Origin and early evolution of vertebrate skeletonization

Abstract

Data from living and extinct faunas of primitive vertebrates imply very different scenarios for the origin and evolution of the dermal and oral skeletal developmental system. A direct reading of the evolutionary relationships of living primitive vertebrates implies that the dermal scales, teeth, and jaws arose synchronously with a cohort of other characters that could be considered unique to jawed vertebrates: the dermoskeleton is primitively composed of numerous scales, each derived from an individual dental papilla; teeth are primitively patterned such that they are replaced in a classical conveyor-belt system. The paleontological record provides a unique but complementary perspective in that: 1) the organisms in which the skeletal system evolved are extinct and we have no recourse but to fossils if we aim to address this problem; 2) extinct organisms can be classified among, and in the same way as, living relatives; 3) a holistic approach to the incorporation of all data provides a more complete perspective on early vertebrate evolution. This combined approach is of no greater significance than in dealing with the origin of the skeleton and, combined with recent discoveries and new phylogenetic analyses, we have been able to test and reject existing hypotheses for the origin of the skeleton and erect a new model in their place.

Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): Differential involvement in the visceral skeleton and braincase

“…It is well known that the visceral arch skeleton is evolutionarily older than the neurocranium. A visceral arch skeleton, albeit of noncollagenous nature and non-neural crest-derived, is already present in nonvertebrate chordates such as Amphioxus, which lack a braincase (De Beer, 1937;Donoghue and Sansom, 2002). Only later, in the earliest vertebrates, was the splanchnocranium enlarged and its development taken over by neural crest.…”

“…Only later, in the earliest vertebrates, was the splanchnocranium enlarged and its development taken over by neural crest. A neurocranium arose in basal vertebrates (Donoghue and Sansom, 2002), largely from mesodermal mesenchyme. Some elements, although functionally related to the neurocranium, have been argued to be evolutionary related to the splanchnocranium, in particular the trabeculae, and the prevomer and parasphenoid bone (De Beer, 1937;Daget, 1964;Kuratani et al, 1997).…”

“…These bones have a separate evolutionary origin (Smith and Hall, 1990;Donoghue and Sansom, 2002) and cannot replace each other, not phylogenetically, not ontogenetically (Patterson, 1977). During vertebrate evolution, the relative participation of cartilage bones and dermal bones in building the skeleton has changed significantly.…”

“…The neural crest typically supplies the branchial arches of the splanchnocranium with mesenchyme from which cartilages and bones differentiate. In the neurocranium, the embryonic origin of the cartilages and bones (whether neural crest or mesoderm-derived) is less clear; some components, e.g., occipital bones, being derived from transformed vertebrae, are obviously mesodermal, whereas others, like the nasal capsules, are without doubt neural crest-derived, at least in jawed vertebrates (Donoghue and Sansom, 2002). Given the separate evolutionary origin of neurocranium versus splanchnocranium, and of cartilage bones versus dermal bones, one can hypothesize that these different categories of bones show differences in the molecular control underlying their differentiation process.…”

Significance of the cranial neural crest

“…5). There are many fossil fish that display extensive postcranial exoskeletal coverings of dermal bone and dentine, two cells types that derive from neural crest cells (Maisey, 1988;Smith and Hall, 1990;Donoghue and Sansom, 2002). The skeletogenic potential of trunk crest is also expressed, albeit to a limited extent, in some extant vertebrates.…”