The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina

The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual systems of the coral reef fish family Holocentridae (squirrelfish and soldierfish). In addition to their nocturnality, this family is particularly interesting for dim-light vision studies due to its ecological and evolutionary connection to deeper habitats. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae having a slightly more developed photopic visual system than Myripristinae. Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of multibank retina and its potential for dim-light colour vision.

The Neural Basis of Dim-Light Vision in Echolocating Bats

Echolocating bats evolved a sophisticated biosonar imaging system that allows for a life in dim-light habitats. However, especially for far-range operations such as homing, bats can support biosonar by vision. Large eyes and a retina that mainly consists of rods are assumed to be the optical adjustments that enable bats to use visual information at low light levels. In addition to optical mechanisms, many nocturnal animals evolved neural adaptations such as elongated integration times or enlarged spatial sampling areas to further increase the sensitivity of their visual system by temporal or spatial summation of visual information. The neural mechanisms that underlie the visual capabilities of echolocating bats have, however, so far not been investigated. To shed light on spatial and temporal response characteristics of visual neurons in an echolocating bat, Phyllostomus discolor, we recorded extracellular multiunit activity in the retino-recipient superficial layers of the superior colliculus (SC). We discovered that response latencies of these neurons were generally in the mammalian range, whereas neural spatial sampling areas were unusually large compared to those measured in the SC of other mammals. From this we suggest that echolocating bats likely use spatial but not temporal summation of visual input to improve visual performance under dim-light conditions. Furthermore, we hypothesize that bats compensate for the loss of visual spatial precision, which is a byproduct of spatial summation, by integration of spatial information provided by both the visual and the biosonar systems. Given that knowledge about neural adaptations to dim-light vision is mainly based on studies done in non-mammalian species, our novel data provide a valuable contribution to the field and demonstrate the suitability of echolocating bats as a nocturnal animal model to study the neurophysiological aspects of dim-light vision.

Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity.