Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish

The distinct behaviours of animals and the varied habitats in which animals live place different requirements on their visual systems. A trade-off exists between resolution and sensitivity, with these properties varying across the retina. Spectral sensitivity, which affects both achromatic and chromatic (colour) vision, also varies across the retina, though the function of this inhomogeneity is less clear. We previously demonstrated spatially varying spectral sensitivity of double cones in the cichlid fish Metriaclima zebra owing to coexpression of different opsins. Here, we map the distributions of ganglion cells and cone cells and quantify opsin coexpression in single cones to show these also vary across the retina. We identify an area centralis with peak acuity and infrequent coexpression, which may be suited for tasks such as foraging and detecting male signals. The peripheral retina has reduced ganglion cell densities and increased opsin coexpression. Modeling of cichlid visual tasks indicates that coexpression might hinder colour discrimination of foraging targets and some fish colours. But, coexpression might improve contrast detection of dark objects against bright backgrounds, which might be useful for detecting predators or zooplankton. This suggests a trade-off between acuity and colour discrimination in the central retina versus lower resolution but more sensitive contrast detection in the peripheral retina. Significant variation in the pattern of coexpression among individuals, however, raises interesting questions about the selective forces at work

Retinal ganglion cell topography and spatial resolving power in echolocating and non-echolocating bats

Bats are nocturnal mammals known for their ability to echolocate, yet all bats can see, and most bats of the family Pteropodidae (fruit bats) do not echolocate-instead they rely mainly on vision and olfaction to forage. We investigated whether echolocating bats, given their limited reliance on vision, have poorer spatial resolving power (SRP) than pteropodids and whether tongue click echolocating fruit bats differ from non-echolocating fruit bats in terms of visual performance. We compared the number and distribution of retinal ganglion cells (RGCs) as well as the maximum anatomical SRP derived from these distributions in 4 species of bats: Myotis daubentonii, a laryngeal echolocating bat from the family Vespertilionidae, Rousettus aegyptiacus, a tongue clicking echolocating bat from the family Pteropodidae, and Pteropus alecto and P. poliocephalus, 2 non-echolocating bats (also from the Pteropodidae). We find that all 3 pteropodids have a similar number (≈200,000 cells) and distribution of RGCs and a similar maximum SRP (≈4 cycles/degree). M. daubentonii has fewer (∼6,000 cells) and sparser RGCs than the pteropodids and thus a significantly lower SRP (0.6 cycles/degree). M. daubentonii also differs in terms of the distribution of RGCs by having a unique dorsal area of specialization in the retina. Our findings are consistent with the existing literature and suggest that M. daubentonii likely only uses vision for orientation, while for pteropodids vision is also important for foraging

The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophidae)

The mesopelagic zone of the deep-sea (200-1000 m) is characterised by exponentially diminishing levels of downwelling sunlight and by the predominance of bioluminescence emissions. The ability of mesopelagic organisms to detect and behaviourally react to downwelling sunlight and/or bioluminescence will depend on the visual task and ultimately on the eyes and their capacity for detecting low levels of illumination and intermittent point sources of bioluminescent light. In this study, we investigate the diversity of the visual system of the lanternfish (Myctophidae). We focus specifically on the photoreceptor cells by examining their size, arrangement, topographic distribution and contribution to optical sensitivity in 53 different species from 18 genera. We also examine the influence(s) of both phylogeny and ecology on these photoreceptor variables using phylogenetic comparative analyses in order to understand the constraints placed on the visual systems of this large group of mesopelagic fishes at the first stage of retinal processing. We report great diversity in the visual system of the Myctophidae at the level of the photoreceptors. Photoreceptor distribution reveals clear interspecific differences in visual specialisations (areas of high rod photoreceptor density), indicating potential interspecific differences in interactions with prey, predators and/or mates. A great diversity in photoreceptor design (length and diameter) and density is also present. Overall, the myctophid eye is very sensitive compared to other teleosts and each species seems to be specialised for the detection of a specific signal (downwelling light or bioluminescence), potentially reflecting different visual demands for survival. Phylogenetic comparative analyses highlight several relationships between photoreceptor characteristics and the ecological variables tested (depth distribution and luminous tissue patterns). Depth distribution at night was a significant factor in most of the models tested, indicating that vision at night is of great importance for lanternfishes and may drive the evolution of their photoreceptor design

