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.

Highlights

  • Reviewed by: David Marjanović, Museum of Natural History Berlin (MfN), Germany Kevin Stevens, Ruhr University Bochum, Germany

  • 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

  • Extant chondrichthyans are subdivided into two groups: elasmobranchs and holocephalans, which last shared a common ancestor at least 385 million years ago (Janvier and Pradel, 2015; Frey et al, 2019; Cohen et al, 2021)

Read more

Summary

Homologous Skeletal Characters in Vertebrates

Many organisms utilize biominerals to harden the deep (endo) or more superficial (exo-) supporting skeleton through a process termed biomineralization. Biomineralization occurs by deposition of biological apatite into collagen-/amelogenin-rich matrices, and this process gives rise to the main types of mineralized (or calcified) tissues: bone, mineralized cartilage, dentine, enamel, and enameloid (Hall, 1975; Kemp, 1989; Donoghue et al, 2006) Given that these mineralized tissue types were already distinct in ancestral vertebrates, later-diverged vertebrate groups mostly modified ancestral mineral and organic components in order to mineralize their skeletal tissues (Enlow and Brown, 1958; Francillon-Vieillot et al, 1990). Extant chondrichthyans are subdivided into two groups: elasmobranchs (sharks, skates, and rays) and holocephalans (chimaeras), which last shared a common ancestor at least 385 million years ago (Janvier and Pradel, 2015; Frey et al, 2019; Cohen et al, 2021) Despite their predominantly cartilaginous endoskeleton, chondrichthyans exhibit a great diversity of derived and ancestral mineralized tissues. We consider how recent analyses of chondrichthyan tesserae and centra shed light upon the evolution of mineralized tissues in the vertebrate endoskeleton, including examining whether chondrichthyans make bone, but first we briefly summarize some basic concepts in skeletal biology (mostly from studies of tetrapods)

MINERALIZATION PATTERNS AND DEVELOPMENTAL PROCESSES OF BONE AND CARTILAGE
WHAT HISTOLOGICAL REGIONS OF TESSERAE PRODUCE TESSERAL MINERALIZATION PATTERNS?
THE ELASMOBRANCH CENTRUM EXHIBITS A UNIQUE AREOLAR MINERALIZATION PATTERN
USING COMPARATIVE TRANSCRIPTOMICS TO TEST FOR CHONDRICHTHYAN BONE
CONCLUSION

Talk to us

Join us for a 30 min session where you can share your feedback and ask us any queries you have

Schedule a call

Disclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.