Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton

Keating, Joseph N.; Donoghue, Philip C. J.

doi:10.1098/rspb.2015.2917

Cited by 57 publications

(88 citation statements)

References 40 publications

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“…A peculiar bone‐like tissue devoid of osteocytes, called aspidin, has long been known in the dermal skeleton of †heterostracans, a group of Palaeozoic jawless vertebrates (Gross, ; Halstead, ). Similar tissues were later described in other early jawless stem gnathostome lineages, such as †anaspids, †thelodonts and †galeaspids (Stensiö, ; Sire, Donoghue & Vickaryous, ; Keating & Donoghue, ). Aspidin appears to be structurally very similar to teleost acellular bone, with probable collagen bundles (akin to the ‘tubules’ of teleosts) penetrating the mineralised tissue (Keating et al , ).…”

Section: Phylogenetic Distribution Of Acellular Bonesupporting

confidence: 63%

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

et al. 2019

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Vertebrate bone is composed of three main cell types: osteoblasts, osteoclasts and osteocytes, the latter being by far the most numerous. Osteocytes are thought to play a fundamental role in bone physiology and homeostasis, however they are entirely absent in most extant species of teleosts, a group that comprises the vast majority of bony 'fishes', and approximately half of vertebrates. Understanding how this acellular (anosteocytic) bone appeared and was maintained in such an important vertebrate group has important implications for our understanding of the function and evolution of osteocytes. Nevertheless, although it is clear that cellular bone is ancestral for teleosts, it has not been clear in which specific subgroup the osteocytes were lost. This review aims to clarify the phylogenetic distribution of cellular and acellular bone in teleosts, to identify its precise origin, reversals to cellularity, and their implications. We surveyed the bone type for more than 600 fossil and extant ray-finned fish species and optimised the results on recent large-scale molecular phylogenetic trees, estimating ancestral states. We find that acellular bone is a probable synapomorphy of Euteleostei, a group uniting approximately two-thirds of teleost species. We also confirm homoplasy in these traits: acellular bone occurs in some non-euteleosts (although rarely), and cellular bone was reacquired several times independently within euteleosts, in salmons and relatives, tunas and the opah (Lampris sp.). The occurrence of peculiar ecological (e.g. anadromous migration) and physiological (e.g. red-muscle endothermy) strategies in these lineages might explain the reacquisition of osteocytes. Our review supports that the main contribution of osteocytes in teleost bone is to mineral homeostasis (via osteocytic osteolysis) and not to strain detection or bone remodelling, helping to clarify their role in bone physiology.

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Section: Phylogenetic Distribution Of Acellular Bonesupporting

confidence: 63%

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

et al. 2019

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“…Some authors consider that true anaspids are only those taxa that possess tri-radiate post-branchial spines: this includes the scaled anaspids, or birkeniids, and members of the genus Lasanius (Arsenault & Janvier, 1991;Blom, 2012;Blom et al, 2002;Janvier, 1996bJanvier, , 1996c. We favour the more inclusive view whereby the 'naked-anaspids' or Jamoytiiformes, a group that shares with other anaspids the possession of a strongly hypocercal tail, are nested within the Anaspida (Blom & Märss, 2010;Chevrinais et al, 2018;Keating & Donoghue, 2016;Kiaer, 1924;Robertson, 1941;Stensiö, 1939;von Zittel & Woodward, 1902).…”

Section: Anaspidamentioning

confidence: 92%

A critical appraisal of appendage disparity and homology in fishes

2019

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Fishes are both extremely diverse and morphologically disparate. Part of this disparity can be observed in the numerous possible fin configurations that may differ in terms of the number of fins as well as fin shapes, sizes and relative positions on the body. Here, we thoroughly review the major patterns of disparity in fin configurations for each major group of fishes and discuss how median and paired fin homologies have been interpreted over time. When taking into account the entire span of fish diversity, including both extant and fossil taxa, the disparity in fin morphologies greatly complicates inferring homologies for individual fins. Given the phylogenetic scope of this review, structural and topological criteria appear to be the most useful indicators of fin identity. We further suggest that it may be advantageous to consider some of these fin homologies as nested within the larger framework of homologous fin‐forming morphogenetic fields. We also discuss scenarios of appendage evolution and suggest that modularity may have played a key role in appendage disparification. Fin modules re‐expressed within the boundaries of fin‐forming fields could explain how some fins may have evolved numerous times independently in separate lineages (e.g., adipose fin), or how new fins may have evolved over time (e.g., anterior and posterior dorsal fins, pectoral and pelvic fins). We favour an evolutionary scenario whereby median appendages appeared from a unique field of competence first positioned throughout the dorsal and ventral midlines, which was then redeployed laterally leading to paired appendages.

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“…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.…”

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confidence: 99%

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

O'Shea

Keating

Donoghue

2019

Journal of Morphology

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Osteostracans are the closest jawless relatives of jawed vertebrates, informing the gradual assembly of the vertebrate mineralised skeleton. Conflicting interpretations of their dermal skeletal histology arise from failure to account for topological variation, obscuring their significance in elucidating vertebrate skeletal evolution. To resolve this, we characterize the cranial and trunk dermal skeleton of a single individual of Tremataspis mammillata (Osteostraci, Thyestiida) at submicron resolution using synchrotron‐ and computed‐ tomography. Our results show that the architecture of the Tremataspis dermal skeleton is, for the most part, conserved over the skeleton and is broadly consistent with previous histological hypotheses based on 2D thin section study. We resolve debate over the homology of the basal layer, identifying it as osteogenic acellular isopedin rather than odontogenic elasmodine or metaplastic ossification of the stratum compactum of the dermis. We find topological variation between all dermal skeletal elements studied, and particularly between the cranial and postcranial dermal skeleton. This variation can be largely explained by reduction in differentiation due to geometric constraints imposed within smaller skeletal elements, such as scales. Our description of the dermal skeleton of Tremataspis mammillata provides a foundation for interpreting data from cursory topological samples of dermal skeletal diversity obtained in other osteostracans. This reveals general aspects of histological structure that must be ancestral for osteostracans and, likely, ancestral jawed vertebrates. Finally, we draw the distinction between hypotheses and descriptions in palaeohistology.

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Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton

Cited by 57 publications

References 40 publications

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

A critical appraisal of appendage disparity and homology in fishes

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

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