Abstract
ABSTRACTLiving 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.
Highlights
The vertebrate mineralised skeleton and its canonical cell and tissue types are among the most formative innovations in vertebrate evolutionary history
Each tubercle contains a network of vascular canals, interpreted as pulp canals, about which dentine is developed centripetally, and from which highly polarised odontoblast canaliculi radiate
We have found no direct evidence of such a tissue in the dermal skeleton of any heterostracan, it is possible that L1 develops via resorption of the bone of attachment during ontogeny
Summary
The vertebrate mineralised skeleton and its canonical cell and tissue types are among the most formative innovations in vertebrate evolutionary history. Their origins are poorly understood because living vertebrates either lack or possess all of the component mineralised skeletal systems in their entirety. There is a rich fossil record of jawless and jawed vertebrates, characterised as the ‘ostracoderms’, that record this episode (Donoghue and Purnell, 2005), revealing the gradual assembly of mineralised skeletal systems manifest in living jawed vertebrates (Donoghue and Sansom, 2002; Donoghue et al, 2006; Giles et al, 2013)
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