Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus

Abstract

The numerous cushion-shaped tooth-bearing plates attributed to the stem group osteichthyan Lophosteus superbus, which are argued here to represent an early form of the osteichthyan inner dental arcade, display a previously unknown and presumably primitive mode of tooth shedding by basal hard tissue resorption. They carry regularly spaced, recumbent, gently recurved teeth arranged in transverse tooth files that diverge towards the lingual margin of the cushion. Three-dimensional reconstruction from propagation phase-contrast synchrotron microtomography (PPC-SRµCT) reveals remnants of the first-generation teeth embedded in the basal plate, a feature never previously observed in any taxon. These teeth were shed by semi-basal resorption with the periphery of their bases retained as dentine rings. The rings are highly overlapped, which evidences tooth shedding prior to adding the next first-generation tooth at the growing edge of the plate. The first generation of teeth is thus diachronous. Successor teeth at the same sites underwent cyclical replacing and shedding through basal resorption, producing stacks of buried resorption surfaces separated by bone of attachment. The number and spatial arrangement of resorption surfaces elucidates that basal resorption of replacement teeth had taken place at the older tooth sites before the addition of the youngest first-generation teeth at the lingual margin. Thus, the replacement tooth buds cannot have been generated by a single permanent dental lamina at the lingual edge of the tooth cushion, but must have arisen either from successional dental laminae associated with the individual predecessor teeth, or directly from the dental epithelium of these teeth. The virtual histological dissection of these Late Silurian microfossils broadens our understanding of the development of the gnathostome dental systems and the acquisition of the osteichthyan-type of tooth replacement.

Diverse stem-chondrichthyan oral structures and evidence for an independently acquired acanthodid dentition

“…However, it is difficult to assess whether non-shedding parasymphyseal whorls are homologous due to the unclear condition in psarolepids (variably interpreted as stem sarcopterygians or stem osteichthyans (48-52)), in which a whorl is inferred (48,52) but is yet to be described. Finally, the interposition of many non-shedding stem-chondrichthyan taxa between shedding chondrichthyans and shedding osteichthyans confirms that a shedding dentition evolved twice, in two different ways, in crown-gnathostomes (7,10) (3,5,8,11,16,32,41,45,53,54).…”

“…The advent of micro-computed tomography has led to a renewed interest in tooth evolution and development in 'placoderms' (3)(4)(5) and osteichthyans (6)(7)(8)(9)(10). However, 'acanthodians', the earliest-branching members of the chondrichthyan total-group, have received comparatively little study (but see: (11)(12)(13)), despite a bewildering array of dermal oral structures (e.g.…”

Retention of fish-like odontode overgrowth in Permian tetrapod dentition supports outside-in theory of tooth origins

“…The teeth are offset horizontally from one another, indicating that there are no fixed tooth loci (electronic supplementary material, figure S1). The lack of traditionally lingually organized tooth rows or loci in the stem osteichthyans Andreolepis and Lophosteus has led other authors to propose that teeth formed without a fixed lingual location do not come from a traditional permanent dental lamina [26,27].…”

Dental ontogeny in the most primitive bony fishLophosteusreveals the developmental relationship between teeth and dermal odontodes

“…Albeit not basal, the resorption surfaces are wide open, not only to the next added tooth, but also to the replacement tooth bud that formed immediately above them ( Figure 6C-F). In the same way as those of the tooth cushions (the primitive form of inner dental arcades; Chen et al, 2017), the first-generation teeth thus establish the tooth positions for the cyclic replacement teeth. The addition of new first-generation teeth to the lingual ends of tooth files, and the deposition of replacement teeth onto the labial tooth sockets of these files, are likely parallel processes.…”

“…Kosoraspis show no sharp demarcation between teeth and ornament. Kosoraspis-like tooth-ornament gradation is combined with cyclic tooth shedding in Lophosteus (Botella et al, 2007;Chen et al, 2017), as well as in the oldest known stem osteichthyan Andreolepis (424 million years old; Chen et al, 2016). Radotina displays stellate teeth that are extremely similar to the stellate dermal odontodes, which is the characteristic ornament of 'acanthothoracids'.…”