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Pinnipeds, Polar Bear, and Sea Otter

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Pinnipeds, Polar Bear, and Sea Otter UC San Diego UC San Diego Previously Published Works Title Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter Permalink https://escholarship.org/uc/item/8sg757mn Journal Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology, 192(8) ISSN 0340-7594 Authors Levenson, D H Ponganis, P J Crognale, M A et al. Publication Date 2006-08-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California J Comp Physiol A (2006) 192: 833–843 DOI 10.1007/s00359-006-0121-x ORIGINAL PAPER David H. Levenson Æ Paul J. Ponganis Michael A. Crognale Æ Jess F. Deegan II Andy Dizon Æ Gerald H. Jacobs Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter Received: 2 December 2005 / Revised: 27 February 2006 / Accepted: 4 March 2006 / Published online: 30 March 2006 Ó Springer-Verlag 2006 Abstract Rod and cone visual pigments of 11 marine the use of conditions previously shown to evoke cone carnivores were evaluated. Rod, middle/long-wave- responses in other mammals, no cone responses could be length sensitive (M/L) cone, and short-wavelength sen- elicited from any of these pinnipeds. Rod photoreceptor sitive (S) cone opsin (if present) sequences were obtained responses for all three species were as predicted by the from retinal mRNA. Spectral sensitivity was inferred genetic data. through evaluation of known spectral tuning residues. The rod pigments of all but one of the pinnipeds were Keywords Pinnipeds Æ Polar bear Æ Sea otter Æ Visual similar to those of the sea otter, polar bear, and most pigments Æ Opsins other terrestrial carnivores with spectral peak sensitivi- ties (kmax) of 499 or 501 nm. Similarly, the M/L cone pigments of the pinnipeds, polar bear, and otter had Introduction inferred kmax of 545 to 560 nm. Only the rod opsin se- quence of the elephant seal had sensitivity characteristic Pinnipeds, a sub-group of the order Carnivora, are un- of adaptation for vision in the marine environment, with ique among mammals in that they are the only large an inferred kmax of 487 nm. No evidence of S cones was monophyletic lineage that is distinctly amphibious. This found for any of the pinnipeds. The polar bear and otter makes them particularly interesting from an evolution- had S cones with inferred kmax of 440 nm. Flicker- ary standpoint in that they represent an intermediate photometric ERG was additionally used to examine the stage between terrestrial and aquatic adaptation. Vision in situ sensitivities of three species of pinniped. Despite is important for pinnipeds, both on land and in water (Schusterman et al. 2000), and there is clear anatomical Electronic Supplementary Material Supplementary material is evidence (e.g., round lens, flattened cornea) that their available for this article at http://dx.doi.org/10.1007/s00359-006- visual systems are markedly evolved from those of their 0121-x and is accessible for authorized users. terrestrial ancestors to enable them to function more D. H. Levenson (&) Æ P. J. Ponganis effectively in these two diverse media (Walls 1942; Scripps Institution of Oceanography, Lavigne et al. 1977). Among the features of the visual UCSD, La Jolla, CA, USA system that may provide a good index for evaluating the E-mail: [email protected] nature and extent of the amphibious adaptation of Tel.: +1-760-2301620 Fax: +1-858-5467003 pinnipeds are the visual pigments. These are often clo- sely correlated with the visual environment, particularly A. Dizon Æ D. H. Levenson in marine habitats, where visual conditions may vary Southwest Fisheries Science Center, NMFS, dramatically (Bowmaker 1995; Hunt et al. 1996; Fasick La Jolla, CA, USA and Robinson 2000). M. A. Crognale Three classes of visual pigments are typically present Department of Psychology, University of Nevada, Reno, in mammalian retinas, each characterized by an under- NV, USA lying opsin protein: rod opsin found in the rod photo- J. F. Deegan II receptors, and two opsin types found in the cone Department of Psychology, California State University, photoreceptors, the short wavelength (S) and middle/ Bakersfield, CA, USA long wavelength (M/L) sensitive cone opsins (Yokoy- ama and Yokoyama 1996). While only three opsin G. H. Jacobs classes exist, alterations in the primary structures of Neuroscience Research Institute, University of California, Santa Barbara, CA, USA individual opsins within these classes can tune the 834 spectral sensitivity of the corresponding visual pigments additional species, P. vitulina, were also examined for over a wide range of wavelengths. The effects of these the presence of S cones and published M/L sequences changes are increasingly better understood allowing one for P. vitulina and P. groenlandicus were used to infer to infer the spectral sensitivity of a visual pigment from their spectral sensitivity. the translated genetic sequence of the opsin (Fasick and Eyes used for molecular analysis were obtained