Repeated evolution of reduced visual investment at the onset of ecological speciation in high-altitude Heliconius butterflies

Colonization of new habitats is typically followed by divergent selection acting on traits that are immediately important for fitness. For example, differences between sensory environments are often associated with variation in sensory traits critical for navigation and foraging. However, the extent to which the initial response to novel sensory conditions is mediated by phenotypic plasticity, and the contribution of sensory or neural adaptation to early species divergence remains unclear. We took advantage of repeated cases of speciation in Heliconius butterflies with independent allopatric distributions in the west of the Colombian and Ecuadorian Andes. Using volumetric brain measurements, we analyzed patterns of investment in primary sensory processing areas of the brain across different localities and habitats. We find that a higher altitude species, Heliconius chestertonii, differs in levels of investment in visual and olfactory brain components compared with its lower altitude relative H. erato venus, mainly attributable to broad-sense heritable variation as inferred from comparisons between wild and common-garden-reared individuals. We provide evidence that this variation is consistent with divergent selection, and compare these shifts with those reported for another high-altitude species, H. himera, and its parapatric lowland counterpart, H. erato cyrbia, to demonstrate parallel reductions in the size of specific optic lobe neuropils. Conversely, for the antennal lobe, we detected different trait shifts in H. himera and H. chestertonii relative to their lowland H. erato neighbors. Overall, our findings add weight to the adaptive potential of neuroanatomical divergence related to sensory processing during early species formation.