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Light in nature addresses the optical phenomena we see in our everyday lives, ranging from rainbows and auroras to insect wing colors. Explanations of these phenomena draw from fields that include optical science, physics, engineering, chemistry, biology, astronomy, photography, and art. What is light? How do the beautiful and often colorful features in nature appear? What are the best ways of observing and studying these things? How does human vision affect what we see with these phenomena? Join this virtual live event panel discussion for an exploration into light in nature.

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’s 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.

Synopsis Locomotion is a hallmark of organisms which has enabled adaptive radiation to an extraordinarily diverse class of ecological niches, and allows animals to move across vast distances. Sampling from multiple sensory modalities enables animals to acquire rich information to guide locomotion. Locomotion without sensory feedback is haphazard; therefore, sensory and motor systems have evolved complex interactions to generate adaptive behavior. Notably, sensory-guided locomotion acts over broad spatial and temporal scales to permit goal-seeking behavior, whether to localize food by tracking an attractive odor plume or to search for a potential mate. How does the brain integrate multimodal stimuli over different temporal and spatial scales to effectively control behavior? In this review, we classify locomotion into three ordinally ranked hierarchical layers that act over distinct spatiotemporal scales: stabilization, motor primitives, and higher-order tasks, respectively. We discuss how these layers present unique challenges and opportunities for sensorimotor integration. We focus on recent advances in invertebrate locomotion due to their accessible neural and mechanical signals from the whole brain, limbs, and sensors. Throughout, we emphasize neural-level description of computations for multimodal integration in genetic model systems, including the fruit fly, Drosophila melanogaster, and the yellow fever mosquito, Aedes aegypti. We identify that summation (e.g., gating) and weighting—which are inherent computations of spiking neurons—underlie multimodal integration across spatial and temporal scales, therefore suggesting collective strategies to guide locomotion.

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.

Abstract In the context of mate choice, males may vary continuously in their expression of assessment signals, typically reflecting information about variation in mate quality. Similarly, females may exhibit variation in mate preference, which could be due to differences in how individual females perceive signals. The extent to which perception varies across individuals, however, and whether differences in sensory physiology underlie perceptual differences is poorly understood. Carotenoid pigments create the orange-red coloration of many assessment signals, and they also play a role in color discrimination in many vertebrates via their presence in retinal oil droplets. Here, we link variation in oil droplet carotenoid concentration with the ability of female zebra finches (Taeniopygia guttata) to discriminate an orange-red color continuum that parallels variation in male beak color, a mate assessment signal. We have shown previously that zebra finch females perceive this color range categorically, meaning they label color stimuli from this continuum as belonging to two categories and exhibit better discrimination between colors from different categories as compared with equally different colors from within a category. We quantified behavioral color discrimination and R-type (red) cone oil droplet spectral absorption, a proxy for carotenoid concentration. Oil droplet absorption was strongly predictive of variation in behavioral color discrimination ability. In particular, higher carotenoid concentration in oil droplets correlated with increased discrimination of colors from different sides of the previously identified category boundary. These data show that differences in the sensory periphery can correlate with individual variation in perception of a signal-relevant color range. Significance statement Signal receivers vary in their preferences for signaling traits, but whether this is due to variation in how different receivers perceive signals is not well-understood. We show that variation between individual zebra finch females in perception of an orange-red continuum range correlates with the carotenoid concentration of retinal oil droplets. These data provide the first direct evidence that individual variation in oil droplet carotenoid concentration can lead to variation in color discrimination ability. Linking variation in signal-relevant color discrimination ability with variation in retinal physiology suggests a potential mechanism contributing to individual variation in signal assessment.

Rod spectral sensitivity data (λmax ), measured by microspectrophotometry, were compiled for 403 species of ray-finned fishes 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 to 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.

Across diverse taxa, an increasing number of photoreceptive systems are being discovered in tissues outside of the eye, such as in the skin. Dermal photoreception is believed to serve a variety of functions, including rapid color change via specialized cells called chromatophores. In vitro studies of this system among color-changing fish have suggested the use of a phototransduction signaling cascade that fundamentally differs from that of the retina. Thus, the goal of this study was to identify phototransduction genes and compare their expression in the retina and skin of a color-changing fish, the hogfish Lachnolaimus maximus. De novo transcriptomics revealed the expression of genes that may underlie distinct, yet complete phototransduction cascades in L. maximus retina and skin. In contrast to the five visual opsin genes and cGMP-dependent phototransduction components expressed in the retina of L. maximus, only a single short-wavelength sensitive opsin (SWS1) and putative cAMP-dependent phototransduction components were expressed in the skin. These data suggest a separate evolutionary history of phototransduction in the retina and skin of certain vertebrates and, for the first time, indicate an expression repertoire of genes that underlie a non-retinal phototransduction pathway in the skin of a color-changing fish.

