Abstract

Central to the story of vertebrate evolution is the origin of the vertebrate head, a problem difficult to approach using paleontology and comparative morphology due to a lack of unambiguous intermediate forms. Embryologically, much of the vertebrate head is derived from two ectodermal tissues, the neural crest and cranial placodes. Recent work in protochordates suggests the first chordates possessed migratory neural tube cells with some features of neural crest cells. However, it is unclear how and when these cells acquired the ability to form cellular cartilage, a cell type unique to vertebrates. It has been variously proposed that the neural crest acquired chondrogenic ability by recruiting proto-chondrogenic gene programs deployed in the neural tube, pharynx, and notochord. To test these hypotheses we examined the expression of 11 amphioxus orthologs of genes involved in neural crest chondrogenesis. Consistent with cellular cartilage as a vertebrate novelty, we find that no single amphioxus tissue co-expresses all or most of these genes. However, most are variously co-expressed in mesodermal derivatives. Our results suggest that neural crest-derived cartilage evolved by serial cooption of genes which functioned primitively in mesoderm.

Highlights

  • The transition from sessile filter feeding to active predation in the vertebrate lineage was made possible by the evolution of a robust head skeleton

  • Most vertebrate craniofacial cartilages and all pharyngeal cartilages are derived from the neural crest[1], a migratory and multipotent cell population formed at the edges of the nascent central nervous system

  • In this study we examined whether any tissue in the basal chordate amphioxus could be considered an evolutionary precursor, or latent homolog[33], of neural crest-derived cartilage. We reasoned that such a tissue should broadly co-express most factors required for neural crest chondrogenesis, including upstream transcriptional regulators and downstream markers of overt cartilage differentiation

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Summary

Introduction

The transition from sessile filter feeding to active predation in the vertebrate lineage was made possible by the evolution of a robust head skeleton. Several genes mark post-migratory cranial neural crest cells as they populate the pharynx and form cartilage These genes can be classified into three groups based on their expression patterns and demonstrated regulatory interactions (Figure 1A). The first set of genes is expressed broadly in neural crest cells during migration, and persists at high levels in postmigratory cranial neural crest This group includes, but is not limited to, Sox9[7] (SoxE), Sox5/6[8] (SoxD), Twist1/2[9], Id2/ 3[10], and Ets1/2[11]. Essential for the differentiation of neural crest-derived cartilage are two classes of signaling molecules, FGFs[20] and endothelins[21] These factors are secreted from adjacent pharyngeal endoderm and overlying ectoderm and are necessary for both cartilage differentiation and patterning via Dlx, Msx, Hand, Bapx, and Gsc transcription factors[21]

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