from Robinson 2000; Yokoyama and Radlwimmer 2001; Shi animals that had died of natural causes or that had been and Yokoyama 2003). euthanized in captivity or wildlife rehabilitation facilities Evidence suggests that pinniped visual pigments are as a consequence of terminal illness/injury. Samples were different from those of terrestrial carnivores. Although collected as soon as possible after death and subsequently some of these animals have rod pigments similar to those kept frozen at À20°C or colder. To obtain retinal of terrestrial mammals (Crescitelli 1958; Lavigne and mRNA, each eye was thawed, the excised retinal tissue Ronald 1975), some deep-diving species have been was homogenized in Trizol (Gibco BRL, Rockville, MD; shown to have modified rod pigments that provide in- 1 ml/100 mg of tissue) and RNA was extracted and creased sensitivity to the blue-green wavelengths of light precipitated with chloroform and isopropanol. Extracted that predominate in deep ocean water, k475 nm samples were incubated in DNase I (Ambion, Austin, (Lythgoe and Dartnall 1970; Kirk 1994; Southall et al. TX, USA) at 37°C for 45 min to eliminate any DNA 2002). There is also evidence that the cone visual pig- contamination. The purified mRNA was then converted ments of some pinnipeds have been modified for use in to cDNA by incubating 50 ng with MMLV reverse- the marine environment. Although most mammals transcriptase (Clontech/BD Biosciences, Palo Alto, CA, possess two distinct cone pigment types (Jacobs 1993; USA), oligonucleotide (dt)18 primer, and excess dNTPs Yokoyama and Yokoyama 1996), several pinniped for 60 min at 42°C. Nonretinal, nuclear DNA was species have been found to possess only M/L cones obtained for P. vitulina from skin using a lithium–chloride (Peichl and Moutairou 1998; Peichl et al. 2001; Griebel extraction and ethanol precipitation procedure (Hillis and Peichl 2003). At present, the only large group of et al. 1996). mammals known to uniformly lack S cones is the Rod and cone opsin gene sequences were amplified exclusively aquatic cetaceans (Levenson and Dizon and sequenced from the cDNA using polymerase chain 2003). Available information on the M/L cones of reaction (PCR) and dideoxy-terminator cycle sequenc- pinnipeds is limited, and equivocal. In ERG experi- ing (Sanger et al. 1977). An attempt was made to amplify ments, the harbor seal (Phoca vitulina) had peak spectral and sequence rod, M/L, and S cone opsins from the sensitivity near 510 nm (Crognale et al. 1998). A retinal cDNA of every individual examined. Oligonu- behavioral evaluation of the harp seal (Pagophilus cleotide primers for PCR and sequencing were 15–23 groenlandicus) also reported a peak in spectral sensitivity base pairs (bp) in length and were designed from between 500 and 525 nm, as well as a second peak near homologous gene sequences obtained from Genbank of 550 nm (Lavigne and Ronald 1972; Lavigne et al. 1977). cow, dog, cat, and harbor seal (see Table 1, Fig. 1). Although these data provide some evidence sugges- Some PCR primers for the S cone opsin were addi- tive of adaptation for aquatic vision in the photopig- tionally optimized using the pinniped sequence obtained ments of pinnipeds, further evaluation of additional from nuclear DNA. For each opsin gene, two pairs of species is necessary to better understand the nature of forward and reverse primers were used to obtain two their amphibious adaptation. Towards this end, we have overlapping 400–650 bp sequence fragments. Primer used molecular genetic methods to examine the opsin annealing locations were chosen so that the consensus of proteins underlying the rod, S cone, and M/L cone the two fragments would provide sequence data for photoreceptor pigments of numerous species represent- nearly the entire gene, including all of the currently de- ing all three pinniped families. For comparative pur- scribed spectral tuning sites for each opsin. Studies poses, opsins of the sea otter (Enhydra lutris) and the indicate that variability in the distal portions of the N polar bear (Ursus maritimus) were also examined. and C-terminal regions of the opsin protein are unlikely Finally, flicker-photometric electroretinography (ERG) to affect its spectral properties and so they were not was used to compare in situ spectral sensitivity with that evaluated (Hargrave 1982; Hunt et al. 2001; Shi and predicted from the genetic data. Yokoyama 2003). Each 50 ll PCR reaction consisted of 5 ll of cDNA (100 ng), 36 ll of water, 5 llof10·PCR buffer with Methods MgCl2 (2.0 mM), 1 ll of each oligonucleotide primer (10 lM), and 1 llofTaq DNA polymerase. For Genetic evaluation of rod and cone visual pigments amplification, reactions were initially denatured for 5 min at 94°C and then cycled 35 times through the To evaluate the visual pigments expressed in the retinas following conditions: denature for 45 s (94°C), anneal of some marine carnivores, rod and cone opsin sequence for 1 min (55°C), and extend for 1.5 min (72°C).
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