Ultrastructural changes associated with loss of transparency in the primary spectacle and cornea of spawning sea lamprey

Pederson, Harlan J.; Horn, Diane L. Van; Edelhauser, Henry F.

doi:10.1016/0014-4835(71)90139-4

Cited by 10 publications

(21 citation statements)

References 7 publications

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“…The surface holes in the epithelium of the dermal cornea of Geotria australis appear to be a characteristic feature in high abundance with an inverse relationship between the size of the holes and the size of the epithelial cells. The presence of these holes has been previously reported for the Pouched lamprey Geotria australis ( Collin and Collin, 2000a , 2006 ), the Shorthead lamprey, Mordacia mordax ( Collin and Collin, 2006 ), the ammocoete stage ( Dickson et al, 1982 ), but not the adult stage, of the Sea lamprey ( Petromyzon marinus ) ( Van Horn et al, 1969a ; Pederson et al, 1971 ; Dickson et al, 1982 ), the Black shark, Dalatias licha ( Collin and Collin, 2000b , 2006 ), and the Australian lungfish, Neoceratodus forsteri ( Collin and Collin, 2006 ). Surface holes also occur in the pre-metamorphic Axolotl, Ambystoma mexicanum ( Collin and Collin , 2000b , 2006 , 2021a ) but have almost completely disappeared in the post-metamorphic stage ( Collin and Collin, 2021a ).…”

Section: Discussionmentioning

confidence: 64%

“…The eyes of humans, mammals and birds have only one cornea, while some other vertebrates possess two corneas. A primary spectacle (or dermal cornea) and a scleral cornea are found in lampreys ( Walls, 1942 ), including, G. australis (this study), the Sea lamprey, Petroymyzon marinus ( Van Horn et al, 1969a , b ; Pederson et al, 1971 ), the European river lamprey, Lampetra fluviatilis ( Dickson and Graves, 1981 ; Dickson et al, 1982 ) and tadpoles and aquatic adult amphibians ( Walls, 1942 ). The formation of a primary spectacle occurs when the superficial layers of the cornea derived from the surface ectoderm (primary spectacle) do not fuse with the deeper layers of mesodermal origin (scleral cornea) ( Pederson et al, 1971 ).…”

Section: Discussionmentioning

confidence: 64%

“…A primary spectacle (or dermal cornea) and a scleral cornea are found in lampreys ( Walls, 1942 ), including, G. australis (this study), the Sea lamprey, Petroymyzon marinus ( Van Horn et al, 1969a , b ; Pederson et al, 1971 ), the European river lamprey, Lampetra fluviatilis ( Dickson and Graves, 1981 ; Dickson et al, 1982 ) and tadpoles and aquatic adult amphibians ( Walls, 1942 ). The formation of a primary spectacle occurs when the superficial layers of the cornea derived from the surface ectoderm (primary spectacle) do not fuse with the deeper layers of mesodermal origin (scleral cornea) ( Pederson et al, 1971 ). A similar arrangement may also occur in bottom-dwelling fishes, where dermal and scleral corneas have been reported, i.e., in the Salamanderfish Lepidogalalaxias salamandroides ( Collin and Collin, 1996 ) and the Pipefish, Corythoichthyes paxtoni ( Collin and Collin, 1995 ) and both mudskippers ( Periophthalmus spp.)…”

Section: Discussionmentioning

confidence: 64%

“…The split corneas of the Northern hemisphere lampreys including the Sea lamprey, Petromyzon marinus ( Van Horn et al, 1969a , b ; Pederson et al, 1971 ) and the European river lamprey, Lampetra fluviatilis ( Dickson and Graves, 1981 ) have previously been described. The dermal cornea is thick with a layer of stratified squamous epithelial cells overlying a stroma of collagen lamellae, many of which are linked by sutural fibres that inhibit swelling and prevent the loss of transparency during environmental changes ( Van Horn et al, 1969b ; Pederson et al, 1971 ). A mucoid layer bounded by mesodermal layers of cells, overlies a scleral cornea with a stroma that lacks fibroblasts and a posterior layer of endothelial cells.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The Functional Anatomy of the Cornea and Anterior Chamber in Lampreys: Insights From the Pouched Lamprey, Geotria australis (Geotriidae, Agnatha)

