Global Constraints within the Developmental Program of the Drosophila Wing

  1. Vasyl Alba
  2. James Carthew
  3. Richard W Carthew
  4. Madhav Mani  Is a corresponding author
  1. Northwestern University, United States

Abstract

Organismal development is a complex process, involving a vast number of molecular constituents interacting on multiple spatio-temporal scales in the formation of intricate body structures. Despite this complexity, development is remarkably reproducible and displays tolerance to both genetic and environmental perturbations. This robustness implies the existence of hidden simplicities in developmental programs. Here, using the Drosophila wing as a model system, we develop a new quantitative strategy that enables a robust description of biologically salient phenotypic variation. Analyzing natural phenotypic variation across a highly outbred population, and variation generated by weak perturbations in genetic and environmental conditions, we observe a highly constrained set of wing phenotypes. Remarkably, the phenotypic variants can be described by a single integrated mode that corresponds to a non-intuitive combination of structural variations across the wing. This work demonstrates the presence of constraints that funnel environmental inputs and genetic variation into phenotypes stretched along a single axis in morphological space. Our results provide quantitative insights into the nature of robustness in complex forms while yet accommodating the potential for evolutionary variations. Methodologically, we introduce a general strategy for finding such invariances in other developmental contexts.

Data availability

Data will be made publicly available at Mani, Madhav, 2021, "Imaging data from "Global Constraints within the Developmental Program of the Drosophila Wing"", https://doi.org/10.7910/DVN/UFGJFB, Harvard Dataverse, V1

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Vasyl Alba

    Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. James Carthew

    Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Richard W Carthew

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0343-0156
  4. Madhav Mani

    Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, United States
    For correspondence
    madhav.mani@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5812-4167

Funding

National Science Foundation (DMS-1547394)

  • James Carthew

National Science Foundation (1764421)

  • Richard W Carthew
  • Madhav Mani

Simons Foundation (597491)

  • Vasyl Alba
  • Richard W Carthew
  • Madhav Mani

Simons Foundation (Investigator - MMLS)

  • Madhav Mani

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Danelle Devenport, Princeton University, United States

Publication history

  1. Received: January 21, 2021
  2. Accepted: June 25, 2021
  3. Accepted Manuscript published: June 28, 2021 (version 1)
  4. Version of Record published: July 5, 2021 (version 2)

Copyright

© 2021, Alba 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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  1. Vasyl Alba
  2. James Carthew
  3. Richard W Carthew
  4. Madhav Mani
(2021)
Global Constraints within the Developmental Program of the Drosophila Wing
eLife 10:e66750.
https://doi.org/10.7554/eLife.66750

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