Abstract
Two major skeletal systems—the endoskeleton and exoskeleton—are recognized in vertebrate evolution. Here, we propose that these two systems are distinguished primarily by their relative positions, not by differences in embryonic histogenesis or cell lineage of origin. Comparative embryologic analyses have shown that both types of skeleton have changed their mode of histogenesis during evolution. Although exoskeletons were thought to arise exclusively from the neural crest, recent experiments in teleosts have shown that exoskeletons in the trunk are mesodermal in origin. The enameloid and dentine-coated postcranial exoskeleton seen in many vertebrates does not appear to represent an ancestral condition, as previously hypothesized, but rather a derived condition, in which the enameloid and dentine tissues became accreted to bones. Recent data from placoderm fossils are compatible with this scenario. In contrast, the skull contains neural crest-derived bones in its rostral part. Recent developmental studies suggest that the boundary between neural crest- and mesoderm-derived bones may not be consistent throughout evolution. Rather, the relative positions of bony elements may be conserved, and homologies of bony elements have been retained, with opportunistic changes in the mechanisms and cell lineages of development.
Highlights
Two major skeletal systems—the endoskeleton and exoskeleton—are recognized in vertebrate evolution
Because vertebrate skeletons can be viewed as aggregates of apparently discrete units, namely bones, they have attracted the interest of comparative anatomists since even before the dawn of the concept of evolution [2]
Before the concept of evolution was established, two distinct types of bones were recognized in vertebrate skeletons and were thought to reflect their embryonic development; whether the bone arose from a cartilaginous precursor or not (e.g., [9,10])
Summary
“Is histological development as complete a test of homology as morphological development?” (Huxley, 1864 [1]: 296). A recent study tracing the lineages of transgenic cells revealed that trunk neural crest cells do not generate a skeletogenic tissue (that is, ectomesenchyme) [76] they have skeletogenic potential in the developing head [122] These lines of evidence, in combination with the fossil evidence from placoderms [52,53] (see above), suggest that the exoskeleton of the trunk develops from the mesoderm in the ancestral condition in the jawed vertebrates and that accretions of the enameloid and dentine tissues (i.e., odontogenic component) to the trunk exoskeleton occurred in many lineages, distinct from what had previously been hypothesized (e.g., [127]). Transgenic and chimeric approaches have revealed that the cranium of the frog violates generally accepted rules of development—that is, the developmental origins of the visceral arch and craniofacial skeletons are not found in a canonical set of crest cell streams that are divided into mandibular, hyoid, and branchial arch streams; instead, morphologically homologous dermal elements are derived from inconsistent cell lineages in frog embryos (Figure 6D-F) [111,138].
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