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The Visual Pigments of Diving Tetrapods: Genetic and Electroretinographic Investigations of Pinnipeds, Cetaceans, Sea Turtles, and Penguins

Abstract

To evaluate how terrestrially descended, marine-living tetrapods have adapted their vision for life in the ocean environment, the rod and cone visual pigments of diving turtles, birds, and mammals were examined. Genetics was used primarily. When possible, in situ electroretinography (ERG) was also used.

Of the three visual pigments possessed by most mammals, cetacean rod and middle/long-wavelength sensitive (M/L) cone visual pigments had previously been shown to be shifted towards the wavelengths (λ) of light that predominant in marine habits, λ~475 nm. The genetic sequences of the short-wavelength sensitive (S) cones of numerous cetaceans were examined from nuclear DNA. The distribution of mis­-sense mutations found in their S cone opsin genes indicates that all members ofthe cetacean order lack S cones. Genetic evaluation of the retinal mRNA of seven pinniped species revealed that these mammals also lack S cones. The convergent loss of S cones in pinnipeds and cetaceans suggests that this loss may be adaptive for vision in the marine environment. Rod and M/L cone pigments of pinnipeds were also examined. In contrast to the cetaceans, one pinniped, the deep-diving northern elephant seal was found to possess a short-wavelength-shifted visual pigment, its rod pigment. The rod and M/L cone visual pigments of the other pinnipeds were similar to those of terrestrial carnivores. An ERG investigation of three pinnipeds including the elephant seal supported the genetic results.

Finally, the rod visual pigments of five sea turtle and three penguin species were examined with genetics. None was found to be markedly marine-adapted. Additional examination of cone sensitivity in sea turtles with ERG indicated limited departure from the terrestrial condition. Clearly, the cetaceans are the most marine adapted ofthe groups examined. The pinnipeds and sea turtles showed limited adaptation, and the penguins were not apparently different from terrestrial birds. As the cetaceans are the only completely aquatic lineage among these groups, it seems that the terrestrial life-stage may still be of selective significance to some or all of the other groups. Particularly in the case of the sea turtles and penguins, which are highly photopic by ancestry, phylogenetic inertia may also limit the plasticity of the visual systems in adapting for vision in the marine environment.

XIV

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