Plasticity and genetic effects contribute to different axes of neural divergence in a community of mimetic Heliconius butterflies

Laura Hebberecht Lopez, Benito Wainwright, Charlotte Thompson, Simon Kershenbaum, W. Owen McMillan, Stephen H Montgomery*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

6 Citations (Scopus)

Abstract

Changes in ecological preference, often driven by spatial and temporal variation in resource distribution, can expose populations to environments with divergent information content. This can lead to adaptive changes in the degree to which individuals invest in sensory systems and downstream processes, to optimize behavioural performance in different contexts. At the same time, environmental conditions can produce plastic responses in nervous system development and maturation, providing an alternative route to integrating neural and ecological variation. Here, we explore how these two processes play out across a community of Heliconius butterflies. Heliconius communities exhibit multiple Mullerian mimicry rings, associated with habitat partitioning across environmental gradients. These environmental differences have previously been linked to heritable divergence in brain morphology in parapatric species pairs. They also exhibit a unique dietary adaptation, known as pollen feeding, that relies heavily on learning foraging routes, or trap-lines, between resources, which implies an important environmental influence on behavioural development. By comparing brain morphology across 133 wild-caught and insectary reared individuals from seven Heliconius species, we find strong evidence for interspecific variation in patterns of neural investment. These largely fall into two distinct patterns of variation; first, we find consistent patterns of divergence in the size of visual brain components across both wild and insectary reared individuals, suggesting genetically encoded divergence in the visual pathway. Second, we find interspecific differences in mushroom body size, a central component of learning and memory systems, but only among wild caught individuals. The lack of this effect in common-garden individuals suggests an extensive role for developmental plasticity in interspecific variation in the wild. Finally, we illustrate the impact of relatively small-scale spatial effects on mushroom body plasticity by performing experiments altering the cage size and structure experienced by individual H. hecale. Our data provide a comprehensive survey of community level variation in brain structure, and demonstrate that genetic effects and developmental plasticity contribute to different axes of interspecific neural variation.
Original languageEnglish
Pages (from-to)1116-1132
Number of pages17
JournalJournal of Evolutionary Biology
Volume36
Issue number8
Early online date21 Jun 2023
DOIs
Publication statusPublished - 8 Aug 2023

Bibliographical note

Funding Information:
We are indebted to the environmental agencies in Panama, for permission to carry out this work. We thank Adriana Tapia, Moises Abanto, Oscar Paneso, Cruz Batista Saez, Chi-Yun Kuo, Morgan Oberweiser, the McMillan, Jiggins and EBaB labs, and STRI for support at the Gamboa insectaries, Panama. We also thank the University College London Confocal Imaging facility, and Matt Wayland and the Department of Zoology Imaging Facility, University of Cambridge, for assistance. This work was funded by a Royal Commission for the Great Exhibition Research Fellowship, a Leverhulme Trust Early Career Fellowship, a short-term STRI Fellowship, British Ecological Society Research Grant (3066), an ERC Starter Grant (758508) and a NERC IRF (NE/N014936/1) to SHM, and NERC DTP Scholarship to JBW.

Funding Information:
We are indebted to the environmental agencies in Panama, for permission to carry out this work. We thank Adriana Tapia, Moises Abanto, Oscar Paneso, Cruz Batista Saez, Chi‐Yun Kuo, Morgan Oberweiser, the McMillan, Jiggins and EBaB labs, and STRI for support at the Gamboa insectaries, Panama. We also thank the University College London Confocal Imaging facility, and Matt Wayland and the Department of Zoology Imaging Facility, University of Cambridge, for assistance. This work was funded by a Royal Commission for the Great Exhibition Research Fellowship, a Leverhulme Trust Early Career Fellowship, a short‐term STRI Fellowship, British Ecological Society Research Grant (3066), an ERC Starter Grant (758508) and a NERC IRF (NE/N014936/1) to SHM, and NERC DTP Scholarship to JBW.

Publisher Copyright:
© 2023 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.

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