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Evolution of connectivity architecture in the Drosophila mushroom body

Author

Listed:
  • Kaitlyn Elizabeth Ellis

    (University of Utah)

  • Sven Bervoets

    (University of Utah)

  • Hayley Smihula

    (University of Utah)

  • Ishani Ganguly

    (Center for Theoretical Neuroscience)

  • Eva Vigato

    (University of Utah)

  • Thomas O. Auer

    (University of Lausanne
    University of Fribourg)

  • Richard Benton

    (University of Lausanne)

  • Ashok Litwin-Kumar

    (Center for Theoretical Neuroscience)

  • Sophie Jeanne Cécile Caron

    (University of Utah)

Abstract

Brain evolution has primarily been studied at the macroscopic level by comparing the relative size of homologous brain centers between species. How neuronal circuits change at the cellular level over evolutionary time remains largely unanswered. Here, using a phylogenetically informed framework, we compare the olfactory circuits of three closely related Drosophila species that differ in their chemical ecology: the generalists Drosophila melanogaster and Drosophila simulans and Drosophila sechellia that specializes on ripe noni fruit. We examine a central part of the olfactory circuit that, to our knowledge, has not been investigated in these species—the connections between projection neurons and the Kenyon cells of the mushroom body—and identify species-specific connectivity patterns. We found that neurons encoding food odors connect more frequently with Kenyon cells, giving rise to species-specific biases in connectivity. These species-specific connectivity differences reflect two distinct neuronal phenotypes: in the number of projection neurons or in the number of presynaptic boutons formed by individual projection neurons. Finally, behavioral analyses suggest that such increased connectivity enhances learning performance in an associative task. Our study shows how fine-grained aspects of connectivity architecture in an associative brain center can change during evolution to reflect the chemical ecology of a species.

Suggested Citation

  • Kaitlyn Elizabeth Ellis & Sven Bervoets & Hayley Smihula & Ishani Ganguly & Eva Vigato & Thomas O. Auer & Richard Benton & Ashok Litwin-Kumar & Sophie Jeanne Cécile Caron, 2024. "Evolution of connectivity architecture in the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48839-4
    DOI: 10.1038/s41467-024-48839-4
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    References listed on IDEAS

    as
    1. Sophie J. C. Caron & Vanessa Ruta & L. F. Abbott & Richard Axel, 2013. "Random convergence of olfactory inputs in the Drosophila mushroom body," Nature, Nature, vol. 497(7447), pages 113-117, May.
    2. Thomas O. Auer & Mohammed A. Khallaf & Ana F. Silbering & Giovanna Zappia & Kaitlyn Ellis & Raquel Álvarez-Ocaña & J. Roman Arguello & Bill S. Hansson & Gregory S. X. E. Jefferis & Sophie J. C. Caron , 2020. "Olfactory receptor and circuit evolution promote host specialization," Nature, Nature, vol. 579(7799), pages 402-408, March.
    3. Vanessa Ruta & Sandeep Robert Datta & Maria Luisa Vasconcelos & Jessica Freeland & Loren L. Looger & Richard Axel, 2010. "A dimorphic pheromone circuit in Drosophila from sensory input to descending output," Nature, Nature, vol. 468(7324), pages 686-690, December.
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    1. Suguru Takagi & Gizem Sancer & Liliane Abuin & S. David Stupski & J. Roman Arguello & Lucia L. Prieto-Godino & David L. Stern & Steeve Cruchet & Raquel Álvarez-Ocaña & Carl F. R. Wienecke & Floris Bre, 2024. "Olfactory sensory neuron population expansions influence projection neuron adaptation and enhance odour tracking," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Ishani Ganguly & Emily L. Heckman & Ashok Litwin-Kumar & E. Josephine Clowney & Rudy Behnia, 2024. "Diversity of visual inputs to Kenyon cells of the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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