Adaptation of Drosophila larva foraging in response to changes in food resources

  1. Marina E Wosniack
  2. Dylan Festa
  3. Nan Hu
  4. Julijana Gjorgjieva  Is a corresponding author
  5. Jimena Berni  Is a corresponding author
  1. Max Planck Institute for Brain Research, Germany
  2. Technical University of Munich, Germany
  3. University of Cambridge, United Kingdom
  4. University of Sussex, United Kingdom

Abstract

All animals face the challenge of finding nutritious resources in a changing environment. To maximize life-time fitness, the exploratory behavior has to be flexible, but which behavioral elements adapt and what triggers those changes remain elusive. Using experiments and modeling, we characterized extensively how Drosophila larvae foraging adapts to different food quality and distribution and how the foraging genetic background influences this adaptation. Our work shows that different food properties modulated specific motor programs. Food quality controls the travelled distance by modulating crawling speed and frequency of pauses and turns. Food distribution, and in particular the food-no food interphase, controls turning behavior, stimulating turns towards the food when reaching the patch border and increasing the proportion of time spent within patches of food. Finally, the polymorphism in the foraging gene (rover-sitter) of the larvae adjusts the magnitude of the behavioral response to different food conditions. This study defines several levels of control of foraging and provides the basis for the systematic identification of the neuronal circuits and mechanisms controlling each behavioral response.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files 1 and 2; Source Data files have been provided formal experimental data: Figures 1, 3, 4 and 6.

Article and author information

Author details

  1. Marina E Wosniack

    Computation in Neural Circuits Group, Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2175-9713
  2. Dylan Festa

    School of Life Sciences, Technical University of Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Nan Hu

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Julijana Gjorgjieva

    Computation in Neural Circuits Group, Max Planck Institute for Brain Research, Frankfurt, Germany
    For correspondence
    gjorgjieva@brain.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7118-4079
  5. Jimena Berni

    Brighton and Sussex Medical School,, University of Sussex, Brighton, United Kingdom
    For correspondence
    j.berni@sussex.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5068-1372

Funding

Royal Society (105568/Z/14/Z)

  • Jimena Berni

Wellcome Trust (105568/Z/14/Z)

  • Jimena Berni

Max-Planck-Gesellschaft

  • Marina E Wosniack
  • Julijana Gjorgjieva

Alexander von Humboldt-Stiftung

  • Marina E Wosniack

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

Copyright

© 2022, Wosniack 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.

Metrics

  • 1,879
    views
  • 256
    downloads
  • 9
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Marina E Wosniack
  2. Dylan Festa
  3. Nan Hu
  4. Julijana Gjorgjieva
  5. Jimena Berni
(2022)
Adaptation of Drosophila larva foraging in response to changes in food resources
eLife 11:e75826.
https://doi.org/10.7554/eLife.75826

Share this article

https://doi.org/10.7554/eLife.75826

Further reading

    1. Neuroscience
    Ulrike Pech, Jasper Janssens ... Patrik Verstreken
    Research Article

    The classical diagnosis of Parkinsonism is based on motor symptoms that are the consequence of nigrostriatal pathway dysfunction and reduced dopaminergic output. However, a decade prior to the emergence of motor issues, patients frequently experience non-motor symptoms, such as a reduced sense of smell (hyposmia). The cellular and molecular bases for these early defects remain enigmatic. To explore this, we developed a new collection of five fruit fly models of familial Parkinsonism and conducted single-cell RNA sequencing on young brains of these models. Interestingly, cholinergic projection neurons are the most vulnerable cells, and genes associated with presynaptic function are the most deregulated. Additional single nucleus sequencing of three specific brain regions of Parkinson’s disease patients confirms these findings. Indeed, the disturbances lead to early synaptic dysfunction, notably affecting cholinergic olfactory projection neurons crucial for olfactory function in flies. Correcting these defects specifically in olfactory cholinergic interneurons in flies or inducing cholinergic signaling in Parkinson mutant human induced dopaminergic neurons in vitro using nicotine, both rescue age-dependent dopaminergic neuron decline. Hence, our research uncovers that one of the earliest indicators of disease in five different models of familial Parkinsonism is synaptic dysfunction in higher-order cholinergic projection neurons and this contributes to the development of hyposmia. Furthermore, the shared pathways of synaptic failure in these cholinergic neurons ultimately contribute to dopaminergic dysfunction later in life.

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.