Extensive and diverse patterns of cell death sculpt neural networks in insects

  1. Sinziana Pop
  2. Chin-Lin Chen
  3. Connor J Sproston
  4. Shu Kondo
  5. Pavan Ramdya
  6. Darren W Williams  Is a corresponding author
  1. King's College London, United Kingdom
  2. EPFL, Switzerland
  3. National Institute of Genetics, Japan

Abstract

Changes to the structure and function of neural networks are thought to underlie the evolutionary adaptation of animal behaviours. Among the many developmental phenomena that generate change programmed cell death appears to play a key role. We show that cell death occurs continuously throughout insect neurogenesis and happens soon after neurons are born. Mimicking an evolutionary role for increasing cell numbers, we artificially block programmed cell death in the medial neuroblast lineage in Drosophila melanogaster, which results in the production of 'undead' neurons with complex arborisations and distinct neurotransmitter identities. Activation of these 'undead' neurons and recordings of neural activity in behaving animals demonstrate that they are functional. Focusing on two dipterans which have lost flight during evolution we reveal that reductions in populations of flight interneurons are likely caused by increased cell death during development. Our findings suggest that the evolutionary modulation of death-based patterning could generate novel network configurations.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting figures.

Article and author information

Author details

  1. Sinziana Pop

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8811-8307
  2. Chin-Lin Chen

    School of Life Sciences, Brain Mind Institute and Interfaculty Institute of Bioengineering, Neuroengineering Laboratory, EPFL, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Connor J Sproston

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Shu Kondo

    Genetic Strains Research Center, National Institute of Genetics, Mishima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Pavan Ramdya

    School of Life Sciences, Brain Mind Institute and Interfaculty Institute of Bioengineering, Neuroengineering Laboratory, EPFL, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0699-5825
  6. Darren W Williams

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    For correspondence
    darren.williams@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5917-4935

Funding

Biotechnology and Biological Sciences Research Council (BB/P025552/1)

  • Darren W Williams

Biotechnology and Biological Sciences Research Council (BB/L022672/1)

  • Darren W Williams

SNSF (175667)

  • Pavan Ramdya

Eccellenza (181239)

  • Pavan Ramdya

R'Equip (177102)

  • Pavan Ramdya

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: June 2, 2020
  2. Accepted: September 6, 2020
  3. Accepted Manuscript published: September 7, 2020 (version 1)
  4. Version of Record published: October 5, 2020 (version 2)
  5. Version of Record updated: October 6, 2020 (version 3)

Copyright

© 2020, Pop 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. Sinziana Pop
  2. Chin-Lin Chen
  3. Connor J Sproston
  4. Shu Kondo
  5. Pavan Ramdya
  6. Darren W Williams
(2020)
Extensive and diverse patterns of cell death sculpt neural networks in insects
eLife 9:e59566.
https://doi.org/10.7554/eLife.59566

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