New histological information on Holoptychius Agassiz, 1839 (Sarcopterygii, Porolepiformes) provides insights into the palaeoecological implications and evolution of the basal plate of the scales of osteichthyans

Abstract

The porolepiform sarcopterygian Holoptychius Agassiz, 1839 from the Upper Devonian is one of the most widely found vertebrates in the Palaeozoic fossil record. Holoptychius is considered to display a more ubiquitous mode of life and a greater potential of dispersion than any other sarcopterygian taxon, consistent with its cosmopolitan distribution and profuse fossil record, mainly represented by scales. Previous histological studies on the squamation of Holoptychius have discussed the variable ornamentation of the superficial layer, however the basal plate has been less explored. Here we furnish new histological data on the scales of Holoptychius, focusing on the mineralization rate and organization of the lamellar bone. Ground sections show that the basal plate is made of a stacking of thick collagenous layers with a plywood-like structure. Collagenous fibres are parallel within layers, with two successive layers orthogonally arranged and with every second layer rotated by an angle of 36º. This condition, known as a double-twisted plywood-like organization, is similar to that of other sarcopterygians like Eusthenopteron and extant coelacanths and dipnoans. The new palaeohistological data provide insights into the morphofunctional, palaeoecological and phylogenetical implications of the microstructural characteristics of the scales, adding to our knowledge of the histological diversity of osteichthyans.

Exploring the three-dimensional vasculature of dermal hard tissues in thyestiid osteostracans using synchrotron radiation microtomography

“…Furthermore, the smaller spaces are not homogeneously distributed in the matrix of the basal layer and they generally only occur in close association with the lines of intersection between bundles of lamellae, but not in-between (). In addition, these spaces show no sign of elongated extensions, as it would be expected in the case of cell spaces (canaliculi; Mondéjar Fernández & Meunier, 2020). O'Shea et al (2019) further ruled out the possibility of the basal layer being composed of elasmodine (because the middle layer was interpreted as cellular bone), or as an ossification of the stratum compactum of the dermis.…”

“…In accordance with the growth series presented by Denison (1947), the first mineralization fronts of the basal layer originate at the contact with the middle layer, and they eventually concentrate around basal canals. The mineralization of pre-existing fiber bundles in this way is reminiscent of the subsequential mineralization process seen in the elasmodine of osteichthyan scales (Meunier, 1981; Schönbörner et al, 1979), but also in the basal plate of Polypterus (Mondéjar Fernández & Meunier, 2020), as well as in lamellar bone, circumpulpar dentine, and enamel of mammals (Bernard, 1971, 1972). No Mandl's corpuscles, i.e., separate initiation-sites of mineralization within elasmodine (Meunier, 1981), have been identified in the CT data.…”

A microanatomical and histological study of the scales of the Devonian sarcopterygianMiguashaia bureauiand the evolution of the squamation in coelacanths

“…We have observed the presence of five fibrillary directions (Figure 8a), indicating that a repetitive pattern occurs every five layers (Figures 3c and 7b) and that each fibre rotates from one layer to the next with an angle of approximately 36°, thus constituting a twisted plywood. But contrary to the basal plate of the scales of Latimeria (Figure 8b,c), no arciform patterns, characteristic of a double-twisted plywood (Giraud et al, 1978a,b;Meunier, 1981;Mondéjar Fernández & Meunier, 2020), occur in transversal section, thus indicating that the isopedine of the scales in M. bureaui is composed of a simple twisted plywood. Several small osteocytic lacunae and canaliculi are visible between the plies, showing that the collagenous network enclosed elongate osteocytes (elasmocytes sensu Meunier, 1984;Francillon-Vieillot et al, 1990) with their cytoplasmic processes extending along the collagen fibres (Figures 4c,d and 8a).…”

“…The combination of this microstructural arrangement with a rounded outline allows to ascribe the scales of coelacanths to the elasmoid type (Bertin, 1944;Castanet et al, 1975;Hadiaty & Rachmatika, 2003;Meunier & Zylberberg, 1999;Meunier et al, 2008;Miller, 1979;Smith et al, 1972), a scale morpho-and histotype that is widely spread and convergently acquired in osteichthyans (e.g. Francillon-Vieillot et al, 1990;Mondéjar Fernández & Meunier, 2020;Schultze, 1977Schultze, , 2015Schultze, , 2018. The general structure of the elasmoid scales displayed in Miguashaia has been maintained across coelacanth evolution until the Recent as evidenced in Latimeria (Castanet et al, 1975;Meunier et al, 2008), although the ornamentation patterns, ossification rate, and relative thickness of the various layers differ across taxa.…”

“…A double-twisted plywood is also known to occur convergently in other extinct sarcopterygians with rounded scales, like in the tetrapodomorph Eusthenopteron foordi (Zylberberg et al, 2010) and the dipnomorph Holoptychius sp. (Mondéjar Fernández & Meunier, 2020), as well as in the living dipnoans Neoceratodus forsteri, Lepidosiren paradoxa and Protopterus (P. annectens and P.…”