Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

Abstract

Living vertebrates are divided into those that possess a fully formed and fully mineralised skeleton (gnathostomes) versus those that possess only unmineralised cartilaginous rudiments (cyclostomes). As such, extinct phylogenetic intermediates of these living lineages afford unique insights into the evolutionary assembly of the vertebrate mineralised skeleton and its canonical tissue types. Extinct jawless and jawed fishes assigned to the gnathostome stem evidence the piecemeal assembly of skeletal systems, revealing that the dermal skeleton is the earliest manifestation of a homologous mineralised skeleton. Yet the nature of the primitive dermal skeleton, itself, is poorly understood. This is principally because previous histological studies of early vertebrates lacked a phylogenetic framework required to derive evolutionary hypotheses. Nowhere is this more apparent than within Heterostraci, a diverse clade of primitive jawless vertebrates. To this end, we surveyed the dermal skeletal histology of heterostracans, inferred the plesiomorphic heterostracan skeleton and, through histological comparison to other skeletonising vertebrate clades, deduced the ancestral nature of the vertebrate dermal skeleton. Heterostracans primitively possess a four‐layered skeleton, comprising a superficial layer of odontodes composed of dentine and enameloid; a compact layer of acellular parallel‐fibred bone containing a network of vascular canals that supply the pulp canals (L1); a trabecular layer consisting of intersecting radial walls composed of acellular parallel‐fibred bone, showing osteon‐like development (L2); and a basal layer of isopedin (L3). A three layered skeleton, equivalent to the superficial layer L2 and L3 and composed of enameloid, dentine and acellular bone, is possessed by the ancestor of heterostracans + jawed vertebrates. We conclude that an osteogenic component is plesiomorphic with respect to the vertebrate dermal skeleton. Consequently, we interpret the dermal skeleton of denticles in chondrichthyans and jawless thelodonts as independently and secondarily simplified. J. Morphol. 276:657–680, 2015. © 2015 The Authors Journal of Morphology Published by Wiley Periodicals, Inc.

The dermal skeleton of the jawless vertebrateTremataspis mammillata(Osteostraci, stem‐Gnathostomata)

“…Tremataspis mammillata represents an early stage in dermal skeletal differentiation across the trunk and cranium, with reduction of the middle layer posteriorly until it is almost absent in the caudal scales. A similar level of skeletal differentiation is seen in heterostracans, where the middle layer is well developed in the headshield, but reduced or absent in the trunk scales (Keating et al, ). In Tremataspis , this is associated with a reduction in differentiation between the lower mesh canals and the superficial + lower canal networks.…”

“…Historically, many hypotheses about the evolution of the dermal skeleton have focussed on the stratigraphic sequence of appearance. Crown gnathostomes ancestrally possessed a fully developed dermal skeleton of cellular bone overlain by odontodes (dermal tooth-like structures; Donoghue & Sansom, 2002;Giles, Rücklin, & Donoghue, 2013;Keating & Donoghue, 2016;Keating, Marquart, & Donoghue, 2015;Keating, Marquart, Marone, & Donoghue, 2018;Sire, Donoghue, & Vickaryous, 2009). In contrast, extant jawless vertebrates and invertebrate chordates entirely lack a mineralised skeleton.…”

Phylogenetic relationships of psammosteid heterostracans (Pteraspidiformes), Devonian jawless vertebrates

“…For each psammosteid taxon, text and graphic data on the type specimens were used (Elliott, Mark-Kurik, and Daeschler, 2004;Elliott and Mark-Kurik, 2005;Halstead Tarlo, 1964aLyarskaya, 1971;Mark-Kurik, 1968, 1999Novitskaya, 1965Novitskaya, , 2004Obruchev, 1940;Obruchev and Mark-Kurik, 1965;Růžička, 1929;Tarlo, 1961). The most recent data on the general morphology, ornamentation and histology of psammosteids were also encoded (Glinskiy, 2014;Glinskiy and Mark-Kurik, 2016;Glinskiy and Nilov, 2017;Glinskiy and Pinakhina, 2018;Keating, Marquart, and Donoghue, 2015;Moloshnikov, 2001). All characters are discrete (binary or multistate), mostly unordered, but 21 multistate characters are ordered as specified by the relationship of character states within the transformation series (1,8,16,21,30,31,38,54,57,64,71,79,81,83,86,87,88,89,99,108,117).…”

“…Aspidin reticular layer (L1) of the median plates of cephalothorax: (0) absent, (1) present. Histological information from Novitskaya (1965), Novitskaya (2004), Keating et al (2015). 119.…”

Paleoictiofauna da Formação Pimenteira (Devoniano), Bacia do Parnaíba, Pi, Brasil

“…Uma característica dita importante na classificação de muitas placas dermais é a sua superfície coberta de dentículos dérmicos (Tarlo, 1962). Porém, estudos têm mostrado que a presença de tais nódulos seria plesiomórfico para Placodermi (Keating et al, 2015), complicando a classificação deste táxon. O exemplar descrito aqui possui em sua superfície um grande número de pequenos nódulos ou grânulos que são facilmente comparáveis aos nódulos de dentina (Figura 9A'-D'), embora não seja possível determinar se estas estruturas seriam mesmo de dentina, já que este espécime precisaria ser analisado com mais detalhes através de cortes histológicos, porém inviáveis até o momento devido a sua importância histórica e raridade.…”