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

The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arises across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-million-year-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. 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) relaxed selection on visual opsins, perhaps mediated by habitat preference, (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 the perceptual, processing and molecular level.

Fiddler crab electroretinograms reveal vast circadian shifts in visual sensitivity and temporal summation in dim light.

Many animals with compound eyes undergo major optical changes to adjust visual sensitivity from day to night, often under control of a circadian clock. In fiddler crabs, this presents most conspicuously in the huge volume increase of photopigment-packed rhabdoms and the widening of crystalline cone apertures at night. These changes are hypothesised to adjust the light flux to the photoreceptors and to alter optical sensitivity as the eye moves between light- and dark-adapted states. Here, we compared optical sensitivity in fiddler crab (Gelasimus dampieri) eyes during daytime and night via three electroretinogram (ERG) experiments performed on light- and dark-adapted crabs. (1) Light intensity required to elicit a threshold ERG response varied over six orders of magnitude, allowing more sensitive vision for discriminating small contrasts in dim light after dusk. During daytime, the eyes remained relatively insensitive, which would allow effective vision on bright mudflats, even after prolonged dark adaptation. (2) Flicker fusion frequency (FFF) experiments indicated that temporal summation is employed in dim light to increase light-gathering integration times and enhance visual sensitivity during both night and day. (3) ERG responses to flickering lights during 60 min of dark adaptation increased at a faster rate and to a greater extent after sunset compared with daytime. However, even brief, dim and intermittent light exposure strongly disrupted dark-adaptation processes. Together, these findings demonstrate effective light adaptation to optimise vision over the large range of light intensities that these animals experience.

Light adaptation mechanisms in the eye of the fiddler crab Afruca tangeri.

A great diversity of adaptations is found among animals with compound eyes and even closely related taxa can show variation in their light-adaptation strategies. A prime example of a visual system evolved to function in specific light environments is the fiddler crab, used widely as a model to research aspects of crustacean vision and neural pathways. However, questions remain regarding how their eyes respond to the changes in brightness spanning many orders of magnitude, associated with their habitat and ecology. The fiddler crab Afruca tangeri forages at low tide on tropical and semi-tropical mudflats, under bright sunlight and on moonless nights, suggesting that their eyes undergo effective light adaptation. Using synchrotron X-ray tomography, light and transmission electron microscopy and in vivo ophthalmoscopy, we describe the ultrastructural changes in the eye between day and night. Dark adaptation at dusk triggered extensive widening of the rhabdoms and crystalline cone tips. This doubled the ommatidial acceptance angles and increased microvillar surface area for light capture in the rhabdom, theoretically boosting optical sensitivity 7.4 times. During daytime, only partial dark-adaptation was achieved and rhabdoms remained narrow, indicating strong circadian control on the process. Bright light did not evoke changes in screening pigment distributions, suggesting a structural inability to adapt rapidly to the light level fluctuations frequently experienced when entering their burrow to escape predators. This should enable fiddler crabs to shelter for several minutes without undergoing significant dark-adaptation, their vision remaining effectively adapted for predator detection when surfacing again in bright light.