Comparative Analysis of Mineralized Endoskeletal Tissues in Extant Cartilaginous Fishes Reveals Shared Trabecular and Areolar Patterns but Absence of Tesseral and Bone-like Features in Chimaeras

Core Concepts

Extant cartilaginous fishes share trabecular and areolar mineralization patterns in their endoskeletons, but lack the tesseral and bone-like tissues found in some elasmobranchs. Chimaeras also display skeletal paedomorphism compared to elasmobranchs.

Abstract

This study provides a comprehensive comparative analysis of the mineralized endoskeletal tissues in three extant cartilaginous fish representatives - the little skate, small-spotted catshark, and spotted ratfish (a chimaera). The key findings are: Trabecular and areolar mineralization patterns are shared features across extant chondrichthyans, but polygonal tesserae and bone-like tissues are absent in chimaeras. The chimaera endoskeleton retains more ancestral embryonic features, exhibiting skeletal paedomorphism compared to elasmobranchs. This is evidenced by lower tissue mineral density, unconstricted vertebral centra morphology, and histological similarities to elasmobranch embryonic centra. The histological "cap zone" correlates with the polygonal tesseral mineralization pattern, while the "body zone" correlates with trabecular mineralization patterns, regardless of whether they are organized into tesseral arrays or not. The authors propose new terminology to describe the diverse mineralization patterns observed, including "non-tesseral trabecular mineralization" to distinguish the irregular trabecular patterns in some species from the arrayed tesseral patterns. Overall, this study clarifies the shared and divergent features of the mineralized endoskeleton across extant cartilaginous fishes, providing insights into the evolution of skeletal tissues in this ancient vertebrate lineage.

Stats

Tissue mineral density (TMD) of the synarcual, neural arches, and centra in ratfish were significantly lower than in little skate and catshark. The TMD of ratfish synarcual was 0.31 ± 0.11 gHA/cm3, compared to 0.94 ± 0.04 gHA/cm3 in little skate. The TMD of ratfish neural arches was 0.40 ± 0.05 gHA/cm3, compared to 0.96 ± 0.04 gHA/cm3 in little skate and 0.81 ± 0.04 gHA/cm3 in catshark. The TMD of ratfish centra was 0.42 ± 0.10 gHA/cm3, compared to 0.88 ± 0.05 gHA/cm3 in little skate and 0.84 ± 0.02 gHA/cm3 in catshark.

Quotes

"Trabecular and areolar, but not polygonal, mineralization patterns are shared by extant chondrichthyans." "Three separate analyses argued that the chimaera endoskeleton retains ancestral embryonic features (i.e., paedomorphic)." "Larger and laterally extensive cap zones appeared to be the reason why polygonal tesserae displayed a superficial polygonal mineralization pattern."

Key Insights Distilled From

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

by Atake,O. J.,... at www.biorxiv.org 01-08-2024

https://www.biorxiv.org/content/10.1101/2024.01.07.574539v1

Deeper Inquiries

How might the genetic basis of skeletal mineralization, particularly the SCPP gene family, differ between elasmobranchs and chimaeras, and how could this contribute to the observed skeletal paedomorphism in chimaeras?

The genetic basis of skeletal mineralization, particularly the SCPP gene family, plays a crucial role in the development and maintenance of mineralized tissues in vertebrates. Elasmobranchs, such as sharks and rays, have been shown to express SCPP genes, which are essential for the formation of mineralized tissues like bone and dentin. In contrast, the genome of the chimaera Callorhinchus milii, a representative of the Holocephali subclass, does not contain any SCPP genes. This difference in gene expression could contribute to the observed skeletal paedomorphism in chimaeras. SCPP genes are known to regulate the deposition of calcium and phosphate ions in the extracellular matrix, promoting the mineralization of tissues. Without the presence of SCPP genes, chimaeras may have a reduced capacity for mineralization, leading to lower tissue mineral density and potentially affecting the overall skeletal development. This reduced skeletal mineralization could result in skeletal structures that resemble embryonic forms, as seen in the case of chimaeras exhibiting paedomorphic centra. The absence of SCPP genes in chimaeras may indicate a divergence in the genetic mechanisms underlying skeletal mineralization between elasmobranchs and chimaeras. This genetic difference could contribute to the unique skeletal characteristics observed in chimaeras, including their skeletal paedomorphism.

How might the genetic basis of skeletal mineralization, particularly the SCPP gene family, differ between elasmobranchs and chimaeras, and how could this contribute to the observed skeletal paedomorphism in chimaeras?

The genetic basis of skeletal mineralization, particularly the SCPP gene family, plays a crucial role in the development and maintenance of mineralized tissues in vertebrates. Elasmobranchs, such as sharks and rays, have been shown to express SCPP genes, which are essential for the formation of mineralized tissues like bone and dentin. In contrast, the genome of the chimaera Callorhinchus milii, a representative of the Holocephali subclass, does not contain any SCPP genes. This difference in gene expression could contribute to the observed skeletal paedomorphism in chimaeras. SCPP genes are known to regulate the deposition of calcium and phosphate ions in the extracellular matrix, promoting the mineralization of tissues. Without the presence of SCPP genes, chimaeras may have a reduced capacity for mineralization, leading to lower tissue mineral density and potentially affecting the overall skeletal development. This reduced skeletal mineralization could result in skeletal structures that resemble embryonic forms, as seen in the case of chimaeras exhibiting paedomorphic centra. The absence of SCPP genes in chimaeras may indicate a divergence in the genetic mechanisms underlying skeletal mineralization between elasmobranchs and chimaeras. This genetic difference could contribute to the unique skeletal characteristics observed in chimaeras, including their skeletal paedomorphism.

How might the genetic basis of skeletal mineralization, particularly the SCPP gene family, differ between elasmobranchs and chimaeras, and how could this contribute to the observed skeletal paedomorphism in chimaeras?

The genetic basis of skeletal mineralization, particularly the SCPP gene family, plays a crucial role in the development and maintenance of mineralized tissues in vertebrates. Elasmobranchs, such as sharks and rays, have been shown to express SCPP genes, which are essential for the formation of mineralized tissues like bone and dentin. In contrast, the genome of the chimaera Callorhinchus milii, a representative of the Holocephali subclass, does not contain any SCPP genes. This difference in gene expression could contribute to the observed skeletal paedomorphism in chimaeras. SCPP genes are known to regulate the deposition of calcium and phosphate ions in the extracellular matrix, promoting the mineralization of tissues. Without the presence of SCPP genes, chimaeras may have a reduced capacity for mineralization, leading to lower tissue mineral density and potentially affecting the overall skeletal development. This reduced skeletal mineralization could result in skeletal structures that resemble embryonic forms, as seen in the case of chimaeras exhibiting paedomorphic centra. The absence of SCPP genes in chimaeras may indicate a divergence in the genetic mechanisms underlying skeletal mineralization between elasmobranchs and chimaeras. This genetic difference could contribute to the unique skeletal characteristics observed in chimaeras, including their skeletal paedomorphism.