Ontogeny of the tessellated skeleton: insight from the skeletal growth of the round stingray Urobatis halleri

Abstract

The majority of the skeleton of elasmobranch fishes (sharks, rays and relatives) is tessellated: uncalcified cartilage is overlain by a superficial rind of abutting, mineralized, hexagonal blocks called tesserae. We employed a diversity of imaging techniques on an ontogenetic series of jaw samples to investigate the development of the tessellated skeleton in a stingray ( Urobatis halleri ). We compared these data with the cellular changes that characterize cartilage calcification in bony skeletons. Skeletal growth is characterized by the appearance of tesserae as well as changes in chondrocyte shape, arrangement and density. Yolk sac embryos (35-56 mm disc width, DW) have untessellated lower jaw tissue wrapped in perichondrium and densely packed with chondrocytes. Chondrocyte density decreases dramatically after yolk sac absorption (histotroph stage: 57-80 mm DW) until the formation of tesserae, which are first visible using our techniques as thin (~60 μ m), sub-perichondral plaques. During the histotroph stage, flattened chondrocytes align parallel to the perichondrium at the tissue periphery, where we believe they are incorporated into developing tesserae to form the cell-rich laminae observed within tesserae; in older animals peripheral cells in the uncalcified phase are rounder and less uniformly oriented. By parturition (~75 mm DW), cell density and the number of adjoining chondrocyte pairs (an indicator of cell division) have dropped to less than a third of their initial values; these remain low and tesserae continue to grow in size. The tessellated skeleton is a simple solution to the conundrum of growth in an endoskeleton with external mineralization and no remodeling. Although we see parallels with endochondral ossification (e.g. chondrocytes decreasing in density with age), the lack of chondrocyte hypertrophy and the fact that mineralization is sub-perichondral (not the case in mammalian cartilage) suggest that the similarities end there.

Flexural stiffness and composition of the batoid propterygium as predictors of punting ability

“…The high metabolic activity of bone allows for osteoblasts and osteoclasts to carry out such remodeling by continuously laying down and removing bone tissue, respectively (Currey, 2002). In contrast, very little is known about how the elasmobranch cartilaginous skeleton, which has very low metabolic activity and appears to lack cells for remodeling (Dean et al, 2009), adapts to similar biological loads either on an ontogenetic or an evolutionary time scale.…”

“…Recent studies (Summers, 2000;Summers et al, 2004) have also demonstrated adaptations of tessellated cartilage in high-stress environments. Tessellated cartilage is composed of an outer layer mosaic of hydroxyapatite tiles, termed tesserae (hundreds of microns deep and wide in adults), which are joined together by intertesseral collagencomposed of water and proteoglycan in a matrix of collagen fibers (Dean et al, 2008;Dean et al, 2009) (Fig.1). In durophagous elasmobranchs, the jaws, which bear very large loads, are composed of multiple layers of tessellated cartilage, arranged to maximize the second moment of area with respect to crushing loads (Summers, 2000;Summers et al, 2004).…”

Ontogenetic development of an exceptionally preserved Devonian cartilaginous skeleton

“…Among jawed vertebrates, perichondral bone and GCC characterize basal taxa such as placoderms (Ørvig, '51, '57) and chondrichthyans (Dean et al, 2009), although endochondral bone is absent (Donoghue et al, 2006;Witten and Huysseune, 2007).…”

“…An important developmental difference involves the inductive ability of the hypertrophied cartilage cells, these being associated with endochondral bone, but absent in chondrichthyan cartilage (Dean et al, 2009), and in GCC (Witten and Huysseune, 2007;contra Sanchez et al, 2010). Gene expression for osteoblast differentiation and vascular invasion may have been lost, but an alternative hypothesis is that although hypertrophic chondrocytes are present in Palaeospondylus, the vital inductive role they play in conversion to endochondral bone had not yet evolved.…”

Cartilage of Marine Vertebrates

“…The structure and ultrastructure of calcifi ed cartilage in the endoskeletal tesserae have been characterized not only of sharks (Bargmann 1939 ;Kemp and Westrin 1979 ;Dean et al 2008 ) but also of stingrays (Summers et al 1998 ;Dean and Summers 2006 ;Dean 2007 ;Dean et al 2007Dean et al , 2009aDean et al , b , 2010. For example, growth of the jaw cartilage as well as the tessellation of the round stingray Urobatis halleri has been recently studied in the Lab of Adam Summers.…”