Retinal photoreceptor arrangement, SWS1 and LWS opsin sequence, and electroretinography in the South American marsupial Thylamys elegans (Waterhouse, 1839)

Abstract

We studied the retinal photoreceptors in the mouse opossum Thylamys elegans, a nocturnal South American marsupial. A variety of photoreceptor properties and color vision capabilities have been documented in Australian marsupials, and we were interested to establish what similarities and differences this American marsupial showed. Thylamys opsin gene sequencing revealed two cone opsins, a longwave-sensitive (LWS) opsin and a shortwave-sensitive (SWS1) opsin with deduced peak sensitivities at 560 nm and 360 nm (ultraviolet), respectively. Immunocytochemistry located these opsins to separate cone populations, a majority of LWS cones (density range 1,600-5,600/mm(2)) and a minority of SWS1 cones (density range 100-690/mm(2)). With rod densities of 440,000-590,000/mm(2), the cones constituted 0.4-1.2% of the photoreceptors. This is a suitable adaptation to nocturnal vision. Cone densities peaked in a horizontally elongated region ventral to the optic nerve head. In ventral-but not dorsal-retina, roughly 40% of the LWS opsin-expressing cones occurred as close pairs (double cones), and one member of each double cone contained a colorless oil droplet. The corneal electroretinogram (ERG) showed a high scotopic sensitivity with a rod peak sensitivity at 505 nm. At mesopic light levels, the spectral ERG revealed the contributions of a UV-sensitive SWS1 cone mechanism and an LWS cone mechanism with peak sensitivities at 365 nm and 555 nm, respectively, confirming the tuning predictions from the cone opsin sequences. The two spectral cone types provide the basis for dichromatic color vision, or trichromacy if the rods contribute to color processing at mesopic light levels.

Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution

“…The three visual opsins found in therian mammals-short wavelength-sensitive 1 (SWS1), long wavelength-sensitive (LWS) and rod opsin (RH1)-differ in their peak absorption wavelength (l max ), with SWS1 ranging from ultraviolet-sensitive (350-370 nm; UVS) to violet-sensitive (400-457 nm; VS). UVS pigments are typically considered rare in mammals, having been directly measured in only 10 rodents [1][2][3][4][5][6] and four marsupials [7][8][9], although predictions based on SWS1 opsin sequences suggest that UVS pigments may be more widespread [8,[10][11][12][13][14][15][16][17][18][19][20]. The utility of UVS versus VS pigments may be related to the detection of specific stimuli, particularly cues for foraging and communication [21][22][23].…”

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

“…Carleton et al, 2000;Siebeck and Marshall, 2001;Siebeck and Marshall, 2007;Siebeck et al, 2010), data on other vertebrate linages are relatively scant and encompass few species [e.g. amphibians (Govardovskiĭ and Zueva, 1974;Perry and McNaughton, 1991;Takahashi and Yokoyama, 2005), mammals (Jacobs et al, 1991;Winter et al, 2003;Wang et al, 2004;Palacios et al, 2010;Carvalho et al, 2012), turtles (Ventura et al, 1999;Loew and Govardovskiĭ, 2001), crocodiles (Sillman et al, 1991) and Squamata, i.e. lizards and snakes (Fleishman et al, 1997;Fleishman et al, 2011;Sillman et al, 1999;Sillman et al, 2001;Loew et al, 2002)].…”

Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution

“…In conclusion, our work widens our understanding of the evolution of cone-based visual capacities in the Chiroptera and the fact that some species retain cone-based UV vision means that bats are the third mammalian taxon to do so (JACOBS et al 1991, JACOBS et al 2001, ARRESE et al 2006, PALACIOS et al 2010. To further our work, corresponding field investigations are now also required.…”

“…Following methods used for the demonstration of possible cone-based pathways (JACOBS et al 1991, AMIR & ROBINSON 1996, JACOBS et al 2001, ARRESE et al 2006, PALACIOS et al 2010, only behavioral studies can confirm proposed UV vision (JACOBS 1993, GRIEBEL & PEICHL 2003. Classical fear conditioning occurs when an affectively neutral stimulus (conditioned stimulus -CS) is paired with a noxious aversive stimulus (unconditioned stimulus -US) such as footshock (WALKER et al 2002).…”