Shifting balances in the weighting of sensory modalities are predicted by divergence in brain morphology in incipient species of Heliconius butterflies

Abstract

Integrating and weighting sensory perception across modalities is crucial to how animals adapt to their environment. Divergence in brain structure is often in sensory processing regions, suggesting that investment reflects ecological needs. Here, we use two parapatric closely related species, Heliconius erato cyrbia and Heliconius himera, to test the hypothesis that divergence in sensory brain regions affects foraging decisions. These butterflies are isolated across an ecological gradient, which is linked to differences in brain morphology, with H. e. cyrbia investing more in visual centres and H. himera investing in olfactory centres. Here, we demonstrate that these two species vary in how they associate visual and olfactory cues with positive food rewards. We found that when individuals were trained on paired olfactory and visual stimuli, then presented with these stimuli in conflict, they showed distinct behavioural responses. Heliconius himera was more likely to favour positive olfactory cues than H. e. cyrbia, which favoured visual cues regardless of the paired stimulus. This suggests that these species have diverged in the emphasis placed on these different sensory domains during foraging, consistent with observed differences in brain morphology. This result strengthens evidence that speciation initiated by local adaptation is partly facilitated by changes in the neural basis of key behavioural functions.