Seeing Picasso: an investigation into the visual system of the triggerfish Rhinecanthus aculeatus.

Vision is used by animals to find food and mates, avoid predators, defend resources and navigate through complex habitats. Behavioural experiments are essential for understanding animals' perception but are often challenging and time-consuming; therefore, using species that can be trained easily for complex tasks is advantageous. Picasso triggerfish, Rhinecanthus aculeatus, have been used in many behavioural studies investigating vision and navigation. However, little is known about the molecular and anatomical basis of their visual system. We addressed this knowledge gap here and behaviourally tested achromatic and chromatic acuity. In terms of visual opsins, R. aculeatus possessed one rod opsin gene (RH1) and at least nine cone opsins: one violet-sensitive SWS2B gene, seven duplicates of the blue-green-sensitive RH2 gene (RH2A, RH2B, RH2C1-5) and one red-sensitive LWS gene. However, only five cone opsins were expressed: SWS2B expression was consistent, while RH2A, RH2C-1 and RH2C-2 expression varied depending on whether fish were sampled from the field or aquaria. Levels of LWS expression were very low. Using fluorescence in situ hybridisation, we found SWS2B was expressed exclusively in single cones, whereas RH2A and RH2Cs were expressed in opposite double cone members. Anatomical resolution estimated from ganglion cell densities was 6.8 cycles per degree (cpd), which was significantly higher than values obtained from behavioural testing for black-and-white achromatic stimuli (3.9 cpd) and chromatic stimuli (1.7-1.8 cpd). These measures were twice as high as previously reported. This detailed information on their visual system will help inform future studies with this emerging focal species.

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.

Cardinalfishes (Apogonidae) show visual system adaptations typical of nocturnally and diurnally active fish.

Animal visual systems adapt to environmental light on various timescales. In scotopic conditions, evolutionary time-scale adaptations include spectral tuning to a narrower light spectrum, loss (or inactivation) of visual genes, and pure-rod or rod-dominated retinas. Some fishes inhabiting shallow coral reefs may show activity during the day and at night. It is unclear whether these fishes show adaptations typical of exclusively nocturnal or deep-sea fishes, or of diurnally active shallow-water species. Here, we investigated visual pigment diversity in cardinalfishes (Apogonidae). Most cardinalfishes are nocturnal foragers, yet they aggregate in multispecies groups in and around coral heads during the day, engaging in social and predator avoidance behaviours. We sequenced retinal transcriptomes of 28 species found on the Great Barrier Reef, assessed the diversity of expressed opsin genes and predicted the spectral sensitivities of resulting photopigments using sequence information. Predictions were combined with microspectrophotometry (MSP) measurements in seven cardinalfish species. Retinal opsin expression was rod opsin (RH1) dominated (>87%), suggesting the importance of scotopic vision. However, all species retained expression of multiple cone opsins also, presumably for colour vision. We found five distinct quantitative expression patterns among cardinalfishes, ranging from short-wavelength-shifted to long-wavelength-shifted. These results indicate that cardinalfishes are both well adapted to dim-light conditions and have retained a sophisticated colour vision sense. Other reef fish families also show both nocturnal and diurnal activity while most are strictly one or the other. It will be interesting to compare these behavioural differences across different phylogenetic groups using the criteria and methods developed here.

Short-term colour vision plasticity on the reef: changes in opsin expression under varying light conditions differ between ecologically distinct fish species.

Vision mediates important behavioural tasks such as mate choice, escape from predators and foraging. In fish, photoreceptors are generally tuned to specific visual tasks and/or to their light environment, according to depth or water colour to ensure optimal performance. Evolutionary mechanisms acting on genes encoding opsin, the protein component of the photopigment, can influence the spectral sensitivity of photoreceptors. Opsin genes are known to respond to environmental conditions on a number of time scales, including short time frames due to seasonal variation, or through longer-term evolutionary tuning. There is also evidence for 'on-the-fly' adaptations in adult fish in response to rapidly changing environmental conditions; however, results are contradictory. Here, we investigated the ability of three reef fish species that belong to two ecologically distinct families, yellow-striped cardinalfish (Ostorhinchus cyanosoma), Ambon damselfish (Pomacentrus amboinensis) and lemon damselfish (Pomacentrus moluccensis), to alter opsin gene expression as an adaptation to short-term (weeks to months) changes of environmental light conditions, and attempted to characterize the underlying expression regulation principles. We report the ability for all species to alter opsin gene expression within months and even a few weeks, suggesting that opsin expression in adult reef fish is not static. Furthermore, we found that changes in opsin expression in single cones generally occurred more rapidly than in double cones, and identified different responses of RH2 opsin gene expression between the ecologically distinct reef fish families. Quantum catch correlation analysis suggested different regulation mechanisms for opsin expression dependent on gene class.