Trichromacy in Australian Marsupials

Abstract

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.

Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus)

“…However, in this study, no data were presented that enabled these sequences to be correlated with the different cone classes identified by MSP (Arrese et al 2002). It remained uncertain therefore whether the SWS1 sequence encoded a UVS pigment and the LWS gene encoded the MWS or LWS pigment.…”

“…and 509 nm, respectively, in the fat-tailed dunnart and 502 and 505 nm, respectively, in the honey possum (Arrese et al 2002). It would also account for the similar photochemical properties of the rods and MWS cones with a post-bleach build-up of photoproduct that absorbed below 430 nm (Arrese et al 2002).…”

“…It would also account for the similar photochemical properties of the rods and MWS cones with a post-bleach build-up of photoproduct that absorbed below 430 nm (Arrese et al 2002). Unfortunately, in the absence of any differences in the coding exons, it is not possible to confirm that both gene copies are expressed or to demonstrate that mRNA from one copy is present in cones and the other in rods.…”

Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity

“…Usually, the oil droplet completely covers the entrance aperture of the outer segment, and most of the incident light passes through it before reaching the visual pigment (Wortel and Nuboer, 1986). The oil droplets found in the photoreceptors of some species of chondrostean fishes (Walls and Judd, 1933), anuran amphibians (Hailman, 1976), geckos (Ellingson et al, 1995), monotremes (Walls, 1942) and marsupials (O'Day, 1935;Arrese et al, 2002;Arrese et al, 2005) do not have obvious pigmentation. The cone oil droplets of birds, turtles, lizards and the Australian lungfish, however, have a pale green, greenish yellow, golden yellow or ruby red colouration, depending on the spectral identity of the cone and the species (Walls and Judd, 1933;Robinson, 1994;Bailes et al, 2006).…”

Cone opsins and response of female chamois (Rupicapra rupicapra) to differently coloured raincoats

“…Immunohistochemistry allows a straightforward approach to test whether eyes at least have the photoreceptor cells necessary to detect colour (e.g. Hemmi and Grünert 1999;Dkhissi-Benyahya et al 2001;Arrese et al 2003a). Whereas rods are responsible for perceiving differences in brightness and for monochromatic vision in low light levels (Kaskan et al 2005), two or more cones are necessary to enable colour vision.…”