Search

Some vertebrate species have evolved means of extending their visual sensitivity beyond the range of human vision. One mechanism of enhancing sensitivity to long-wavelength light is to replace the 11-cis retinal chromophore in photopigments with 11-cis 3,4-didehydroretinal. Despite over a century of research on this topic, the enzymatic basis of this perceptual switch remains unknown. Here, we show that a cytochrome P450 family member, Cyp27c1, mediates this switch by converting vitamin A1 (the precursor of 11-cis retinal) into vitamin A2 (the precursor of 11-cis 3,4-didehydroretinal). Knockout of cyp27c1 in zebrafish abrogates production of vitamin A2, eliminating the animal's ability to red-shift its photoreceptor spectral sensitivity and reducing its ability to see and respond to near-infrared light. Thus, the expression of a single enzyme mediates dynamic spectral tuning of the entire visual system by controlling the balance of vitamin A1 and A2 in the eye.

SummarySunlight is attenuated rapidly in the ocean, resulting in little visually useful light reaching deeper than ∼1000 m in even the clearest water [1]. To maximize sensitivity to the relatively brighter downwelling sunlight, to view the silhouette of animals above them, and to increase the binocular overlap of their eyes, many mesopelagic animals have developed upward-pointing tubular eyes [2–4]. However, these sacrifice the ability to detect bioluminescent [5] and reflective objects in other directions. Thus, some mesopelagic fish with tubular eyes extend their visual fields laterally and/or ventrally by lensless ocular diverticula, which are thought to provide unfocused images, allowing only simple detection of objects, with little spatial resolution [2–4]. Here, we show that a medial mirror within the ventrally facing ocular diverticulum of the spookfish, Dolichopteryx longipes, consisting of a multilayer stack derived from a retinal tapetum, is used to reflect light onto a lateral retina. The reflective plates are not orientated parallel to the surface of the mirror. Instead, plate angles change progressively around the mirror, and computer modeling indicates that this provides a well-focused image. This is the first report of an ocular image being formed in a vertebrate eye by a mirror.

We are constantly surprised by the ability of relatively simple animals to perform precise visually guided movements within complex visual scenes, often using eyes with limited resolution. Exceptional examples include the capture of airborne prey by dragonflies [1], the learning flights of bees and wasps [2], and the tracking of conspecifics by crabs on intertidal mudflats [3-5]. Most studies have focused on how animals do this using sensitivity to intensity or color. However, it is increasingly evident that a third ability, polarization vision, may contribute to such tasks. In many insects, polarization-sensitive photoreceptors are confined within an area of the eye known as the dorsal rim [6], which detects the polarized sky pattern specifically for navigation [7]. However, some animals, including fiddler crabs, are sensitive to the polarization of light across the majority of their image-forming eyes [8, 9], potentially allowing them to use polarization information to increase perceived contrast for general visual tasks [10-13]. Investigations into the use of polarization image-parsing by animals have largely been confined to laboratory settings under artificial lighting [10, 13-18]. This approach can occasionally mislead if the lighting conditions are different from natural [19]. This study presents the first behavioral evidence from the natural context for a function of polarization image parsing. Using experimental manipulations in wild populations of the fiddler crab Uca stenodactylus, we provide evidence that these animals use their polarization vision to enhance contrast in their visual environment, thereby increasing their ability to detect and respond to objects on the mudflat surface.

Summary For animals that can see it, the polarisation of light adds another dimension to vision, analogous to adding colour to a black and white image [1,2]. Whilst some animals use the orientation of the electric field vector (e-vector) for navigation and orientation [3], the ability to discriminate angular differences in e-vector has been implicated in object recognition for predator/prey detection [4,5] as well as signalling and communication [6]. In all animals previously tested, however, the resolution of e-vector angle discrimination has been found to be in the range 10–20° [5,7,8], which is inadequate for the typical e-vector differences measured in relevant natural visual scenes [9]. In this study, we found that mourning cuttlefish ( Sepia plangon ) are able to detect differences between e-vector orientations as small as 1°. Not only is this the most acute e-vector angle discrimination measured behaviourally in any animal, but it provides a high enough resolution to be relevant to real world visual tasks. We analysed natural underwater scenes using computer based polarisation imaging. When we increased the resolution of our system, we discovered information not detected using normal-resolution imaging polarimetry and invisible to animals lacking fine e-vector angle discrimination. For example, we found that high-resolution e-vector discrimination provides a new way of breaking typical intensity-based background matching. S. plangon lacks colour vision, like most other cephalopods, and high-resolution polarisation vision may provide an alternative source of contrast information that is just as fine-scale.