment of a basic body plan. Beyond these milestones greater variability in developmental processes builds species-specific form. We reasoned that developmental milestones might also act within a species to achieve robustness against environmental or physiological perturbation. To address this, we first developed a staging scheme for the progression of pattern in the wing disc across developmental time. We then explored how perturbing environmental or physiological stimuli known to alter the rate of development affected the progression of pattern in the wing disc. We found two developmental milestones, the moult to the third instar and pupariation, where wing disc patterning aligned with the development of the whole body. This suggests that robustness against environmental and physiological conditions is achieved by coordinating tissue with whole-body development at developmental milestones.
Citation: Oliveira MM, Shingleton AW, Mirth CK (2014) Coordination of Wing and Whole-Body Development at Developmental Milestones Ensures Robustness against Environmental and Physiological Perturbations.
PLoS Genet 10(6): e1004408. doi:10.1371/journal.pgen.1004408
Editor: Marc Robinson-Rechavi, University of Lausanne, Switzerland
Received: January 7, 2014; Accepted: April 14, 2014; Published: June 19, 2014
Copyright: © 2014 Oliveira et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: MMO is supported by a doctoral fellowship from the Fundação para a Ciência e a Tecnologia (SFRH/BD/51181/2010) and by Fundação Calouste Gulbenkian. This work was funded by the Fundação Calouste Gulbenkian to CKM and by the National Science Foundation (IOS-0845847 and IOS-0919855) to AWS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
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