The classical understanding of mammalian vision is that it occurs through "duplex" retinae containing both rod and cone photoreceptors, the signals from which are processed through rod- and/or cone-specific signaling pathways. The recent discovery of rod monochromacy in some cetacean lineages provides a novel opportunity to investigate the effects of an evolutionary loss of cone photoreception on retinal organization. Sequence analysis of right whale (Eubalaena glacialis; family Balaenidae) cDNA derived from long-wavelength sensitive (LWS) cone opsin mRNA identified several mutations in the opsin coding sequence, suggesting the loss of cone cell function, but maintenance of non-photosensitive, cone opsin mRNA-expressing cells in the retina. Subsequently, we investigated the retina of the closely related bowhead whale (Balaena mysticetus; family Balaenidae) to determine how the loss of cone-mediated photoreception affects light signaling pathways in the retina. Anti-opsin immunofluorescence demonstrated the total loss of cone opsin expression in B. mysticetus, whereas light microscopy, transmission electron microscopy, and bipolar cell (protein kinase C-α [PKC-α] and recoverin) immunofluorescence revealed the maintenance of cone soma, putative cone pedicles, and both rod and cone bipolar cell types. These findings represent the first immunological and anatomical evidence of a naturally occurring rod-monochromatic mammalian retina, and suggest that despite the loss of cone-mediated photoreception, the associated cone signaling structures (i.e., cone synapses and cone bipolar cells) may be maintained for multichannel rod-based signaling in balaenid whales. J. Comp. Neurol. 524:2873-2885, 2016. © 2016 Wiley Periodicals, Inc.

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, and 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.

Fish that undergo ontogenetic migrations between habitats often encounter new light environments that require changes in the spectral sensitivity of the retina. For many fish, sensitivity of the retina changes to match the environmental spectrum, but the timing of retinal change relative to habitat shift remains unknown. Does retinal change in fish precede habitat shift, or is it a response to encountered changes in environmental light? Spectral sensitivity changes were examined over the development of the Atlantic tarpon (Megalops atlanticus) retina relative to ontogenetic shifts in habitat light. Opsin gene isoform expression and inferred chromophore use of visual pigments were examined over the course of M. atlanticus development. Spectral sensitivity of the retina was then determined by electroretinography and compared to the spectroradiometric measurements of habitat light encountered by M. atlanticus from juveniles to adults. These data, along with previously known microspectrophotometric measurements of sensitivity in M. atlanticus, indicate retinal spectral sensitivity that matches the dominant wavelengths of environmental light for juvenile and adult fish. For the intervening subadult stage, however, spectral sensitivity does not match the dominant wavelength of light it occupies but better matches the dominant wavelengths of light in the habitat of its forthcoming migration. These results first indicate that the relationship between environmental light spectrum and spectral sensitivity of the retina changes during M. atlanticus development and then suggest that such changes may be programmed to support visual anticipation of new photic environments.

North Atlantic right whales (Eubalaena glacialis) feed during the spring and early summer in marine waters off the northeast coast of North America. Their food primarily consists of planktonic copepods, Calanus finmarchicus, which they consume in large numbers by ram filter feeding. The coastal waters where these whales forage are turbid, but they successfully locate copepod swarms during the day at depths exceeding 100 m, where light is very dim and copepod patches may be difficult to see. Using models of E. glacialis visual sensitivity together with measurements of light in waters near Cape Cod where they feed and of light attenuation by living copepods in seawater, we evaluated the potential for visual foraging by these whales. Our results suggest that vision may be useful for finding copepod patches, particularly if E. glacialis searches overhead for silhouetted masses or layers of copepods. This should permit the whales to locate C. finmarchicus visually throughout most daylight hours at depths throughout their foraging range. Looking laterally, the whales might also be able to see copepod patches at short range near the surface.

The ability to perceive the Earth's magnetic field, or magnetoreception, exists in numerous animals. Although the mechanism underlying magnetoreception has not been clearly established in any species, in salmonid fish, it is hypothesized to occur by means of crystals of magnetite associated with nervous tissue such as the brain, olfactory organ or retina. In this study, rainbow trout ( Oncorhynchus mykiss ) were exposed to a brief magnetic pulse known to disrupt magnetic orientation behaviour in several animals. Changes in gene expression induced by the pulse were then examined in the retina. Analyses indicated that the pulse elicited differential expression of only a single gene, gamma-crystallin M3-like ( crygm3 ). The near absence of an effect of the magnetic pulse on gene expression in the retina stands in sharp contrast to a recent study in which 181 genes were differentially expressed in brain tissue of O. mykiss after exposure to the same pulse. Overall, our results suggest either that magnetite-based magnetoreceptors in trout are not located in the retina, or else that they are unaffected by magnetic pulses that can disrupt magnetic orientation behaviour in animals.

North Atlantic right whales ( Eubalaena glacialis ) feed during the spring and early summer in marine waters off the northeast coast of North America. Their food primarily consists of planktonic copepods, Calanus finmarchicus , which they consume in large numbers by ram filter feeding. The coastal waters where these whales forage are turbid, but they successfully locate copepod swarms during the day at depths exceeding 100 m, where light is very dim and copepod patches may be difficult to see. Using models of E. glacialis visual sensitivity together with measurements of light in waters near Cape Cod where they feed and of light attenuation by living copepods in seawater, we evaluated the potential for visual foraging by these whales. Our results suggest that vision may be useful for finding copepod patches, particularly if E. glacialis searches overhead for silhouetted masses or layers of copepods. This should permit the whales to locate C. finmarchicus visually throughout most daylight hours at depths throughout their foraging range. Looking laterally, the whales might also be able to see copepod patches at short range near the surface. This article is part of the themed issue ‘Vision in dim light’.