Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

Abstract

The striking structural variation seen in arthropod visual systems can be explained by availability of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arise across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific, intraspecific and intraindividual variation in the visual system of four ithomiine butterfly species. These species are part of a diverse Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. By using a combination of selection analyses on visual opsin sequences, in-vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy, and neural tracing, we quantify and describe physiological, anatomical, and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including i) habitat-associated relaxed selection on visual opsins, ii) interspecific shifts in visual system physiology and anatomy, and iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at both the perceptual, processing, and molecular level.