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

Abstract

When 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.

Looking across the gap: Understanding the evolution of eyes and vision among insects

“…However, higher throughput connectomics is needed to better understand the function and evolution of visual systems within and between species. Finally, even where eye development and structure are well understood, especially within and among Drosophila species, a greater focus on the consequences for vision and how this underpins behavioral and ecological differences as exemplified in recent studies [45,68] is needed in future research.…”

“…[67] H. cydno has larger eyes, composed of more ommatidia, and bigger visual neuropil volume compared to H. melpomene and these morphological differences are under directional selection. [68][69][70] The males of both species also have larger eyes than the females. [68,70] These differences are presumably adaptations to the different habitats they occupy and for males to find mates.…”

“…[68][69][70] The males of both species also have larger eyes than the females. [68,70] These differences are presumably adaptations to the different habitats they occupy and for males to find mates. [68] Interestingly the eyes of the hybrid F1s of these two species are similar to H. melpomene while their neuropils are similar to H. cydno or intermediate between the species.…”

“…[68,70] These differences are presumably adaptations to the different habitats they occupy and for males to find mates. [68] Interestingly the eyes of the hybrid F1s of these two species are similar to H. melpomene while their neuropils are similar to H. cydno or intermediate between the species. [69] This exciting finding suggests there are differences in the coordination of eye and optic lobe development between these species, which disrupts hybrid visual systems and may affect their fitness.…”

“…[69] This exciting finding suggests there are differences in the coordination of eye and optic lobe development between these species, which disrupts hybrid visual systems and may affect their fitness. [68,69] This system has great potential to identify the genes underlying these differences in eye morphology and coordination with optic lobe development because these butterflies can be cultured and genetic mapping is possible (e.g. [71] ).…”