Spectral Sensitivity in Ray-Finned Fishes: Diversity, Ecology and Shared Descent

A major goal of sensory ecology is to identify factors that underlie sensory-trait variation. One open question centers on why fishes show the greatest diversity among vertebrates in their capacity to detect color (i.e. spectral sensitivity). Over the past several decades, λmax values (photoreceptor class peak sensitivity) and chromacy (photoreceptor class number) have been cataloged for hundreds of fish species, yet the ecological basis of this diversity and the functional significance of high chromacy levels (e.g. tetra- and pentachromacy) remain unclear. In this study, we examined phylogenetic, physiological and ecological patterns of spectral sensitivity of ray-finned fishes (Actinoptergyii) via a meta-analysis of data compiled from 213 species. Across the fishes sampled, our results indicate that trichromacy is most common, ultraviolet λmax values are not found in monochromatic or dichromatic species, and increasing chromacy, including from tetra- to pentachromacy, significantly increases spectral sensitivity range. In an ecological analysis, multivariate phylogenetic latent liability modeling was performed to analyze correlations between chromacy and five hypothesized predictors (depth, habitat, diet, body coloration, body size). In a model not accounting for phylogenetic relatedness, each predictor with the exception of habitat significantly correlated with chromacy: a positive relationship in body color and negative relationships with body size, diet and depth. However, after phylogenetic correction, the only remaining correlated predictor was depth. The findings of this study indicate that phyletic heritage and depth are important factors in fish spectral sensitivity and impart caution about excluding phylogenetic comparative methods in studies of sensory trait variation

Dynamic light filtering over dermal opsin as a sensory feedback system in fish color change

Dynamic color change has evolved multiple times, with a physiological basis that has been repeatedly linked to dermal photoreception via the study of excised skin preparations. Despite the widespread prevalence of dermal photoreception, both its physiology and its function in regulating color change remain poorly understood. By examining the morphology, physiology, and optics of dermal photoreception in hogfish (Lachnolaimus maximus), we describe a cellular mechanism in which chromatophore pigment activity (i.e., dispersion and aggregation) alters the transmitted light striking SWS1 receptors in the skin. When dispersed, chromatophore pigment selectively absorbs the short-wavelength light required to activate the skin’s SWS1 opsin, which we localized to a morphologically specialized population of putative dermal photoreceptors. As SWS1 is nested beneath chromatophores and thus subject to light changes from pigment activity, one possible function of dermal photoreception in hogfish is to monitor chromatophores to detect information about color change performance. This framework of sensory feedback provides insight into the significance of dermal photoreception among color-changing animals

Altered environmental light drives retinal change in the Atlantic Tarpon (Megalops atlanticus) over timescales relevant to marine environmental disturbance

Abstract Background For many fish species, retinal function changes between life history stages as part of an encoded developmental program. Retinal change is also known to exhibit plasticity because retinal form and function can be influenced by light exposure over the course of development. Aside from studies of gene expression, it remains largely unknown whether retinal plasticity can provide functional responses to short-term changes in environmental light quality. The aim of this study was to determine whether the structure and function of the fish retina can change in response to altered light intensity and spectrum—not over the course of a developmental regime, but over shorter time periods relevant to marine habitat disturbance. Results The effects of light environment on sensitivity of the retina, as well as on cone photoreceptor distribution were examined in the Atlantic tarpon (Megalops atlanticus) on 2- and 4-month timescales. In a spectral experiment, juvenile M. atlanticus were placed in either ‘red’ or ‘blue’ light conditions (with near identical irradiance), and in an intensity experiment, juveniles were placed in either ‘bright’ or ‘dim’ light conditions (with near identical spectra). Analysis of the retina by electroretinography and anti-opsin immunofluorescence revealed that relative to fish held in the blue condition, those in the red condition exhibited longer-wavelength peak sensitivity and greater abundance of long-wavelength-sensitive (LWS) cone photoreceptors over time. Following pre-test dark adaption of the retina, fish held in the dim light required less irradiance to produce a standard retinal response than fish held in bright light, developing a greater sensitivity to white light over time. Conclusions The results show that structure and function of the M. atlanticus retina can rapidly adjust to changes in environmental light within a given developmental stage, and that such changes are dependent on light quality and the length of exposure. These findings suggest that the fish retina may be resilient to disturbances in environmental light, using retinal plasticity to compensate for changes in light quality over short timescales

Variation in Rod Spectral Sensitivity of Fishes is Best Predicted by Habitat and Depth

