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

Abstract

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.

The functional anatomy of the cornea of the Shorthead lamprey, Mordacia mordax (Mordaciidae, Agnatha): A comparison between downstream and upstream migrants

“…However, the presence of four basement membranes is unusual and differs among species. Basement membranes do not normally face relatively empty spaces, such as the mucoid layer and the anterior chamber of the eye, but all three basement membranes are present in M. mordax (this study), G. australis (H. B. Collin et al, 2021) and P. marinus (Van Horn et al, 1969a). The basement membrane between the anterior monocellular layer and the scleral stroma of the Shorthead lamprey is absent in the Pouched lamprey (H. B. Collin et al, 2021) (Table 6).…”

“…We were unable to ascertain whether the space between this mucoid layer and the scleral cornea is present in the live animals; however, as the fluidity of the mucoid layer allows free movement of the globe (Dickson & Graves, 1981; Duke‐Elder, 1958) beneath the primary spectacle, the presence of a space would further increase eye movements. The diameter of the collagen fibrils in the mucoid layer of the M. mordax is 17.88 nm in downstream and 20.77 nm in upstream migrants, compared with downstream migrants of G. australis (21.5 ± 3.7 nm; H. B. Collin et al, 2021) and all are significantly ( p < .00001) thinner than their neighbouring dermal stromal collagen fibrils.…”

“…Numerous microholes are present in the epithelial surface of the Shorthead lamprey M. mordax (245 ± 15 nm) and the Pouched lamprey Geotria australis (395 ± 15 nm) (S. P. Collin & Collin, 2006). Although there is a significant inverse relationship between the diameter of the epithelial surface microholes and the cell size in G. australis (H. B. Collin et al, 2021) and in the pre‐metamorphic axolotl Amblystoma mexicanum (S. P. Collin & Collin, 2021), in that the largest holes are present in the smallest cells and the smallest holes are in the larger cells (the largest cells have no holes), following a further examination of the original data (S. P. Collin & Collin, 2006), such a relationship could not be established in M. mordax .…”

“…Although there was considerable interest in the lamprey eye in the early 20th century (Duke‐Elder, 1958; Rochon‐Duvigneaud, 1943; Walls, 1942), there have been few ultrastructural studies of the lamprey cornea and these have mostly concentrated on the Northern hemisphere Sea lamprey Petromyzon marinus (Pederson et al, 1971; Van Horn et al, 1969a, 1969b) and the European river lamprey Lampetra fluviatilis (Dickson & Graves, 1981). Studies of the Southern hemisphere lampreys have examined the surface structure of the cornea of the Pouched lamprey ( Geotria australis ) and the Shorthead lamprey ( M. mordax ) (H. B. Collin & Collin, 2000; S. P. Collin & Collin 2006; S. P. Collin & Potter, 2000) and the ultrastructure of the cornea of the recently metamorphosed downstream Pouched lamprey (H. B. Collin et al, 2021). However, there have been no ultrastructural studies of the anatomy of the cornea of the Shorthead lamprey, M. mordax and no comparative study of the cornea in both downstream and upstream migrants.…”

From morphological to ecological adaptation of the cornea in Oxudercinae fishes

“…These microprojections increase the surface area available for the transport of nutritional and waste products across the cell surface (Collin and Collin, 2000a). Superficial epithelial cells are covered by numerous microprojections (microridges, microvilli, microplicae, and microholes) (Collin and Collin, 2000b;Collin et al, 2021). In different habitats, the corneal microstructure and cellular morphology of these vertebrates have evolved corresponding adaptations.…”