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

Abstract

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.

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

“…Their large eyes (Schmitz and Wainwright 2011), short focal length (McFarland 1991), roddominated retina (this study), extremely high RH1 expression compared to other coral reef fishes [i.e. > 95% in holocentrids (this study) vs 50-70% in damselfishes , Stieb et al 2019) and diurnal apogonids (Luehrmann et al 2019)], and their rod spectral sensitivity tuned to their respective depth range (Toller 1996), indicate a visual system well-adapted to dim-light vision and a need for increased sensitivity. Therefore, multibank retinas in holocentrids are likely to contribute toward enhancing the overall light sensitivity of their eyes.…”

Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae)

“…After removal of the cornea, the lens was extracted and its diameter measured (Table S1). Species were identified based on morphology and colouration and, where possible, subsequently confirmed via RNA sequencing and by cross‐referencing cytochrome c oxidase subunit 1 gene ( COI )sequences to public databases (boldsystems.org; Luehrmann et al, ).…”

“…We used proportional opsin gene expression data from our previous work on 26 cardinalfish species collected from the same locations (Luehrmann et al, ; Table S5). These included all of the species used for microhabitat partitioning analysis (Table ) and those for which relative eye sizes and retinal topography maps were obtained (Tables S1 and S3).…”

“…Here, to control for potentially confounding factors like phylogenetic constraint, we focused on a group of closely related reef fishes with remarkable visual system diversity, the cardinalfishes (Apogonidae; Fishelson, Ayalon, Zverdling, & Holzman, ; Luehrmann, Carleton, Cortesi, Cheney, & Marshall, ). These fishes are common on shallow tropical coral reefs, are one of the most abundant reef fish families and are predominantly nocturnal foragers (Marnane & Bellwood, ).…”

“…Second, we tested whether their opsin gene expression, and/or relative eye size—as a proxy for light sensitivity (Land, ) — correlated with diurnal microhabitat use. We used our previous opsin expression data which showed that cardinalfishes express multiple visual opsins, and that based on differences in opsin gene expression and spectral sensitivities, species could be placed into five, possibly functionally distinct, groups (Luehrmann et al, ). Third, the retinal photoreceptor and/or ganglion cell topographies of five cardinalfish species from different microhabitats were determined to gain additional insight into these fishes’ adaptations to their environment.…”