Constitutive activation of cellular immunity underlies the evolution of resistance to infection in Drosophila

  1. Alexandre B. Leitão  Is a corresponding author
  2. Ramesh Arunkumar
  3. Jonathan P Day
  4. Emma M Geldman
  5. Ismaël Morin-Poulard
  6. Michele Crozatier
  7. Francis M Jiggins  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. Université de Toulouse, France

Abstract

Organisms rely on inducible and constitutive immune defences to combat infection. Constitutive immunity enables a rapid response to infection but may carry a cost for uninfected individuals, leading to the prediction that it will be favoured when infection rates are high. When we exposed populations of Drosophila melanogaster to intense parasitism by the parasitoid wasp Leptopilina boulardi, they evolved resistance by developing a more reactive cellular immune response. Using single-cell RNA sequencing, we found that immune-inducible genes had become constitutively upregulated. This was the result of resistant larvae differentiating precursors of specialized immune cells called lamellocytes that were previously only produced after infection. Therefore, populations evolved resistance by genetically hard-wiring the first steps of an induced immune response to become constitutive.

Data availability

Unprocessed single cell sequence reads were deposited in the Sequence Read Archive (accession: SRP256887, Bioproject: PRJNA625925). Cell count matrices for all detected genes, cluster identities and processed scRNA-seq results were deposited into Gene Expression Omnibus (accession: GSE148826). The R script used to analyze the scRNA-seq data is available on Github (Repository: dmel_scRNA_hemocyte).

The following data sets were generated

Article and author information

Author details

  1. Alexandre B. Leitão

    Genetics Department, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ac2016@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. Ramesh Arunkumar

    Department of Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Jonathan P Day

    Department of Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Emma M Geldman

    Department of Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Ismaël Morin-Poulard

    Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Michele Crozatier

    Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI),, Université de Toulouse, TOULOUSE, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9911-462X
  7. Francis M Jiggins

    Department of Genetics, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    fmj1001@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7470-8157

Funding

Natural Environment Research Council (NE/P00184X/1)

  • Alexandre B. Leitão
  • Francis M Jiggins

European Molecular Biology Organization (ALT-1556)

  • Alexandre B. Leitão

Natural Sciences and Engineering Research Council of Canada (PDF-516634-2018)

  • Ramesh Arunkumar

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

Reviewing Editor

  1. Bruno Lemaitre, École Polytechnique Fédérale de Lausanne, Switzerland

Publication history

  1. Received: May 21, 2020
  2. Accepted: December 23, 2020
  3. Accepted Manuscript published: December 24, 2020 (version 1)
  4. Version of Record published: January 5, 2021 (version 2)

Copyright

© 2020, Leitão 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. Alexandre B. Leitão
  2. Ramesh Arunkumar
  3. Jonathan P Day
  4. Emma M Geldman
  5. Ismaël Morin-Poulard
  6. Michele Crozatier
  7. Francis M Jiggins
(2020)
Constitutive activation of cellular immunity underlies the evolution of resistance to infection in Drosophila
eLife 9:e59095.
https://doi.org/10.7554/eLife.59095

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