Microspectrophotometry was used to compile rod spectral sensitivity data (λmax) for 403 species of ray‐finned fishes (Actinopterygii) in order to examine four hypothesized predictors of rod spectral sensitivity (depth, habitat, diet and temperature). From this database, a subset of species that were known to be adults and available on a published phylogeny (n = 210) were included in analysis, indicating rod λmax values averaging 503 nm and ranging from 477–541 nm. Linear models that corrected for phylogenetic relatedness showed that variation in rod sensitivity was best predicted by habitat and depth, with shorter wavelength λmax values occurring in fishes found offshore or in the deep sea. Neither diet, nor the interaction of diet and habitat, had significant explanatory power. Although temperature significantly correlated with rod sensitivity, in that fishes in temperate latitudes had longer wavelength rod λmax values than those in tropical latitudes, sampling inequity and other confounds require the role of the temperature to be studied further. Together, these findings indicate that fish rod λmax is influenced by several ecological factors, suggesting that selection can act on even small differences in fish spectral sensitivity

Spectral tuning and deactivation kinetics of marine mammal melanopsins

In mammals, the photopigment melanopsin (Opn4) is found in a subset of retinal ganglion cells that serve light detection for circadian photoentrainment and pupil constriction (i.e., mydriasis). For a given species, the efficiency of photoentrainment and length of time that mydriasis occurs is determined by the spectral sensitivity and deactivation kinetics of melanopsin, respectively, and to date, neither of these properties have been described in marine mammals. Previous work has indicated that the absorbance maxima (λmax) of marine mammal rhodopsins (Rh1) have diversified to match the available light spectra at foraging depths. However, similar to the melanopsin λmax of terrestrial mammals (~480 nm), the melanopsins of marine mammals may be conserved, with λmax values tuned to the spectrum of solar irradiance at the water\u27s surface. Here, we investigated the Opn4 pigments of 17 marine mammal species inhabiting diverse photic environments including the Infraorder Cetacea, as well as the Orders Sirenia and Carnivora. Both genomic and cDNA sequences were used to deduce amino acid sequences to identify substitutions most likely involved in spectral tuning and deactivation kinetics of the Opn4 pigments. Our results show that there appears to be no amino acid substitutions in marine mammal Opn4 opsins that would result in any significant change in λmax values relative to their terrestrial counterparts. We also found some marine mammal species to lack several phosphorylation sites in the carboxyl terminal domain of their Opn4 pigments that result in significantly slower deactivation kinetics, and thus longer mydriasis, compared to terrestrial controls. This finding was restricted to cetacean species previously found to lack cone photoreceptor opsins, a condition known as rod monochromacy. These results suggest that the rod monochromat whales rely on extended pupillary constriction to prevent photobleaching of the highly photosensitive all-rod retina when moving between photopic and scotopic conditions

Surf and turf vision: Patterns and predictors of visual acuity in compound eye evolution

Eyes have the flexibility to evolve to meet the ecological demands of their users. Relative to camera-type eyes, the fundamental limits of optical diffraction in arthropod compound eyes restrict the ability to resolve fine detail (visual acuity) to much lower degrees. We tested the capacity of several ecological factors to predict arthropod visual acuity, while simultaneously controlling for shared phylogenetic history. In this study, we have generated the most comprehensive review of compound eye visual acuity measurements to date, containing 385 species that span six of the major arthropod classes. An arthropod phylogeny, made custom to this database, was used to develop a phylogenetically-corrected generalized least squares (PGLS) linear model to evaluate four ecological factors predicted to underlie compound eye visual acuity: environmental light intensity, foraging strategy (predator vs. non-predator), horizontal structure of the visual scene, and environmental medium (air vs. water). To account for optical constraints on acuity related to animal size, body length was also included, but this did not show a significant effect in any of our models. Rather, the PGLS analysis revealed that the strongest predictors of compound eye acuity are described by a combination of environmental medium, foraging strategy, and environmental light intensity

Dynamic light filtering over dermal opsin as a sensory feedback system in fish color change

Abstract Dynamic color change has evolved multiple times, with a physiological basis that has been repeatedly linked to dermal photoreception via the study of excised skin preparations. Despite the widespread prevalence of dermal photoreception, both its physiology and its function in regulating color change remain poorly understood. By examining the morphology, physiology, and optics of dermal photoreception in hogfish (Lachnolaimus maximus), we describe a cellular mechanism in which chromatophore pigment activity (i.e., dispersion and aggregation) alters the transmitted light striking SWS1 receptors in the skin. When dispersed, chromatophore pigment selectively absorbs the short-wavelength light required to activate the skin’s SWS1 opsin, which we localized to a morphologically specialized population of putative dermal photoreceptors. As SWS1 is nested beneath chromatophores and thus subject to light changes from pigment activity, one possible function of dermal photoreception in hogfish is to monitor chromatophores to detect information about color change performance. This framework of sensory feedback provides insight into the significance of dermal photoreception among color-changing animals

Supplementary Material from Coping with copepods: do right whales (<i>Eubalaena glacialis</i>) forage visually in dark waters?

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Electronic Supplementary Material from Near absence of differential gene expression in the retina of rainbow trout after exposure to a magnetic pulse: implications for magnetoreception

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