Corneal splitting in the developing lamprey Petromyzon marinus L. eye

Abstract

The cornea of the adult lamprey has both dermal (spectacle) and scleral components. These are separated by a thin mucoid layer that allows free movement of the globe. This study has shown that during the larval (ammocoete) stage, the lamprey cornea develops in a manner similar to that of other lower vertebrates. Just prior to the period of transformation to the adult parasite, the outer dermal portion of the ammocoete cornea (spectacle) consists of an anterior stratified columnar epithelium with goblet cells at the surface. The stroma of the dermal cornea consists of a thick outer layer of orthogonally oriented collagen with branching fibroblasts and a thin, loosely organized inner layer with slender elongated fibroblasts. The scleral cornea is lined internally by a flattened monolayer of mesodermal cells, the corneal endothelium. Its narrow stroma is composed entirely of thin, orthogonally arranged, collagen-fiber lamellae, and is bounded externally by a thin continuous mesothelial layer of cells that abuts directly onto the loose stromal component of the dermal cornea. During the early stages of transformation, the anterior epithelium of the dermal cornea becomes stratified squamous in type. Later, the inner loose stroma of the dermal cornea (spectacle) begins to separate from the scleral cornea components, and a third complete mesothelial layer forms a distinct inner border for the dermal cornea. A mucoid layer is formed between the dermal (spectacle) and scleral corneas and remains throughout the adult life.

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

“…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 ).…”

“…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 ).…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…Throughout the larval stage, the lateral eye is beneath a non‐transparent skin and has a flattened immature lens, indicating that it cannot function in image‐forming (Kleerekoper, ). During metamorphosis, the skin around the eye (the cornea, which has both dermal and scleral components in the adult, see Dickson, Graves & Moyles, ) becomes transparent, so the eye becomes visible. In this period, many neurons differentiate as described below.…”

Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup

“…This is broadly the same order as that in which the jawed-vertebrate retina differentiates 54 (see below), although the ammocoete retina differentiates much more slowly. At metamorphosis, the lamprey eye grows considerably in size, the retina differentiates fully, the lens develops, the cornea splits into scleral and dermal layers 55 (allowing the eye to move with respect to the epidermis, as in jawed fish), extraocular muscles develop and the eye erupts at the surface to form a vertebrate-style visual organ.…”