Australia: The Land Where Time Began

A biography of the Australian continent 

Jawed Vertebrates - Marginal Dentition and Multiple Dermal Jawbones as Ancestral Condition

In extant fishes and land vertebrates the dentitions vary in patterns as well as type of tooth replacement. The common ancestral condition has been argued to have been likely to have resembled the nonmarginal, radially-arranged tooth files of arthrodires, which were an early group of armoured fishes. In this study microtomography was used to describe the fossil dentitions of acanthothoracids, the most basal, phylogenetically, group of jawed vertebrates that had teeth of the genera Radotina, Kosoraspis, and Tlamaspis (that were found in Early Devonian deposits in the Czech Republic). The dentitions of these genera differ fundamentally from those of arthrodires; they are marginal, carried by cheek bones or a series of short dermal bones along the edges of the jaw, and teeth are added lingually, as is the case in many chondrichthyans (cartilaginous fish) and osteichthyans (bony fish and tetrapods). Vaškaninová et al. proposed these characteristics as ancestral for all jawed vertebrates.

One of the key events in evolutionary history from jawless to jawed vertebrates was the origin of teeth. There are whorl-like tooth files arranged transversely with lingual addition in stem osteichthyans (Botella et al., 2007; Chen et al., 2016) and most chondrichthyans (Smith & Coates, 2001).Teeth are added in diverging files from the progenitor tooth or region in arthrodires, a clade of jawed stem gnathostomes, and the number of files is highly variable, and addition can be labial as well as lingual or longitudinal (Smith, 2003; Ørvig, 1980; Sith & Johanson, 2003; Smith & Johanson, 2003; Rücklin et al., 2012; Hu et al., 2019). A proposed evolutionary succession (Zhu et al., 2016) in which a bridge is formed between an arthrodire-like condition (which is assumed to be primitive for jawed vertebrates) and the osteichthyan condition (assumed to be primitive for the crown gnathostomes), as the result of a recent discovery of osteichthyan-like marginal dermal jawbones combined with an arthrodire-like body plan in Entelognathus and Qilinyu (Zhu et al., 2013; Zhu et al., 2016). The dentitions of Entelognathus and Qilinyu are, however, poorly understood.

In this study dentitions have been presented of the acanthothoracid stem gnathostomes Radotina, Kosoraspis, and Tlamaspis from the Early Devonian of the Czech Republic, and the only described acanthothoracid dentition, specimen CPW.9 from the Canadian Arctic (mistakenly assigned to Romundina by some authors) (Smith & Johanson, 2003; Goujet & Young, 2004) has been re-examined. The only jawed vertebrates that have an anteriorly projecting precerebral trabecula region (Dupret et al., 2014) are the Acanthothoracids, antiarchs and Brindabellaspis (Young, 1980). This distinctive facial geometry resembles those of jawless stem gnathostomes especially galeaspids (Kuratani & Ahlberg, 2016). Antiarchs, Brindabellaspis, and acanthothoracids as basal to other jawed vertebrates (Zhu et al., 2016; Dupret et al., 2014; Qiao et al., 2016), a position they retain when the (not analysed previously) genera that are discussed herein are included in the analysis. The jaws and dentition of Brindabellaspis are not known, whereas antiarchs don’t have teeth (Young, 1984). The teeth of acanthothoracids have, therefore, the unique potential to illuminate the origin of vertebrate dentition. In the dentition of CPW.9, the tooth addition, which comprises a pair of supragnathal plates on a snout (Goujet & Young, 2004), has been described as concentric (Smith & Johanson, 2003; Smith, Clark, Goujet & Johanson, 2017). As a result of this, a dermal tessera that is detached that has concentrically arranges odontodes from the same formation was misinterpreted as an acanthothoracid supragnathal (Smith, Clark, Goujet & Johanson, 2017; Rücklin & Donoghue, 2015; Burrow, Hu & Young, 2016). By reanalysing micro-computed tomography (micro-CT) scans of CPW.9 the supragnathals suture labially with the dermal premedian plate. Tooth Addition is radial, in fact, from a labial founder region, and there is no addition of a labial tooth. The oldest small teeth in the founder region become overgrown by larger dermal odontodes instead, as was observed in the stem osteichthyans Andreolepis (Chen et al., 2016).

