N. Thomas

Trichromacy in Australian Marsupials

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 influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri

SUMMARY The 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 wild-caught animals, indicating that the expression of cone opsin genes is also regulated by environmental light.

Retinal characteristics of the ornate dragon lizard, Ctenophorus ornatus

The retina of a diurnal insectivorous lizard, Ctenophorus ornatus (Agamidae) was investigated using microspectrophotometry and light and electron microscopy. A prominent broad yellow band was observed that extended across the mid‐retina. The yellow coloration was found to originate from both oil droplets and diffuse pigmentation within cone inner segments. Microspectrophotometric analysis revealed yellow oil droplets with variable absorption of wavelengths below 520 nm and transparent oil droplets with no detectable absorptance between 350 and 750 nm. Cones with transparent oil droplets lacked the diffuse yellow pigmentation. The mean wavelengths of maximum absorbance of visual pigments in the isolated cone outer segments were at 440, 493, and 571 nm. The retina was found to possess a deep convexiclivate fovea located within the yellow band, slightly dorsotemporal of the retinal midpoint. The topography of the retinal ganglion cells revealed that the fovea was contained within an area centralis. Photoreceptors were either single (80%) or unequal double (20%) cones. Within the region of the fovea, the cones were approximately 20% the diameter of those in the peripheral retina. Colored oil droplets and yellow pigment may increase visual acuity by absorbing short wavelength light scattered either by the atmosphere or the optical structures of the eye. The presence of a fovea containing slender cone photoreceptors and three visual pigments suggests that the lizard has high acuity and the potential for color vision. J. Comp. Neurol. 450:334–344, 2002.

Retinal development of West Australian dhufish, Glaucosoma hebraicum.

An investigation of retinal specializations was carried out in larval and juvenile dhufish, Glaucosoma hebraicum (Glaucosomidae, Teleostei). The development of photoreceptors and formation of the retinal mosaic was followed by light and electron microscopy. At hatching the eye was undifferentiated. Cone photoreceptors were present by day 3 posthatch (dph), when exogenous feeding began. Single and multiple cones were present in a row arrangement from 3 dph to 20 dph, when the first rod nuclei were observed. Between 20 dph and approximately 3 months posthatch (mph), the row arrangement was replaced by a square mosaic of four double cones surrounding a single cone, and the cones increased in size, with the outer segments reaching up to 30 microm in length. During the period of spatial rearrangement, triple cones were often observed. From their first appearance, rod photoreceptors were added rapidly. Investigation of ganglion cell topography in 3-mph fish that had attained the adult-like square photoreceptor mosaic was carried out using retinal wholemounts. The highest densities of neurones in the ganglion cell layer were in temporal retina but no well-defined area centralis was observed. Microspectrophotometric measurements of the visual pigments within the outer segments of the photoreceptors of 3-mph fish revealed double cones with identical absorption spectra in each member of the outer segment, and the wavelength of maximum absorption (lambda(max)) located at 522 nm. Single cones were found to possess a visual pigment with lambda(max) at 460 nm and rods with a lambda(max) of 498 nm. The results imply that the larvae and juveniles are adapted for survival in coastal waters and may be active in relatively low light levels from early stages of development.