Conservation of sensory pathways implies a localised change in the mushroom bodies is associated with cognitive evolution in Heliconius butterflies

Abstract

Acquisition of novel behaviour is reflected in changes in sensory investment or integration, but the exact nature of these changes is often unclear. Within the Neotropical butterfly tribe, Heliconiini, the genus Heliconius possess 4-fold larger mushroom bodies, an insect learning and memory centre, than closely related Heliconiini. Mushroom body expansion in Heliconius co-occurred with a dietary innovation, and is associated with systematic spatial foraging and extended lifespans. Heliconiini therefore offer an attractive system for studying how behavioural evolution is facilitated by changes in neural systems. Heliconius foraging relies on visual scene memories and, indeed, Heliconius have more stable visual long-term memory, and evidence of visual specialisation in the mushroom bodies. Here, we explore how vision-specific neuroanatomical and behavioural enhancement in Heliconius impacts sensory pathways upstream of the mushroom bodies by assessing investment across the eyes, sensory structures and projection pathways. Despite evidence of refinement in visually-based behaviour, we found no increased investment in visual structures, brain areas or pathways. This suggests that the rapid expansion of the Heliconius mushroom body occurred in a context of conserved detection and processing of visual cues, and that a localised shift within integrative brain centres facilitated the evolution of Heliconius novel behaviours.