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

Abstract

Uniquely for non-primate mammals, three classes of cone photoreceptors have been previously identified by microspectrophotometry in two marsupial species: the polyprotodont fat-tailed dunnart (Sminthopsis crassicaudata) and the diprotodont honey possum (Tarsipes rostratus). This report focuses on the genetic basis for these three pigments. Two cone pigments were amplified from retinal cDNA of both species and identified by phylogenetics as members of the short wavelength-sensitive 1 (SWS1) and long wavelengthsensitive (LWS) opsin classes. In vitro expression of the two sequences from the fat-tailed dunnart confirmed the peak absorbances at 363 nm in the UV for the SWS1 pigment and 533 nm for the LWS pigment. No additional expressed cone opsin sequences that could account for the middle wavelength cones could be amplified. However, amplification from the fat-tailed dunnart genomic DNA with RH1 (rod) opsin primer pairs identified two genes with identical coding regions but sequence differences in introns 2 and 3. Uniquely therefore for a mammal, the fat-tailed dunnart has two copies of an RH1 opsin gene. This raises the possibility that the middle wavelength cones express a rod rather than a cone pigment.

New perspectives on anthropoid origins

“…The most recent genetic data suggest that such "polymorphic trichromacy" has evolved multiple times among diurnal and cathemeral lemuriform primates as well (86,87), although the functionality of color vision in lemurs needs to be more fully explored (88). Similarly, studies of Australian marsupials suggest that many are routine trichromats like catarrhine primates (89). These data reveal that excellent color vision based on the presence of three cone types is not as rare among mammals as was recently thought.…”

Evolution and spectral tuning of visual pigments in birds and mammals

“…This was first reported for the fat-tailed dunnart, Sminthopsis crassicaudata, and the honey possum, Tarsipes rostratus (Arrese et al 2002), and subsequently extended to the quokka, Setonix brachyurus, and quenda or bandicoot, Isoodon obesulus (Arrese et al 2005). Attempts, however, to identify this third cone pigment have failed, despite extensive efforts in two laboratories (Strachan et al 2004;Cowing et al 2008). A second rod Rh1 pigment gene was however identified in the genome of the fattailed dunnart by Cowing et al (2008), and these authors have advanced the hypothesis that M cones express a rod pigment.…”

Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments

“…However, an examination of these sites in the VS pigments of different primate species shows that only Pro93 is fully conserved across all primate groups (table 1). The other sites show variation in the amino acid present, and there are several instances where the residue present in the UVS pigments of certain rodents [35] and marsupials [14] is also found in primate VS pigments. If, as seems likely, a single tuning mechanism is responsible for the VS of all primate SWS1 pigments, then the only consistent feature to account for this is Pro93.…”

“…To examine this further, the eight different residues found at site 86 in primate SWS1 opsins, together with the corresponding codon sequences, were mapped onto the primate phylogeny reported recently by Perelman et al [36], together with the tree shrew as the species most closely related to primates for which spectral [37] and sequence data (GenBank accession number EU487780) are available (figure 2). The ancestral Phe residue, as found in nonprimate mammalian UVS pigments [14,15,35,38], is encoded by TTC, which is also found in the aye-aye. This codon differs, however, in the SWS1 gene of all other primates.…”