Heliconiini butterflies as a case study in evolutionary cognitive ecology: behavioural innovation and mushroom body expansion

Abstract

AbstractThe evolutionary relationships between ecology, cognition, and neurobiology remain elusive, despite important contributions from functional studies and comparative analyses. Recently, Heliconius butterflies and their Heliconiini allies have emerged as a promising system for investigating the evolution and ecology of cognition. In Heliconius, regions of the brain involved in learning and memory, called the mushroom bodies, have quadrupled in size and contain up to 8 times more neurons than closely related genera. This expansion, largely driven by increased dedication to processing visual input, occurred relatively recently (~12–18 Ma) and coincides with the evolution of a novel foraging behaviour — trapline foraging between pollen resources, which provide an adult source of amino acids. Behavioural experiments show that, relative to other Heliconiini, Heliconius exhibit superior visual long-term memory and non-elemental learning, behaviours which have putative relevance for visual learning during traplining, while exhibiting no differences in shape learning or reversal learning. These cognitive differences are also associated with changes in the plastic response of the mushroom body to learning and experience. Heliconius thus constitute a clear example of a suite of neural adaptations that coincides with a novel behaviour reliant on distinct cognitive shifts. We highlight the Heliconiini as a well-positioned, developing case study in cognitive ecology and evolution, where there is the possibility of synthesising comparative neuroanatomical, developmental and behavioural data with extensive genomic resources. This would provide a rich dataset linking genes, brains, behaviour, and ecology, and offer key insights into the mechanisms and selective pressures shaping the evolution of interspecific cognitive variation.