Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development

Abstract

The stratigraphically earliest and the most primitive examples of vertebrate skeletal mineralization belong to lineages that are entirely extinct. Therefore, palaeontology offers a singular opportunity to address the patterns and mechanisms of evolution in the vertebrate mineralized skeleton. We test the two leading hypotheses for the emergence of the four skeletal tissue types (bone, dentine, enamel, cartilage) that define the present state of skeletal tissue diversity in vertebrates. Although primitive vertebrate skeletons demonstrate a broad range of tissues that are difficult to classify, the first hypothesis maintains that the four skeletal tissue types emerged early in vertebrate phylogeny and that the full spectrum of vertebrate skeletal tissue diversity is explained by the traditional classification system. The opposing hypothesis suggests that the early evolution of the mineralized vertebrate skeleton was a time of plasticity and that the four tissue types did not emerge until later. On the basis of a considerable, and expanding, palaeontological dataset, we track the stratigraphic and phylogenetic histories of vertebrate skeletal tissues. With a cladistic perspective, we present findings that differ substantially from long-standing models of tissue evolution. Despite a greater diversity of skeletal tissues early in vertebrate phylogeny, our synthesis finds that bone, dentine, enamel and cartilage do appear to account for the full extent of this variation and do appear to be fundamentally distinct from their first inceptions, although why a higher diversity of tissue structural grades exists within these types early in vertebrate phylogeny is a question that remains to be addressed. Citing recent evidence that presents a correlation between duplication events in secretory calcium-binding phosphoproteins (SCPPs) and the structural complexity of mineralized tissues, we suggest that the high diversity of skeletal tissues early in vertebrate phylogeny may result from a low diversity of SCPPs and a corresponding lack of constraints on the mineralization of these tissues.

Chronology of early Cambrian biomineralization

“…They are regarded as the earliest known biomineralized chordates (Donoghue, Forey & Aldridge, 2000;Donoghue, Sansom & Downs, 2006). There is a microstructural similarity between the two sub-groups as well as a histological and morphological transition from paraconodonts to euconodonts, and therefore they are united as conodonts (Szaniawski & Bengtson, 1993 (Müller, 1959(Müller, , 1971Dong, 2004) and from Stage 5 deposits of Alaska (Dutro et al 1984), but the former is much better preserved and constrained stratigraphically.…”

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

“…Wang et al (2005) and Donoghue et al (2006) drew comparison between the basal plywood-like layer in heterostracans and osteostracans and the basal 'isopedin' layer of the osteichthyan dermal skeleton. The growth of this tissue layer was first considered by Stensi€ o (1927).…”

“…The dermal skeleton of osteostracans comprises a superficial layer of dentine tubercles surmounted by enameloid caps, a vascular middle layer (equivalent to L2) constructed of true osteons (with osteocyte lacunae) and a lamellar basal layer (equivalent to L3) comparable to isopedin (Gross, 1935(Gross, , 1961Denison, 1951;Smith and Hall, 1990;Donoghue et al, 2006). Giles et al (2013) demonstrated that this dermal architecture is also plesiomorphic with respect to placoderms, regardless of whether they are perceived as monophyletic or paraphyletic.…”

“…Thus, there is a lack of experimental models representative of distinct grades in the evolutionary assembly of the vertebrate skeleton. However, 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).…”

“…1). It is in this skeletal system that the canonical skeletal cell and tissue types are apparent from the first (Donoghue et al, 2000;Donoghue and Sansom, 2002), with dermal bones comprising acellular bone surmounted by tooth-like tubercles composed of enameloid, dentine and bone of attachment (Donoghue et al, 2006). The dermal skeleton comprises much of the skull table of fishes, along with their boney scales-reduced in tetrapods to little more than the frontal bones of the face, palate and part of the shoulder girdle (Le Douarin and Kalcheim, 1999).…”