In this study propagation phase contrast synchrotron microtomography was used, and the previously unknown dentition of Radotina, Kosoraspis, and Tlamaspis was discovered (Vaškaninová & Ahlberg, 2017). All differ substantially from that of CPW.9. The dentition of Radotina was comprised of 4 rows of teeth that were carried on the ventral face of a large dermal cheek bone that was sutured to the external surface of the palatoquadrate. A ventral trough is formed by this ventral face, and the teeth are carried on the labial flank and the floor of the trough that is marked by a row of vascular grooves. The dentition is, therefore, unambiguously marginal, and is located inside the margin of the jaw but external to the palatoquadrate, and a distinct labial edge of exposed bone from the external surface of the cheek. Addition of tooth rows is from the lingual side, and there is a pronounced mineralisation gradient from the oldest to the youngest teeth (S4). The shape of the teeth is elongated bladelike stellate that matches that of dermal ornament odontodes on the tesserae of the cheek. Unlike those odontodes, however, a distinct basal attachment tissue fuses the teeth into rows. The arms of the stellate teeth, which consist of pallial mesodentine, is attached to a central cone of circumpulpal semidentine (Ørvig, 1997; Ørvig, 1875). The large spaces of odontoblast clusters that are enclosed in the arms anastomose with the small, sparser cell spaces in the cone, across the boundary between the pallial and circumpulpal dentine. Each arm is equipped with a blade that is enameloid coated. This is shown to be a functional cutting dentition by well-developed use facets on the teeth. A broken tooth in the lingualmost row has been repaired with a new crown inserted into the break, and there is no evidence of resorption or replacement. There are multiple short jawbones that bear teeth in Kosoraspis (Gross, 1959) and Tlamaspis (Vaškaninová & Ahlberg, 2017). In Kosoraspis their length and shape vary according to their position, though they invariably bear a prominent facial Lamina. The facial lamina carries tooth like odontodes that grade into recurved, pointed teeth on the oral lamina, forming whorl-like files that are obliquely transverse, resembling the first generation tooth-like odontodes and non-shedding teeth in Andreolepis (Chen et al., 2016). Their shape differs from the stellate odontodes on the cheek. The odontodes and teeth both consist of parallel semidentine and the circumpulpal dentine that infills the pulp cavity in mature teeth is an atubular dentinous tissue with fewer cell spaces that are enclosed. The facial lamina of Tlamaspis, by contrast, is mostly unornamented labially, with the exception of 2 or 3 rows of tubercles that abruptly transition into a single row of conical teeth, which are bordered lingually by a toothless flange. Though the teeth are not shed or replaced this is reminiscent of the marginal jawbones of crown osteichthyans. In this case the histology of the tooth is not known.

Acanthothoracids are separated from the gnathostome crown group by 4 internodes in the phylogenetic analysis that was undertaken in this study. There are, nevertheless, distinct similarities between dentitions acanthothoracids and osteichthyans. There are, notably, short dermal jawbones, which are to those of Kosoraspis Tlamaspis, are present in the stem osteichthyan Lophosteus, which has acanthothoracid-like dermal ornament (Jerve et al., 2016). In Kosoraspis the cheek pattern also approaches closely that of primitive crown osteichthyans (Zhu, Yu & Janvier, 1999). Vaškaninová et al. suggested that the possibility that the gnathostome crown is rooted close to acanthothoracids, with arthrodires as well as certain other so-called placoderm groups forming a divergent clade rather than a paraphyletic segment of the gnathostome stem, should be seriously considered.

The acanthothoracid dentitions that are newly described exhibit a combination of shared characteristics and remarkable diversity. There are functional and architectural aspects to the diversity of dentitions. It appears that the dentition of CPW.9 is functionally adapted to crushing, that of Radotina for cutting, and those of Kosoraspis and Tlamaspis adapted for different styles of grasping and piercing. The most striking distinction is, architecturally, between Radotina in which the teeth resemble ornament odontodes and are attached to the cheek plate – and the 3 other taxa, all with separate dermal jawbones and have teeth that do not resemble their dermal ornament. The teeth in all the dentitions are non-shedding and no evidence has been found of resorption. All are carried by dermal bones that have either ornamented facial laminae or (as in the case of CPW.9) suture to facial bones; none show labial tooth addition. Among the least crownwards jawed vertebrates their phylogenetic position suggests that both marginal dermal jawbones, are ancestral for all gnathostome dentitions.

Vaškaninová, V., et al. (2020). "Marginal dentition and multiple dermal jawbones as the ancestral condition of jawed vertebrates." Science 369(6500): 211-216.