Distinct evolutionary trajectories of two integration centres, the central complex and mushroom bodies, across...

Neural circuits evolved to produce variable cognitive processes through adaptive mechanisms operating within a background of developmental and functional constraints. Understanding how this conflict is resolved requires a comparative framework encapsulating clear behavioural variation. We leverage Heliconiini butterflies to examine how selection shaped the evolution of the central complex and mushroom bodies, two insect integration centres involved in navigation. The evolution of systematic spatial foraging in Heliconius has led to changes in brain morphology and learning and memory profiles over a short evolutionary timescale. Here, we show that in contrast to massively expanded mushroom bodies, the central complex is strongly conserved in size and general architecture. However, we identify divergences in the expression of a neuropeptide, Allatostatin A, in the noduli, and in the numbers of GABA-ergic ring neurons and their branching in the fan-shaped body, which are essential members of the anterior compass pathway. These differences are rare examples of divergence inside the central complex network matching expectations of where evolutionary adaptability might occur. We conclude that due to the contrasting volumetric conservation of the central complex, and the massive differences in the mushroom bodies, their circuit logics must determine distinct responses to selection associated with divergent foraging behaviours.