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Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies

Author

Listed:
  • Antoine Couto

    (University of Bristol
    University of Cambridge)

  • Fletcher J. Young

    (University of Bristol
    University of Cambridge
    Smithsonian Tropical Research Institute)

  • Daniele Atzeni

    (University of Bristol
    University of Trieste)

  • Simon Marty

    (University of Cambridge
    Université Claude Bernard Lyon 1, Université de Lyon)

  • Lina Melo‐Flórez

    (Smithsonian Tropical Research Institute)

  • Laura Hebberecht

    (University of Bristol
    University of Cambridge
    Smithsonian Tropical Research Institute)

  • Monica Monllor

    (Smithsonian Tropical Research Institute)

  • Chris Neal

    (University of Bristol)

  • Francesco Cicconardi

    (University of Bristol)

  • W. Owen McMillan

    (Smithsonian Tropical Research Institute)

  • Stephen H. Montgomery

    (University of Bristol
    Smithsonian Tropical Research Institute)

Abstract

Changes in the abundance and diversity of neural cell types, and their connectivity, shape brain composition and provide the substrate for behavioral evolution. Although investment in sensory brain regions is understood to be largely driven by the relative ecological importance of particular sensory modalities, how selective pressures impact the elaboration of integrative brain centers has been more difficult to pinpoint. Here, we provide evidence of extensive, mosaic expansion of an integration brain center among closely related species, which is not explained by changes in sites of primary sensory input. By building new datasets of neural traits among a tribe of diverse Neotropical butterflies, the Heliconiini, we detected several major evolutionary expansions of the mushroom bodies, central brain structures pivotal for insect learning and memory. The genus Heliconius, which exhibits a unique dietary innovation, pollen-feeding, and derived foraging behaviors reliant on spatial memory, shows the most extreme enlargement. This expansion is primarily associated with increased visual processing areas and coincides with increased precision of visual processing, and enhanced long term memory. These results demonstrate that selection for behavioral innovation and enhanced cognitive ability occurred through expansion and localized specialization in integrative brain centers.

Suggested Citation

  • Antoine Couto & Fletcher J. Young & Daniele Atzeni & Simon Marty & Lina Melo‐Flórez & Laura Hebberecht & Monica Monllor & Chris Neal & Francesco Cicconardi & W. Owen McMillan & Stephen H. Montgomery, 2023. "Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39618-8
    DOI: 10.1038/s41467-023-39618-8
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    References listed on IDEAS

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    1. Chris Venditti & Andrew Meade & Mark Pagel, 2011. "Multiple routes to mammalian diversity," Nature, Nature, vol. 479(7373), pages 393-396, November.
    2. Tyler A. Ofstad & Charles S. Zuker & Michael B. Reiser, 2011. "Visual place learning in Drosophila melanogaster," Nature, Nature, vol. 474(7350), pages 204-207, June.
    3. Robert A. Barton & Paul H. Harvey, 2000. "Mosaic evolution of brain structure in mammals," Nature, Nature, vol. 405(6790), pages 1055-1058, June.
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    Cited by:

    1. 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.
    2. Francesco Cicconardi & Edoardo Milanetti & Erika C. Pinheiro de Castro & Anyi Mazo-Vargas & Steven M. Van Belleghem & Angelo Alberto Ruggieri & Pasi Rastas & Joseph Hanly & Elizabeth Evans & Chris D. , 2023. "Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies," Nature Communications, Nature, vol. 14(1), pages 1-24, December.

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