Endoskeletal mineralization in chimaera and a comparative guide to tessellated cartilage in chondrichthyan fishes (sharks, rays and chimaera)

Abstract

An accepted uniting character of modern cartilaginous fishes (sharks, rays, chimaera) is the presence of a mineralized, skeletal crust, tiled by numerous minute plates called tesserae. Tesserae have, however, never been demonstrated in modern chimaera and it is debated whether the skeleton mineralizes at all. We show for the first time that tessellated cartilage was not lost in chimaera, as has been previously postulated, and is in many ways similar to that of sharks and rays. Tesserae in Chimaera monstrosa are less regular in shape and size in comparison to the general scheme of polygonal tesserae in sharks and rays, yet share several features with them. For example, Chimaera tesserae, like those of elasmobranchs, possess both intertesseral joints (unmineralized regions, where fibrous tissue links adjacent tesserae) and recurring patterns of local mineral density variation (e.g. Liesegang lines, hypermineralized ‘spokes’), reflecting periodic accretion of mineral at tesseral edges as tesserae grow. Chimaera monstrosa 's tesserae, however, appear to lack the internal cell networks that characterize tesserae in elasmobranchs, indicating fundamental differences among chondrichthyan groups in how calcification is controlled. By compiling and comparing recent ultrastructure data on tesserae, we also provide a synthesized, up-to-date and comparative glossary on tessellated cartilage, as well as a perspective on the current state of research into the topic, offering benchmark context for future research into modern and extinct vertebrate skeletal tissues.

Diversity and Evolution of Mineralized Skeletal Tissues in Chondrichthyans

“…Previous studies showed poorly developed cartilaginous tissue in the posterior vertebrae of juvenile H. colliei, where histology displayed no sign of modified cartilaginous matrix that could be linked to cartilage mineralization (Debiais-Thibaud, 2019). However, more recent publications pointed out the thin layer of mineralized matrix in the synarcual of the elephant shark Callorhinchus milii (Pears et al, 2020) and recognized thin tesserae in the adult C. milii and rabbit fishes Chimaera monstrosa (Pears et al, 2020;Seidel et al, 2020). In our H. colliei sample, we detect a similar thin layer of mineralized tissue in the synarcual of a hatchling and a juvenile specimen (Figures 4A,G).…”

“…More recent studies have reassessed the diversity of poorly described features of mineralization in cartilaginous fishes (Eames et al, 2007;Enault et al, 2015;Seidel et al, 2017Seidel et al, , 2020Atake et al, 2019;Debiais-Thibaud, 2019;Smith et al, 2019;Chaumel et al, 2020;Pears et al, 2020), raising new questions on the origin and evolution of mineralized tissues in this clade and therefore in vertebrates. Comparative studies of skeletal tissues in non-tetrapods have uncovered a wide range of skeletal tissues that had remained unknown from the sole study of tetrapods (discussed by Huysseune, 2009 andHall andWitten, 2019).…”

“…Extant chondrichthyans include three major clades. Holocephalans are divided into the three extant families Callorhinchidae, Chimaeridae, and Rhinochimaeridae and have long been considered to have a non-mineralized cartilaginous endoskeleton but are now recognized to have tesserae (Finarelli and Coates, 2014;Maisey et al, 2020;Pears et al, 2020;Seidel et al, 2020). Sister to holocephalans, elasmobranchs include selachians (sharks) that are grouped into Galeomorphii (orders: Carcharhiniformes, Heterodontiformes, Lamniformes, and Orectolobiformes) and Squalomorphii (orders: Hexanchiformes, Pristiophoriformes, Squaliformes, Squatiniformes, and the family Echinorhinidae) and batoids (rays, guitarfishes, skates, and sawfishes) that are divided into Myliobatiformes, Rhinopristiformes, Rajiformes, and Torpediniformes (Naylor et al, 2012;Ebert et al, 2013;Last et al, 2016).…”

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

“…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.…”

Biodiversitas dan Status Konservasi Hiu dan Pari di Pelabuhan Perikanan Lampulo Banda Aceh

“…Hiu dan pari merupakan anggota dari subkelas Elasmobranchii (Dulvy et al 2014;Dharmadi & Satria 2015;SEAFDEC 2017;Hara et al 2018;D'Alberto et al 2019;Bernardo et al 2020), dimana Elasmobranchii mencakup sekelompok besar ikan karnivora dan detritivora yang tersebar di seluruh dunia, mulai dari perairan dangkal hingga kedalaman abisal (Tuya et al 2020). Selain itu, hiu dan pari juga tergolong sebagai anggota kelas Chondrichthyes (Bhat et al 2018;Seidel et al 2020;Jambura et al 2020;Herraiz et al 2020;Sternes & Shimada 2020) yaitu ikan bertulang rawan dari salah satu garis keturunan vertebrata tertua yang paling beragam secara ekologisnya dan muncul lebih dari 420 juta tahun yang lalu (Tiktak et al 2020). Menurut Heithaus et al (2008) dan Ferretti et al (2010) hiu dianggap memainkan peran penting dalam penataan jaring-jaring makanan di laut.…”