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Cone visual pigments of aquatic mammals

Published online by Cambridge University Press:  03 February 2006

LUCY A. NEWMAN
Affiliation:
Department of Biological Sciences, University of Maryland—Baltimore County, Baltimore, Maryland Present address: Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD 21201
PHYLLIS R. ROBINSON
Affiliation:
Department of Biological Sciences, University of Maryland—Baltimore County, Baltimore, Maryland

Abstract

It has long been hypothesized that the visual systems of animals are evolutionarily adapted to their visual environment. The entrance many millions of years ago of mammals into the sea gave these new aquatic mammals completely novel visual surroundings with respect to light availability and predominant wavelengths. This study examines the cone opsins of marine mammals, hypothesizing, based on previous studies [Fasick et al. (1998) and Levenson & Dizon (2003)], that the deep-dwelling marine mammals would not have color vision because the pressure to maintain color vision in the dark monochromatic ocean environment has been relaxed. Short-wavelength-sensitive (SWS) and long-wavelength-sensitive (LWS) cone opsin genes from two orders (Cetacea and Sirenia) and an additional suborder (Pinnipedia) of aquatic mammals were amplified from genomic DNA (for SWS) and cDNA (for LWS) by PCR, cloned, and sequenced. All animals studied from the order Cetacea have SWS pseudogenes, whereas a representative from the order Sirenia has an intact SWS gene, for which the corresponding mRNA was found in the retina. One of the pinnipeds studied (harp seal) has an SWS pseudogene, while another species (harbor seal) appeared to have an intact SWS gene. However, no SWS cone opsin mRNA was found in the harbor seal retina, suggesting a promoter or splice site mutation preventing transcription of the gene. The LWS opsins from the different species were expressed in mammalian cells and reconstituted with the 11-cis-retinal chromophore in order to determine maximal absorption wavelengths (λmax) for each. The deeper dwelling Cetacean species had blue shifted λmax values compared to shallower-dwelling aquatic species. Taken together, these findings support the hypothesis that in the monochromatic oceanic habitat, the pressure to maintain color vision has been relaxed and mutations are retained in the SWS genes, resulting in pseudogenes. Additionally, LWS opsins are retained in the retina and, in deeper-dwelling animals, are blue shifted in λmax.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Asenjo, A.B., Rim, J., & Oprian, D.D. (1994). Molecular determinants of human red/green color discrimination. Neuron 12, 11311138.CrossRefGoogle Scholar
Fasick, J.I., Cronin, T.W., Hunt, D.M., & Robinson, P.R. (1998). The visual pigments of the bottlenose dolphin (Tursiops truncatus). Visual Neuroscience 15, 643651.Google Scholar
Fasick, J.I. & Robinson, P.R. (1998). Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37, 433438.CrossRefGoogle Scholar
Fasick, J.I. & Robinson, P.R. (2000). Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Visual Neuroscience 17, 781788.CrossRefGoogle Scholar
Hunt, D.M., Dulai, K.S., Partridge, J.C., Cottrill, P., & Bowmaker, J.K. (2001). The molecular basis for spectral tuning of rod visual pigments in deep-sea fish. Journal of Experimental Biology 204, 33333344.Google Scholar
Jacobs, G.H., Deegan, J.F., Neitz, J., Crognale, M.A., & Neitz, M. (1993). Photopigments and color vision in the nocturnal monkey, Aotus. Vision Research 33, 17731783.CrossRefGoogle Scholar
Jacobs, G.H., Neitz, M., & Neitz, J. (1996). Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proceedings of the Royal Society B (London) 263, 705710.CrossRefGoogle Scholar
Kazmi, M.A., Dubin, R.A., Oddoux, C., & Ostrer, H. (1996). High-level inducible expression of visual pigments in transfected cells. Biotechniques 21, 304311.Google Scholar
Levenson, D.H. & Dizon, A. (2003). Genetic evidence for the ancestral loss of short-wavelength-sensitive cone pigments in mysticete and odontocete cetaceans. Proceedings of the Royal Society B (London) 270, 673679.CrossRefGoogle Scholar
Oprian, D.D., Asenjo, A.B., Lee, N., & Pelletier, S.L. (1991). Design, chemical synthesis, and expression of genes for the three human color vision pigments. Biochemistry 30, 1136711372.CrossRefGoogle Scholar
Peichl, L. & Moutairou, K. (1998). Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). European Journal of Neuroscience 10, 25862594.CrossRefGoogle Scholar
Peichl, L., Behrmann, G., & Kroger, R.H.H. (2001). For whales and seals the ocean is not blue: A visual pigment loss in marine mammals. European Journal of Neuroscience 13, 15201528.CrossRefGoogle Scholar
Robinson, P.R., Griffith, K., Gross, J.M., & O'neill, M.C. (1999). A back-propagation neural network predicts absorption maxima of chimeric human red/green visual pigments. Vision Research 39, 17071712.CrossRefGoogle Scholar
Sun, H., Macke, J.P., & Nathans, J. (1997). Mechanisms of spectral tuning in the mouse green cone pigment. Proceedings of the National Academy of Sciences of the U.S.A. 94, 88608865.CrossRefGoogle Scholar
Weitz, C.J., Miyake, Y., Shinzato, K., Montag, E., Zrenner, E., Went, L.N., & Nathans, J. (1992). Human tritanopia associated with two amino acid substitutions in the blue-sensitive opsin. American Journal of Human Genetics 50, 498507.Google Scholar