Skeletal elements within teleost eyes and a discussion of their homology

Abstract

Scleral ossicles and scleral cartilages form part of the craniofacial skeleton of many vertebrates. Some vertebrates, including all birds and most reptiles, but excluding most mammals, have scleral cartilages as well as scleral ossicles supporting their eyes. The teleost equivalent of these elements has received little attention in the literature. From radiographic and whole-mount analyses of over 400 individuals from 376 teleost species, we conclude that the teleost scleral skeletal elements (ossicles and cartilage) differ significantly from those of reptiles (including birds). Scleral ossicles in teleosts have different developmental origins, different positions within the eyeball, and different relationships with the scleral cartilaginous element than those in reptiles. From whole-mount staining of a growth series of four species of teleost (Danio rerio, Salmo salar, Esox lucius, and Alosa pseudoharengus), we interpret the development of these elements and show that they arise from within an Alcian blue-staining cartilaginous ring that develops around the eye earlier in development. We present possible scenarios on the evolution of these scleral skeletal elements from a common gnathostome ancestor, and consider that teleost scleral skeletal elements may not be homologous to those in reptiles. Our study indicates that homology cannot be assumed for these elements, despite the fact that they share the same name, scleral ossicles.

Phylogeny of the family Characidae (Teleostei: Characiformes): from characters to taxonomy

“…In the condition typical for the Teleostei this cartilage forms two independent ossifications along the anterior and posterior margins of the eye that are separated by the remnants of the original cartilaginous ring (state 1; Fig. 119) (Franz-Odendaal & Hall, 2006). This condition was observed in most outgroup species and some members of the Characidae.…”

Developmental and morphological variation in the teleost craniofacial skeleton reveals an unusual mode of ossification

“…1D) or absent (1E). Teleosts without scleral ossicles maintain the scleral cartilage ring present in juveniles (see Franz-Odendaal and Hall, 2006).In two of the species examined in detail here, Alosa and Astyanax, the ossicles are narrow circumferentially elongated elements, whereas in Danio the ossicles are circular in shape (Fig. 2).…”

“…Schwab (2002), however, reports that the extraocular muscles in swordfish (Xiphias gladius) have six different types of muscle fibres and one special set that has limited contractile ability and serves a thermoregulatory function. It remains unclear whether muscles attach to scleral ossicles in all teleosts, the type of muscle if present, and whether scleral ossicles serve any role in visual acuity in teleosts.During our previous screen we identified that: (i) only some teleosts have scleral ossicles; (ii) typically (and maximally) only two ossicles are present per eye; and (iii) when present the morphology of these elements is not always the same in different teleost species (Franz-Odendaal and Hall, 2006). In addition, we concluded that the scleral ossicles of teleosts should not be assumed to be homologous to the scleral ossicles of reptiles.…”

“…Although much work is now focussed on understanding the development of fish craniofacial, axial and appendicular skeletons, little attention has been directed toward elements that arise later in development, especially elements in the head. The zebrafish skull has 74 cranial ossifications (Cubbage and Mabee, '96 709-721 (2007) The bones associated with the eye, also easily accessible, have been neglected.Although not all teleosts have scleral ossicles, when present, they are conserved in number, most teleosts having two ossicles per eye (Nakamura and Yamaguchi, '91;Franz-Odendaal and Hall, 2006). These bones are situated within the connective tissue ocular coat (the sclera) of the eye.…”

Quantitative estimates of visual performance features in fossil birds

“…Scleral ossifications offer a great possibility to estimate eyeball soft-tissue dimensions. Scleral ossicles are widespread among vertebrates and are secondarily lost only in Serpentes, Mammalia, Crocodylia, and extant Amphibia (Edinger, 1929;Franz-Odendaal and Hall, 2006). Teleostei develop up to four scleral ossicles from endochondral or perichondral ossification in the equatorial part of the eyeball.…”