Visual system development of the spotted unicornfish, Naso brevirostris (Acanthuridae)

Ontogenetic changes of the visual system are often correlated to shifts in habitat and feeding behaviour of animals. Coral reef fishes begin their lives in the pelagic zone and then migrate to the reef. This habitat transition frequently involves a change in diet and light environment as well as major morphological modifications. The spotted unicornfish, , is known to shift diet from zooplankton to algae and back to mainly zooplankton when transitioning from larval to juvenile and then to adult stages. Concurrently, also moves from an open pelagic to a coral-associated habitat before migrating up in the water column when reaching adulthood. Using retinal mapping techniques, we discovered that the distribution and density of ganglion and photoreceptor cells in mostly changes during the transition from the larval to the juvenile stage, with only minor modifications thereafter. Similarly, visual gene (opsin) expression based on RNA sequencing, although qualitatively similar between stages (all fishes mainly expressed the same three cone opsins; ), also showed the biggest quantitative difference when transitioning from larvae to juveniles. The juvenile stage in particular seems mismatched with its reef-associated ecology, which may be due to this stage only lasting a fraction of the lifespan of these fishes. Hence, the visual ontogeny found in is very different from the progressive changes found in other reef fishes calling for a thorough analysis of visual system development of the reef fish community

Developing and adult reef fish show rapid light‐induced plasticity in their visual system

The visual capabilities of fish are optimized for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e.g., ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short-term changes in the light environment, e.g., algal blooms and light pollution. In this study, we investigated the effect of short-term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in juvenile and adult diurnal reef fish (convict surgeonfish; Acanthurus triostegus). Results revealed phenotypic plasticity in the retina across ontogeny, particularly during development. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light and simulated artificial light at night had a lesser effect. Under dim light, juveniles and adults increased absolute expression of the cone opsin genes, sws2a, rh2c and lws, within a few days and juveniles also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes potentially enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species' natural light environment, i.e., a diurnal fish in “constant night”. Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 h. Overall, our study showed rapid, reversible light-induced changes in the retina of A. triostegus, demonstrating phenotypic plasticity in the visual system of a reef fish throughout life

Development of dim-light vision in the nocturnal reef fish family Holocentridae. II: Retinal morphology

International audienceOntogenetic changes in the habitats and lifestyles of animals are often reflected in their visual systems. Coral reef fishes start life in the shallow open ocean but inhabit the reef as juveniles and adults. Alongside this change in habitat, some species also change lifestyles and become nocturnal. However, it is not fully understood how the visual systems of nocturnal reef fishes develop and adapt to these significant ecological shifts over their lives. Therefore, we used a histological approach to examine visual development in the nocturnal coral reef fish family, Holocentridae. We examined 7 representative species spanning both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes). Pre-settlement larvae showed strong adaptation for photopic vision with high cone densities and had also started to develop a multibank retina (i.e. multiple rod layers), with up to two rod banks present. At reef settlement, holocentrids showed greater adaptation for scotopic vision, with higher rod densities and higher summation of rods onto the ganglion cell layer. By adulthood, they had well-developed scotopic vision with a highly rod-dominated multibank retina comprising 5-17 rod banks and enhanced summation of rods onto the ganglion cell layer. Although the ecological demands of the two subfamilies were similar throughout their lives, their visual systems differed after settlement, with Myripristinae showing more pronounced adaptation for scotopic vision than Holocentrinae. Thus, it is likely that both ecology and phylogeny contribute to the development of the holocentrid visual system

Development of dim-light vision in the nocturnal reef fish family Holocentridae. I: Retinal gene expression

Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well adapted to photopic conditions with pre-settlement larvae having high levels of cone opsin gene expression and a broad cone opsin gene repertoire (8 genes). At reef settlement, holocentrids started to invest more in their scotopic visual system, and compared with adults, showed upregulation of genes involved in cell differentiation/proliferation. By adulthood, holocentrids had well developed scotopic vision with high levels of rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems diverged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny are likely to determine the development of the holocentrid visual system

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 system of the nocturnal reef fish family Holocentridae. 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 (squirrelfish) having a slightly more developed photopic visual system than Myripristinae (soldierfish). 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 the multibank retina and its potential for dim-light colour vision