Adaptive divergence in the eyes ofHeliconiusbutterflies likely contributes to pre- and post-mating isolation

Abstract

AbstractWhen populations experience different sensory conditions, natural selection may favor whole sensory system divergence, from the peripheral structures to the brain. We characterized the outer eye morphology of sympatricHeliconiusspecies from different forest types, and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama,Heliconius cydnooccurs in closed forests, whereasHeliconius melpomeneresides in more open areas. Previous work has shown that, among wild individuals,H. cydnohas larger eyes thanH. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm thatH. cydnohas larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is moreH. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Thus, eye morphology differences betweenH. cydnoandH. melpomeneare consistent with adaptive divergence, and when combined with previous neuroanatomy data, suggest hybrid visual system disruption due to mismatched patterns of intermediacy and dominance in the visual pathway.