Mosaic evolution of a learning and memory circuit in Heliconiini butterflies.

Abstract

How do neural circuits accommodate changes that produce cognitive variation? We explore this question by analyzing the evolutionary dynamics of an insect learning and memory circuit centered within the mushroom body. Mushroom bodies are composed of a conserved wiring logic, mainly consisting of Kenyon cells, dopaminergic neurons, and mushroom body output neurons. Despite this conserved makeup, there is huge diversity in mushroom body size and shape across insects. However, empirical data on how evolution modifies the function and architecture of this circuit are largely lacking. To address this, we leverage the recent radiation of a Neotropical tribe of butterflies, the Heliconiini (Nymphalidae), which show extensive variation in mushroom body size over comparatively short phylogenetic timescales, linked to specific changes in foraging ecology, life history, and cognition. To understand how such an extensive increase in size is accommodated through changes in lobe circuit architecture, we combined immunostainings of structural markers, neurotransmitters, and neural injections to generate new, quantitative anatomies of the Nymphalid mushroom body lobe. Our comparative analyses across Heliconiini demonstrate that some Kenyon cell sub-populations expanded at higher rates than others in Heliconius and identify an additional increase in GABA-ergic feedback neurons, which are essential for non-elemental learning and sparse coding. Taken together, our results demonstrate mosaic evolution of functionally related neural systems and cell types and identify that evolutionary malleability in an architecturally conserved parallel circuit guides adaptation in cognitive ability.