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

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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.

No MeSH data available.


Histology of Tesseraspis tesselata. NHM P.73617, SRXTM sections through an isosurface model of a tessera (A); SEM of the external surface morphology of a tessera, showing two distinct tubercle generations, specimen lost (B); etched SEM section through the enameloid capping layer of the superficial layer, specimen lost (C); NHM P.73617, SRXTM volume rendered transverse section through L2, showing the architecture of the intersecting radial walls (D); NHM P.73618, SEM BSE section through L2 showing truncated centripetal lamellae interpreted as resorption (E); volume rendered virtual thin sections of NHM P.73617 (F, G); transverse section through a radial wall of L2, showing the arrangement of thread‐like spaces (F); section through the dermal skeleton of a tessera, showing the arrangement of Sharpey's fibres in L3 (G). S.F., Sharpey's fibres. Scale bar equals 193 μm in (A), 628 μm in (B), 47 μm in (C), 124 μm in (D), 68 μm in (E), 64 μm in (F) and 230 μm in (G).
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jmor20370-fig-0003: Histology of Tesseraspis tesselata. NHM P.73617, SRXTM sections through an isosurface model of a tessera (A); SEM of the external surface morphology of a tessera, showing two distinct tubercle generations, specimen lost (B); etched SEM section through the enameloid capping layer of the superficial layer, specimen lost (C); NHM P.73617, SRXTM volume rendered transverse section through L2, showing the architecture of the intersecting radial walls (D); NHM P.73618, SEM BSE section through L2 showing truncated centripetal lamellae interpreted as resorption (E); volume rendered virtual thin sections of NHM P.73617 (F, G); transverse section through a radial wall of L2, showing the arrangement of thread‐like spaces (F); section through the dermal skeleton of a tessera, showing the arrangement of Sharpey's fibres in L3 (G). S.F., Sharpey's fibres. Scale bar equals 193 μm in (A), 628 μm in (B), 47 μm in (C), 124 μm in (D), 68 μm in (E), 64 μm in (F) and 230 μm in (G).

Mentions: The cephalothoracic shield of Tesseraspis is composed of numerous tessellating plates. These are four‐layered (Fig. 3A), consisting of a superficial layer of elongate ridges, a compact layer of canals (L1), a trabecular middle layer (L2) and a substantial lamellar basal layer (L3).


Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton
Histology of Tesseraspis tesselata. NHM P.73617, SRXTM sections through an isosurface model of a tessera (A); SEM of the external surface morphology of a tessera, showing two distinct tubercle generations, specimen lost (B); etched SEM section through the enameloid capping layer of the superficial layer, specimen lost (C); NHM P.73617, SRXTM volume rendered transverse section through L2, showing the architecture of the intersecting radial walls (D); NHM P.73618, SEM BSE section through L2 showing truncated centripetal lamellae interpreted as resorption (E); volume rendered virtual thin sections of NHM P.73617 (F, G); transverse section through a radial wall of L2, showing the arrangement of thread‐like spaces (F); section through the dermal skeleton of a tessera, showing the arrangement of Sharpey's fibres in L3 (G). S.F., Sharpey's fibres. Scale bar equals 193 μm in (A), 628 μm in (B), 47 μm in (C), 124 μm in (D), 68 μm in (E), 64 μm in (F) and 230 μm in (G).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4979667&req=5

jmor20370-fig-0003: Histology of Tesseraspis tesselata. NHM P.73617, SRXTM sections through an isosurface model of a tessera (A); SEM of the external surface morphology of a tessera, showing two distinct tubercle generations, specimen lost (B); etched SEM section through the enameloid capping layer of the superficial layer, specimen lost (C); NHM P.73617, SRXTM volume rendered transverse section through L2, showing the architecture of the intersecting radial walls (D); NHM P.73618, SEM BSE section through L2 showing truncated centripetal lamellae interpreted as resorption (E); volume rendered virtual thin sections of NHM P.73617 (F, G); transverse section through a radial wall of L2, showing the arrangement of thread‐like spaces (F); section through the dermal skeleton of a tessera, showing the arrangement of Sharpey's fibres in L3 (G). S.F., Sharpey's fibres. Scale bar equals 193 μm in (A), 628 μm in (B), 47 μm in (C), 124 μm in (D), 68 μm in (E), 64 μm in (F) and 230 μm in (G).
Mentions: The cephalothoracic shield of Tesseraspis is composed of numerous tessellating plates. These are four‐layered (Fig. 3A), consisting of a superficial layer of elongate ridges, a compact layer of canals (L1), a trabecular middle layer (L2) and a substantial lamellar basal layer (L3).

View Article: PubMed Central - PubMed

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.

No MeSH data available.