2021

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Extant lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes or agnathans, and are therefore of critical importance to our understanding of vertebrate evolution. Anadromous lampreys undergo a protracted lifecycle, which includes metamorphosis from a larval ammocoete stage to an adult that moves between freshwater and saltwater with exposure to a range of lighting conditions. Previous studies have revealed that photoreception differs radically across the three extant families with the Pouched lamprey Geotria australis possessing a complex retina with the potential for pentachromacy. This study investigates the functional morphology of the cornea and anterior chamber of G. australis, which is specialised compared to its northern hemisphere counterparts. Using light microscopy, scanning and transmission electron microscopy and microcomputed tomography, the cornea is found to be split into a primary spectacle (dermal cornea) and a scleral cornea (continuous with the scleral eyecup), separated by a mucoid layer bounded on each side by a basement membrane. A number of other specialisations are described including mucin-secreting epithelial cells and microholes, four types of stromal sutures for the inhibition of stromal swelling, abundant anastomosing and branching of collagen lamellae, and a scleral endothelium bounded by basement membranes. The structure and function of the cornea including an annular and possibly a pectinate ligament and iris are discussed in the context of the evolution of the eye in vertebrates.

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Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 64%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The Functional Anatomy of the Cornea and Anterior Chamber in Lampreys: Insights From the Pouched Lamprey, Geotria australis (Geotriidae, Agnatha)

2021

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“…The fact that gelsolin is the major water-soluble corneal protein of Anableps indicates that the recruitment of gelsolin as a major corneal protein in fish occurred at least 100 million years ago, the time of divergence between zebrafish and Anableps (24,25). It would be of interest to determine whether gelsolin is also a dominant protein in the ancient sea lamprey primary spectacle (dermal cornea), which appears generally similar to the cornea of fish and higher vertebrates (26,27).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2003

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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.

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The corneal epithelial surface in the eyes of vertebrates: Environmental and evolutionary influences on structure and function

Collin

2005

Journal of Morphology

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The smooth optical surface of the cornea is maintained by a tear film, which adheres to a variety of microprojections. These microprojections increase the cell surface area and are thought to improve the movement of oxygen, nutrients, and metabolic products across the outer cell membranes. However, little is known of these structural adaptations in vertebrates inhabiting different environments. This field emission scanning electron microscopic study examined the cell density and surface structure of corneal epithelial cells across 51 representative species of all vertebrate classes from a large range of habitats (aquatic, amphibious, terrestrial, and aerial). In particular, we wished to extend the range of vertebrates to include agnathans and some uniquely Australian species, such as the Australian lungfish (Neoceratodus forsteri), the Australian galah (Eolophus roseicapillus), the Australian koala (Phascolarctos cinereus), and the rat-tailed dunnart (Sminthopsis crassicaudata). Epithelial cell densities ranged from 28,860 +/- 9,214 cells mm(-2) in the flathead sole Hippoglossoides elassodon (a marine teleost) to 2,126 +/- 713 cells mm(-2) in the Australian koala (a terrestrial mammal), which may indicate a reduction in osmotic stress across the corneal surface. A similar reduction in cell density occurred from marine to estuarine to freshwater species. The structure and occurrence of microholes, microplicae, microridges, and microvilli are also described with respect to the demands placed on the cornea in different environments. All species that spend significant periods out of an aquatic environment possess microvilli and/or microplicae. These include all of our species of Mammalia, Aves, Reptilia, Amphibia, and even one species of Teleostei (Australian lungfish). Well-developed microridges occur only in teleosts in high osmolarity environments such as marine or estuarine habitats. Clear interspecific differences in corneal surface structure suggest a degree of adaptive plasticity, in addition to some phylogenetic trends.

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Ultrastructural changes associated with loss of transparency in the primary spectacle and cornea of spawning sea lamprey

Cited by 10 publications

References 7 publications

The Functional Anatomy of the Cornea and Anterior Chamber in Lampreys: Insights From the Pouched Lamprey, Geotria australis (Geotriidae, Agnatha)

The Functional Anatomy of the Cornea and Anterior Chamber in Lampreys: Insights From the Pouched Lamprey, Geotria australis (Geotriidae, Agnatha)

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

The corneal epithelial surface in the eyes of vertebrates: Environmental and evolutionary influences on structure and function

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