Spatial and temporal pattern for the dentition in the Australian lungfish revealed with sonic hedgehog expression profile

Abstract

We report a temporal order of tooth addition in the Australian lungfish where timing of tooth induction is sequential in the same pattern as osteichthyans along the lower jaw. The order of tooth initiation in Neoceratodus starts from the midline tooth, together with left and right ones at jaw position 2, followed by 3 and then 1. This is the pattern order for dentary teeth of several teleosts and what we propose represents a stereotypic initiation pattern shared with all osteichthyans, including the living sister group to all tetrapods, the Australian lungfish. This is contrary to previous opinions that the lungfish dentition is otherwise derived and uniquely different. Sonic hedgehog (shh) expression is intensely focused on tooth positions at different times corresponding with their initiation order. This deployment of shh is required for lungfish tooth induction, as cyclopamine treatment results in complete loss of these teeth when applied before they develop. The temporal sequence of tooth initiation is possibly regulated by shh and is know to be required for dentition pattern in other osteichthyans, including cichlid fish and snakes. This reflects a shared developmental process with jawed vertebrates at the level of the tooth module but differs with the lack of replacement teeth.

Evolution of developmental pattern for vertebrate dentitions: an oro‐pharyngeal specific mechanism

“…In order to examine timing and spatial pattern of tooth initiation, gene expression data for shh in three species of fish, S. canicula, O. mykiss and N. forsteri were compared (Fraser et al, 2004, 2006a, b; Smith et al, 2009a, c). This gene, associated with the initiation of each tooth, may be conserved through evolution and is expressed reiteratively during continuous tooth morphogenesis (Fraser et al, 2006a; Smith et al, 2009a, c). …”

“…The timing of the pattern in space and how this occurs is a topic of debate at present, as for example this pattern is different on each dentate bone for the rainbow trout, O. mykiss (Berkovitz and Moore, '74, '75). In the Australian lungfish ( N. forsteri ), only a single row of dentary teeth occurs and this is not added to by replacement teeth, but gene expression data has revealed that, in this divergent dentition, teeth form initially in the same sequence as in most osteichthyan fishes (Smith et al, 2009c). This temporal sequence for the dentary tooth field suggests a conserved pattern in tooth initiation order and is the proposed plesiomorphic state for osteichthyan dentitions.…”

“… shh expression in comparative stages marking the initial pattern regulation of the primary dentition within four fish groups. ( A – C ) The catshark Scyliorhinus canicula (Smith et al, 2009a); ( D – F ) the Rainbow Trout Oncorhynchus mykiss (Fraser et al, 2004); ( G – I ) a Malawi cichlid Labeotropheus fuelleborni (Fraser et al, 2008); ( J – L ) the Australian lungfish Neoceratodus forsteri (Smith et al, 2009c). Note how similar the stages of tooth initiation are in all species.…”

“…The most precise timing of individual tooth germs was obtained by use of in situ gene expression for shh in N. forsteri where it was shown to reveal a staggered sequence of timing across left and right sides of the tooth row at the margins of the lower jaw (Fig. 4J–L) (Smith et al, 2009c). Here we have illustrated the data from cleared skeletal preparations to see, at selected larval and hatchling stages, the tooth addition order (Fig.…”

“…Nearly all the information gathered on tooth development and associated genetic organization has emerged from studies on the mammalian dentition, specifically the mouse ( Mus musculus ). More recently, comparative gene expression data focused on the developing dentition has been collected from osteichthyan and chondrichthyan fish models including: the rainbow trout Oncorhynchus mykiss (Fraser et al, 2004, 2006a, b); the medaka, Oryzias latipes (Debiais‐Thibaud et al, 2007); the Mexican tetra, Astyanax mexicanus (Jackman et al, 2004; Stock et al, 2006); zebrafish, Danio rerio (Jackman et al, 2004; Stock et al, 2006); a selected set of Lake Malawi cichlid species (Fraser et al, 2008, 2009) and also, studies limited to a single gene ( sonic hedgehog ( shh )) from the catshark, S. canicula (Smith et al, 2009a, b, c), and from the lungfish, Neoceratodus forseri (Smith et al, 2009a, b, c). These all highlight vast genetic conservatism in tooth development.…”