Adaptive differences in the structure and macromolecular compositions of the air and water corneas of the “four‐eyed” fish (Anableps anableps)

Abstract

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 (approximately 1.94 mm radius of curvature), and contains approximately 15-fold more glycogen (0.16 microg/microg water-soluble protein) than the ventral corneal epithelium (5-7 cell layers; approximately 1.63 mm radius of curvature; 0.01 microg glycogen/microg water-soluble protein), which resembles the zebrafish corneal epithelium. Gelsolin is the major water-soluble protein in the zebrafish (approximately 50%) and Anableps dorsal (approximately 38%) and ventral (approximately 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.

Corneal crystallins and the development of cellular transparency

“…Since the corneal epithelium and the lens are both derived from ectoderm, it seems reasonable to propose that the evolution of transparency in these two structures may have co-evolved as an integrated 'refracton' unit. Indeed, data showing that the corneas from a diverse range of species including squid, fish, frogs, crocodiles, birds and mammals abundantly express a few water-soluble proteins is consistent with this theory [6,7,[9][10][11]13]. However, the vast majority of studies identifying corneal crystallin expression have used total corneal extracts or isolated corneal epithelium.…”

“…Later studies have identified BCP54 as aldehyde dehydrogenase 3A1 [4,5] that comprises from 20-40% of the total water-soluble protein content of the bovine corneal epithelium. More recent studies have shown that unlike non-transparent tissues and organs other than lens, the corneas from a wide range of species abundantly express a few water-soluble enzyme/proteins (Table 1) [3,[6][7][8][9][10][11][12][13][14], many of which are identical to the abundantly expressed taxon-specific lens crystallins, including aldehyde dehydrogenase 1A1 (ALDH1A1)/η-crystallin, α-enolase/τ-crystallin, glutathione-S-transferase/Ω-crystallin, lactic dehydrogenase/ε-crystallin, glyceraldehyde-3-phosphate dehydrogenase (G3PDH)/π-crystallin, and arginino-succinate lyase/δ-crystallin [6,8]. Interestingly, several of these corneal enzyme/proteins are abundantly expressed in the lens of the same species, notably argininosuccinate lyase/δ-crystallin in the chicken and glutathione-S-transferase/Ω-crystallin in the squid.…”

Morphogenesis of the anterior segment in the zebrafish eye

“…At the peripheral limbal region, the stroma splits into multiple layers. Just beneath the stroma is a single layer of cells overlying a second, thinner stromal layer with similar collagen organization (Figure 3K, [15]). Subjacent to these cells, an additional collagen-rich extracellular layer can be seen with electron microscopy (Descemet's membrane).…”

The visual system of zebrafish and its use to model human ocular Diseases

“…Like other vertebrates, the zebrafish cornea is avascular. The adult zebrafish cornea has been characterized histologically and ultrastructurally (Swamynathan et al, 2003; Soules and Link, 2005; Zhao et al, 2006; Akhtar et al, 2008). When mature, it is approximately 20 microns thick.…”