Abstract

The evolution of oral teeth is considered a major contributor to the overall success of jawed vertebrates. This is especially apparent in cartilaginous fishes including sharks and rays, which develop elaborate arrays of highly specialized teeth, organized in rows and retain the capacity for life-long regeneration. Perpetual regeneration of oral teeth has been either lost or highly reduced in many other lineages including important developmental model species, so cartilaginous fishes are uniquely suited for deep comparative analyses of tooth development and regeneration. Additionally, sharks and rays can offer crucial insights into the characters of the dentition in the ancestor of all jawed vertebrates. Despite this, tooth development and regeneration in chondrichthyans is poorly understood and remains virtually uncharacterized from a developmental genetic standpoint. Using the emerging chondrichthyan model, the catshark (Scyliorhinus spp.), we characterized the expression of genes homologous to those known to be expressed during stages of early dental competence, tooth initiation, morphogenesis, and regeneration in bony vertebrates. We have found that expression patterns of several genes from Hh, Wnt/β-catenin, Bmp and Fgf signalling pathways indicate deep conservation over ~450 million years of tooth development and regeneration. We describe how these genes participate in the initial emergence of the shark dentition and how they are redeployed during regeneration of successive tooth generations. We suggest that at the dawn of the vertebrate lineage, teeth (i) were most likely continuously regenerative structures, and (ii) utilised a core set of genes from members of key developmental signalling pathways that were instrumental in creating a dental legacy redeployed throughout vertebrate evolution. These data lay the foundation for further experimental investigations utilizing the unique regenerative capacity of chondrichthyan models to answer evolutionary, developmental, and regenerative biological questions that are impossible to explore in classical models.

Highlights

  • Derived dentitions (Juuri et al, 2013)

  • Despite diversity in form and function, a major finding of this wider research is that the molecular basis of tooth development, including the reciprocal interactions between odontogenic mesenchyme and a competent epithelium, and many of the genes involved in this coordinated cross-talk (Thesleff and Sharpe, 1997; Tucker and Sharpe, 2004; Zhang et al, 2005) is a highly stable process; this conservation has been maintained for approximately 450 million years of vertebrate evolution (Fraser et al, 2004; Hariharan et al, 2015; Smith et al, 2015)

  • The odontogenic band (OB) is a field of epithelial cells that marks a region from which the teeth, coincident dental lamina, and other supporting structures form in sharks, including the closely associated rows of taste buds (Figs. 1C, D, and 2)

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Summary

Introduction

Derived dentitions (Juuri et al, 2013). A deeper understanding of the extreme regenerative potential of diverse vertebrate dentitions may forward these goals. Despite diversity in form and function, a major finding of this wider research is that the molecular basis of tooth development, including the reciprocal interactions between odontogenic (neural-crest derived) mesenchyme and a competent epithelium, and many of the genes involved in this coordinated cross-talk (Thesleff and Sharpe, 1997; Tucker and Sharpe, 2004; Zhang et al, 2005) is a highly stable process; this conservation has been maintained for approximately 450 million years of vertebrate evolution (Fraser et al, 2004; Hariharan et al, 2015; Smith et al, 2015) This deep developmental conservation of morphogenetic mechanisms and gross evolutionary stability of a dental gene regulatory network suggests that diversity in vertebrate dentitions, whether tooth shape, number, or regenerative potential must be related to repeated regulatory ‘tinkering’ (Jacob, 1977; Lieberman and Hall, 2007) of the same core conserved gene network in different lineages (Bei, 2009; Fraser et al, 2013; Jernvall and Thesleff, 2012). The dissemination of genomic data from these important vertebrates will accelerate their use as models in the study of evolutionary developmental biology

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