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Adaptive differences in the structure and macromolecular compositions of the air and water corneas of the "four-eyed" fish (Anableps anableps)

SHIVALINGAPPA K. SWAMYNATHAN^*, MARY A. CRAWFORD, W. GERALD ROBISON, JR, JYOTSHNABALA KANUNGO^* and JORAM PIATIGORSKY^*,1

^* Laboratory of Molecular and Developmental Biology,
Laboratory of Immunology,
Laboratory of Mechanisms of Ocular Diseases, National Eye Institute, NIH, Bethesda, Maryland, USA

¹Correspondence: Laboratory of Molecular and Developmental Biology, National Eye Institute, National Institutes of Health, 7 Memorial Dr., Bldg. 7, Room 100A, Bethesda, MD 20892, USA. E-mail: joramp{at}nei.nih.gov

The water meniscus bisects the eyes of the "four-eyed" fish Anableps anableps, resulting in simultaneous vision in air and water. We compare the structure and macromolecular compositions of the Anableps dorsal (air) and ventral (water) corneas with the fully aquatic zebrafish cornea. The Anableps dorsal corneal epithelium is thicker (>20 cell layers), flatter (1.94 mm radius of curvature), and contains 15-fold more glycogen (0.16 µg/µg water-soluble protein) than the ventral corneal epithelium (5–7 cell layers; 1.63 mm radius of curvature; 0.01 µg glycogen/µg water-soluble protein), which resembles the zebrafish corneal epithelium. Gelsolin is the major water-soluble protein in the zebrafish (50%) and Anableps dorsal (38%) and ventral (21%) corneal epithelia, suggesting that gelsolin was recruited for high corneal expression before these two species diverged at least 100 million years ago and that abundant corneal gelsolin is not limited to aquatic vision. Anableps gelsolin, deduced from its cDNA, is 57% identical to zebrafish gelsolin. Paucity of Anableps corneal F-actin (consistent with high gelsolin) was confirmed by the absence of rhodamine-phalloidin staining. We suggest amphibious refraction and protection from UV irradiation and desiccation in air as selective constraints for the specializations of the Anableps dorsal cornea.—Swamynathan, S. K., Crawford, M. A., Robison, W. G., Jr., Kanungo, J., Piatigorsky, J. Adaptive differences in the structure and macromolecular compositions of the air and water corneas of the "four-eyed" fish (Anableps anableps).

Key Words: amphibious vision • gelsolin • crystallin

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