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Abstract
The vertebral column is a key component of the jawed vertebrate (gnathostome) body plan, but the primitive embryonic origin of this skeleton remains unclear. In tetrapods, all vertebral components (neural arches, haemal arches and centra) derive from paraxial mesoderm (somites). However, in teleost fishes, vertebrae have a dual embryonic origin, with arches derived from somites, but centra formed, in part, by secretion of bone matrix from the notochord. Here, we test the embryonic origin of the vertebral skeleton in a cartilaginous fish (the skate, Leucoraja erinacea) which serves as an outgroup to tetrapods and teleosts. We demonstrate, by cell lineage tracing, that both arches and centra are somite-derived. We find no evidence of cellular or matrix contribution from the notochord to the skate vertebral skeleton. These findings indicate that the earliest gnathostome vertebral skeleton was exclusively of somitic origin, with a notochord contribution arising secondarily in teleosts.
Highlights
The presence of vertebrae is a defining feature of the vertebrate body plan
A vertebral skeleton may consist of a series of paired neural arches that cover the spinal cord, paired haemal arches that enclose the caudal artery and vein, and, in many jawed vertebrates, a series of centra that replace the notochord as the predominant support structure
We show that all components of the skate vertebral skeleton derive from paraxial mesoderm, with no evidence for cellular or matrix contributions from the notochord
Summary
The presence of vertebrae is a defining feature of the vertebrate body plan. A vertebral skeleton may consist of a series of paired neural arches that cover the spinal cord, paired haemal arches that enclose the caudal artery and vein, and, in many jawed vertebrates (gnathostomes), a series of centra that replace the notochord as the predominant support structure. Vertebral centra are highly variable in terms of morphology and tissue composition, and likely evolved independently in many different gnathostome lineages, including tetrapods, teleost fishes and cartilaginous fishes [1]. This apparent evolutionary convergence raises questions about the embryonic origin of vertebral skeletal elements across gnathostomes. In teleost ray-finned fishes, the vertebral skeleton appears to have a dual embryonic origin, with contributions from both paraxial mesoderm and the notochord. We use somite and notochord fate mapping experiments, as well as mRNA in situ hybridization for genes encoding skeletal matrix proteins, to test the embryonic origin of the skate vertebral skeleton. In situ hybridization experiments for Col1a1 (GenBank accession number MG017616) and SPARC (GenBank accession number MG017615) were performed on sections as described in O’Neill et al [17], with modifications according to Gillis et al [19]
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