SUMMARYThe correlation between ontogenetic changes in the spectral absorption characteristics of retinal photoreceptors and expression of visual pigment opsins was investigated in the black bream, Acanthopagrus butcheri. To establish whether the spectral qualities of environmental light affected the complement of visual pigments during ontogeny, comparisons were made between fishes reared in: (1) broad spectrum aquarium conditions; (2) short wavelength-reduced conditions similar to the natural environment; or (3) the natural environment (wild-caught). Microspectrophotometry was used to determine the wavelengths of spectral sensitivity of the photoreceptors at four developmental stages: larval, post-settlement, juvenile and adult. The molecular sequences of the rod (Rh1) and six cone (SWS1, SWS2A and B, Rh2Aα and β, and LWS) opsins were obtained and their expression levels in larval and adult stages examined using quantitative RT-PCR. The changes in spectral sensitivity of the cones were related to the differing levels of opsin expression during ontogeny. During the larval stage the predominantly expressed opsin classes were SWS1, SWS2B and Rh2Aα, contrasting with SWS2A, Rh2Aβ and LWS in the adult. An increased proportion of long wavelength-sensitive double cones was found in fishes reared in the short wavelength-reduced conditions and in wildcaught animals, indicating that the expression of cone opsin genes is also regulated by environmental light.
Vertebrate color vision is best developed in fish, reptiles, and birds with four distinct cone receptor visual pigments. These pigments, providing sensitivity from ultraviolet to infrared light, are thought to have been present in ancestral vertebrates. When placental mammals adopted nocturnality, they lost two visual pigments, reducing them to dichromacy; primates subsequently reevolved trichromacy. Studies of mammalian color vision have largely overlooked marsupials despite the wide variety of species and ecological niches and, most importantly, their retention of reptilian retinal features such as oil droplets and double cones. Using microspectrophotometry (MSP), we have investigated the spectral sensitivity of the photoreceptors of two Australian marsupials, the crepuscular, nectivorous honey possum (Tarsipes rostratus) and the arhythmic, insectivorous fat-tailed dunnart (Sminthopsis crassicaudata); these species are representatives of the two major taxonomic divisions of marsupials, the diprotodonts and polyprotodonts, respectively. Here, we report the presence of three spectrally distinct cone photoreceptor types in both species. It is the first evidence for the basis of trichromatic color vision in mammals other than primates. We suggest that Australian marsupials have retained an ancestral visual pigment that has been lost from placental mammals.
The visual pigments in the retinal photoreceptors of 12 species of snappers of the genus Lutjanus (Teleostei; Perciformes; Lutjanidae) were measured by microspectrophotometry. All the species were caught on the Great Barrier Reef (Australia) but differ in the colour of the water in which they live. Some live in the clear blue water of the outer reef, some in the greener water of the middle and inshore reefs and some in the more heavily stained mangrove and estuarine water. All the species had double cones, each member of the pair containing a different visual pigment. Using Baker's and Smith's (1982) model to predict the spectral distribution of ambient light from chlorophyll and dissolved organic matter it was found that the absorption spectra of the visual pigments in the double cones were close to those that confer the maximum sensitivity in the different water types. Single cones contained a blue or violet-sensitive visual pigment. The visual pigments in the rods showed little variation, their wavelength of maximum absorption always being in the region 489-502 nm.
Visual pigments in the rods of 38 species of deep-sea fish were examined by microspectrophotometry. 33 species were found to have a single rhodopsin with a wavelength of maximum absorbance (lambda max) in the range 470-495 nm. Such visual pigments have absorbance maxima close to the wavelengths of maximum spectral transmission of oceanic water. 5 species, however, did not conform to this pattern and visual pigments were found with lambda max values ranging from 451 nm to 539 nm. In 4 of these species two visual pigments were found located in two types of rod. Some 2-pigment species which have unusual red sensitivity, also have red-emitting photophores. These species have both rhodopsin and porphyropsin pigments in their retinae, which was confirmed by HPLC, and the two pigments are apparently located in separate rods in the same retinal area. In deep-sea fishes the occurrence of 'unusual' visual pigments seems to be correlated with aspects of the species' depth ranges. In addition to ecological influences we present evidence, in the form of lambda max spectral clustering, that indicates the degree of molecular constraint imposed on the evolution of visual pigments in the deep-sea.
The morphology and spectral absorption characteristics of the retinal photoreceptors in the southern hemisphere lamprey Geotria australis (Agnatha) were studied using light and electron microscopy and microspectrophotometry. The retinae of both downstream and upstream migrants of Geotria contained two types of cone photoreceptor and one type of rod photoreceptor. Visual pigments contained in the outer segments of these three photoreceptor types had absorbance spectra typical of porphyropsins and with wavelengths of maximum absorbance (downstream/upstream) at 610/616 nm (long-wavelength-sensitive cone, LWS), 515/515 nm (medium-wavelength-sensitive cone, MWS), and 506/500 nm (medium-wavelength-sensitive rod). A "yellow" photostable pigment was present in the myoid region of all three types of photoreceptor in the downstream migrant. The same short-wavelength-absorbing pigment, which prevents photostimulation of the beta band of the visual pigment in the outer segment, was present in the rods and LWS cones of the upstream migrant, but was replaced by a large transparent ellipsosome in the MWS cones. Using microspectrophotometric and anatomical data, the quantal spectral sensitivity of each photoreceptor type was calculated. Our results provide the first evidence of a jawless vertebrate, represented today solely by the lampreys and hagfishes, with two morphologically and physiologically distinct types of cone photoreceptors, in addition to a rod-like photoreceptor containing a colored filter (a cone-like characteristic). In contrast, all other lampreys studied thus far have either (1) one type of cone and one type of rod, or (2) a single type of rod-like photoreceptor. The evolution or retention of a second type of cone in adult Geotria is presumably an adaptation to life in the brightly lit surface waters of the Southern Ocean, where this species lives during the marine phase of its life cycle. The functional significance of the unique visual system of Geotria is discussed in relation to its life cycle and the potential for color vision.
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