Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii)

Abstract

Current knowledge on the skeletogenesis of Chondrichthyes is scarce compared with their extant sister group, the bony fishes. Most of the previously described developmental tables in Chondrichthyes have focused on embryonic external morphology only. Due to its small body size and relative simplicity to raise eggs in laboratory conditions, the small-spotted catshark Scyliorhinus canicula has emerged as a reference species to describe developmental mechanisms in the Chondrichthyes lineage. Here we investigate the dynamic of mineralization in a set of six embryonic specimens using X-ray microtomography and describe the developing units of both the dermal skeleton (teeth and dermal scales) and endoskeleton (vertebral axis). This preliminary data on skeletogenesis in the catshark sets the first bases to a more complete investigation of the skeletal developmental in Chondrichthyes. It should provide comparison points with data known in osteichthyans and could thus be used in the broader context of gnathostome skeletal evolution.

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

“…Tessellated cartilage is therefore a major component of the skeleton and is currently believed to be a synapomorphy for the entire chondrichthyan group (e.g., Maisey et al, 2019Maisey et al, , 2020, but see comments therein regarding morphological and histological disparity in stem-chondrichthyans). Contemporary examination of extant chondrichthyan mineralized skeletons and their tissues, however, have almost exclusively focused on sharks (Kemp and Westrin, 1979;Peignoux-Deville et al, 1982;Clement, 1986Clement, , 1992Bordat, 1987Bordat, , 1988Egerbacher et al, 2006;Eames et al, 2007;Enault et al, 2016) and rays (Dean et al, 2009;Claeson, 2011;Seidel et al, 2016Seidel et al, , 2017aCriswell et al, 2017a,b). In contrast, mineralized skeletal tissues of extant chimaeroids (Holocephali) have been largely ignored, since the descriptions of vertebral development and morphology in the late nineteenth to mid-twentieth centuries (Hasse, 1879;Schauinsland, 1903;Dean, 1906); fossil holocephalans have faced similar neglect (but see Moy-Thomas, 1936;Patterson, 1965;Maisey, 2013).…”

“…In contrast, mineralized skeletal tissues of extant chimaeroids (Holocephali) have been largely ignored, since the descriptions of vertebral development and morphology in the late nineteenth to mid-twentieth centuries (Hasse, 1879;Schauinsland, 1903;Dean, 1906); fossil holocephalans have faced similar neglect (but see Moy-Thomas, 1936;Patterson, 1965;Maisey, 2013). This has led to contradictory descriptions of chimaeroid tissues (Lund and Grogan, 1997;Grogan and Lund, 2004;Pradel et al, 2009), prompting calls for more research (Eames et al, 2007;Dean et al, 2015;Enault et al, 2016). Notably, recent examination of chimaeroid mineralized skeletal tissues identified tesseral structures in the vertebral column (synarcual) and Meckel's cartilage of Chimaera and Hydrolagus (both Family Chimaeridae; Finarelli and Coates, 2014;Debiais-Thibaud, 2019;Seidel et al, 2019aSeidel et al, , 2020 and in the fin skeleton of Callorhinchus (Family Callorhinchidae; Maisey et al, 2020), seemingly refuting the view that extant chimaeroids lack tessellated cartilage.…”

MicroCT survey of larval skeletal mineralization in the Cuban gar Atractosteus tristoechus (Actinopterygii; Lepisosteiformes)

“…TL: total length. SL: Serial length (Slater et al, 2009), mice (Shen et al, 2013;Ho et al, 2015), crocodilians (Dufeau and Witmer, 2015), turtles (Rice et al, 2016) and catsharks (Enault et al, 2016). To the best of our knowledge, however, a description of the development of the whole skeleton in gars with precise timings of ossification is still lacking, and 3D surfaces of the whole ossified skeleton at different stages are not available although it would be a valuable source of additional characters in comparative studies but also in educational contexts.…”

Mineralisation of theCallorhinchusvertebral column (Holocephali; Chondrichthyes)

“…Tessellated cartilage is therefore a major component of the skeleton and is currently believed to be a synapomorphy for the entire chondrichthyan group (e.g., Maisey et al 2019, but see comments therein regarding morphological and histological disparity in stem-chondrichthyans). Contemporary examination of extant chondrichthyan mineralised skeletons and their tissues, however, have almost exclusively focused on sharks (Kemp and Westrin, 1979;Peignoux-Deville et al, 1982;Clement, 1986Clement, , 1992Bordat, 1987Bordat, , 1988Egerbacher et al, 2006;Eames et al, 2007;Enault et al, 2016) and rays (Dean et al, 2009(Dean et al, , 2015Claeson, 2011;Seidel et al, 2016Seidel et al, , 2017aCriswell et al, 2017a, b). In contrast, mineralised skeletal tissues of extant chimaeroids (Holocephali) have been largely ignored, despite available descriptions of vertebral development and morphology in the late nineteenth to mid-twentieth centuries (Hasse, 1879;Schauinsland, 1903;Dean, 1906); fossil holocephalans have faced similar neglect (e.g., Moy-Thomas, 1936;Patterson, 1965;Maisey, 2013).…”

“…In contrast, mineralised skeletal tissues of extant chimaeroids (Holocephali) have been largely ignored, despite available descriptions of vertebral development and morphology in the late nineteenth to mid-twentieth centuries (Hasse, 1879;Schauinsland, 1903;Dean, 1906); fossil holocephalans have faced similar neglect (e.g., Moy-Thomas, 1936;Patterson, 1965;Maisey, 2013). This has led to contradictory descriptions of chimaeroid tissues Grogan, 1997, 2004;Pradel et al, 2009;Dean et al, 2015), prompting calls for more research (Eames et al, 2007;Dean et al, 2015;Enault et al, 2016). Notably, recent examination of chimaeroid mineralised skeletal tissues identified tesseral structures in the vertebral column (synarcual) and Meckel's cartilage of Chimaera and Hydrolagus (both Family Chimaeridae; Finarelli and Coates, 2014;Debiais-Thibaud, 2019;Seidel et al, 2019a), seemingly refuting the view that extant chimaeroids lack tessellated cartilage.…”