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

Antoine Couto; Fletcher J Young; Daniele Atzeni; Simon Marty; Lina Melo-Flórez; Laura Hebberecht Lopez; Monica Monllor; Francesco Cicconardi; Chris R Neal; W. Owen McMillan; Stephen H Montgomery

doi:10.1038/s41467-023-39618-8

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

Antoine Couto, Fletcher J Young, Daniele Atzeni, Simon Marty, Lina Melo-Flórez, Laura Hebberecht Lopez, Monica Monllor, Francesco Cicconardi, Chris R Neal, W. Owen McMillan, Stephen H Montgomery^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

20 Citations (Scopus)

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.

Original language	English
Article number	4024
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-39618-8
Publication status	Published - 7 Jul 2023

Bibliographical note

Funding Information:
We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estación Científica Yasuní, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.).

Funding Information:
We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estación Científica Yasuní, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.).

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© 2023, The Author(s).

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Couto, A., Young, F. J., Atzeni, D., Marty, S., Melo-Flórez, L., Hebberecht Lopez, L., Monllor, M., Cicconardi, F., Neal, C. R., McMillan, W. O., & Montgomery, S. H. (2023). Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies. Nature Communications, 14(1), Article 4024. https://doi.org/10.1038/s41467-023-39618-8

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title = "Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies",

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. ",

author = "Antoine Couto and Young, {Fletcher J} and Daniele Atzeni and Simon Marty and Lina Melo-Fl{\'o}rez and {Hebberecht Lopez}, Laura and Monica Monllor and Francesco Cicconardi and Neal, {Chris R} and McMillan, {W. Owen} and Montgomery, {Stephen H}",

note = "Funding Information: We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estaci{\'o}n Cient{\'i}fica Yasun{\'i}, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.). Funding Information: We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estaci{\'o}n Cient{\'i}fica Yasun{\'i}, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.). Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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AU - Couto, Antoine

AU - Young, Fletcher J

AU - Atzeni, Daniele

AU - Marty, Simon

AU - Melo-Flórez, Lina

AU - Hebberecht Lopez, Laura

AU - Monllor, Monica

AU - Cicconardi, Francesco

AU - Neal, Chris R

AU - McMillan, W. Owen

AU - Montgomery, Stephen H

N1 - Funding Information: We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estación Científica Yasuní, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.). Funding Information: We are very grateful to the environmental ministries of Costa Rica, Panama, French Guiana, Ecuador and Peru for permission to collect and export samples. We thank the Organization for Tropical Studies, Le Leona Eco Lodge, the Smithsonian Tropical Research Institute, the Estación Científica Yasuní, PUCE, F. Ramirez Castro, Neil Rosser, Ronald Mori Pezo the Dasmahapatra group, and the broader Heliconius research community for support in the field and for discussions, and to Swidbert Ott for advice and encouragement early on in this project. We are grateful to the Wolfson Bioimaging Centre, University of Bristol, the University College London Confocal Imaging facility, and Matt Wayland and the Dept. of Zoology Imaging Facility, University of Cambridge, for imaging assistance. This work was supported by a Royal Commission for the Great Exhibition Research Fellowship (S.H.M.), a Leverhulme Trust Early Career Fellowship (S.H.M.), a Short-term STRI Fellowship (S.H.M.), a Royal Society Research Grant (S.H.M.), a Newton Trust INT Research Grant (S.H.M.), a NERC Independent Research Fellowship NE/N014936/1 (S.H.M.), an ERC Starter Grant 758508 (S.H.M.) and a PhD Studentship from Trinity College, Cambridge (F.J.Y.). Publisher Copyright: © 2023, The Author(s).

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N2 - 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.

AB - 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.

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

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Neurological adaptation and ecological specialisation

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

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Bibliographical note

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Neurological adaptation and ecological specialisation

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