Mineralized Cartilage and Bone-Like Tissues in Chondrichthyans Offer Potential Insights Into the Evolution and Development of Mineralized Tissues in the Vertebrate Endoskeleton

Abstract

The impregnation of biominerals into the extracellular matrix of living organisms, a process termed biomineralization, gives rise to diverse mineralized (or calcified) tissues in vertebrates. Preservation of mineralized tissues in the fossil record has provided insights into the evolutionary history of vertebrates and their skeletons. However, current understanding of the vertebrate skeleton and of the processes underlying its formation is biased towards biomedical models such as the tetrapods mouse and chick. Chondrichthyans (sharks, skates, rays, and chimaeras) and osteichthyans are the only vertebrate groups with extant (living) representatives that have a mineralized skeleton, but the basal phylogenetic position of chondrichthyans could potentially offer unique insights into skeletal evolution. For example, bone is a vertebrate novelty, but the internal supporting skeleton (endoskeleton) of extant chondrichthyans is commonly described as lacking bone. The molecular and developmental basis for this assertion is yet to be tested. Subperichondral tissues in the endoskeleton of some chondrichthyans display mineralization patterns and histological and molecular features of bone, thereby challenging the notion that extant chondrichthyans lack endoskeletal bone. Additionally, the chondrichthyan endoskeleton demonstrates some unique features and others that are potentially homologous with other vertebrates, including a polygonal mineralization pattern, a trabecular mineralization pattern, and an unconstricted perichordal sheath. Because of the basal phylogenetic position of chondrichthyans among all other extant vertebrates with a mineralized skeleton, developmental and molecular studies of chondrichthyans are critical to flesh out the evolution of vertebrate skeletal tissues, but only a handful of such studies have been carried out to date. This review discusses morphological and molecular features of chondrichthyan endoskeletal tissues and cell types, ultimately emphasizing how comparative embryology and transcriptomics can reveal homology of mineralized skeletal tissues (and their cell types) between chondrichthyans and other vertebrates.

Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)

“…The irregular shape of these tesserae is a significant departure from the polygonal (or at least symmetrical) tesserae of other batoid taxa (e.g. Urobatis, Aetobatus, Raja; Seidel et al, 2016Seidel et al, , 2020Seidel et al, , 2021Atake and Eames, 2021) and of the smaller Rhina and Rhynchobatus sampled here (Figures 9, 10 and Supplementary Figure S2). Similar irregular tesserae, fused together at their perichondral surfaces, have been observed in the jaw cortices of other species, either in healthy tissues (Maisey, 2013;Maisey et al, 2021) or associated with a callus-building damage response (Dean et al, 2017).…”

“…From an anatomical perspective, mechanical durophagy is a particularly impressive dietary mode for elasmobranch fishes, as shark and ray skeletons are composed predominantly of unmineralized cartilage covered by a mineralized crust of blocks called tesserae, typically arranged in a monolayer merely hundreds of microns thick ( Maisey, 2013 ; Atake and Eames, 2021 ; Berio et al, 2021 ; Maisey et al, 2021 ). A variety of morphological features have been found to be associated with mechanical durophagy (e.g.…”

Extant cartilaginous fishes share trabecular and areolar mineralization patterns, but not tesserae, and evidence for a paedomorphic chimaera skeleton

“…Overall, these data strongly suggest that histological zones of tesserae actually correlate with mineralization patterns. Some chondrichthyans have mineralized endoskeletal tissues that have been characterized as bone-like (Atake and Eames, 2021). For example, the cap zone of tesserae displays bony features, like elongate cell lacunae in a mineralized ECM of densely packed Col1 fibers (Atake et al, 2019;Kemp and Westrin, 1979;Seidel et al, 2017;Seidel et al, 2016).…”

Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

“…1 Due to their key position near the base of phylogeny, the Chondrichthyans are of interest for the evolutionary study of various biological processes or systems such as the adaptive immune system, 2,3 various developmental processes, 4,5 or the endoskeleton evolution. 6 Among the recent advances in the whole genome sequencing of several species, those concerning the elephant shark Callorhinchus milii are the first to have opened new vistas regarding the molecular underpinnings of various cellular processes in Chondrichthyans. 7−11 The genomes of sharks are characterized by reduced molecular evolution rates and their relatively large size, from a 974 Mb length for C. milii to a 4600 Mb length for Carcharodon carcharias and feature large introns and a large content of transposable elements rather than massive gene duplication.…”

“…The small-spotted catshark belongs to the cartilaginous fishes (Chondrichthyes) comprising the Holocephalans (Chimaeras) and the Elasmobranchs (Sharks, rays, and skates), which occupy a unique phylogenetic position as a result of their divergence from Osteichthyes (Bony Vertebrates) estimated to have occurred around 450-million years ago (Mya) . Due to their key position near the base of phylogeny, the Chondrichthyans are of interest for the evolutionary study of various biological processes or systems such as the adaptive immune system, , various developmental processes, , or the endoskeleton evolution . Among the recent advances in the whole genome sequencing of several species, those concerning the elephant shark Callorhinchus milii are the first to have opened new vistas regarding the molecular underpinnings of various cellular processes in Chondrichthyans. − The genomes of sharks are characterized by reduced molecular evolution rates and their relatively large size, from a 974 Mb length for C.…”