The developmental relationship between teeth and dermal odontodes in the most primitive bony fish Lophosteus
- Department of Organismal Biology, Uppsala University, Sweden
- SciLifeLab, Uppsala University, Sweden
- European Synchrotron Radiation Facility, France
- Estonian Marine Institute, University of Tartu, Estonia
Figures
Figure 1
Odontode development and gnathostome phylogeny.
(A) Schematic representation of developing (left) and mature (right) odontode. The odontode shown here lacks enamel, as do the teeth and dermal odontodes of Lophosteus. (B) Phylogenetic position of Lophosteus and some of the other fossil taxa discussed in this paper. The extant gnathostome groups are represented by developmental model organisms, as follows: Holocephali, Callorhinchus milii; Elasmobranchi, Scyliorhinus torazame; Actinopterygii, Danio rerio; Sarcopterygii, Mus musculus. Tree topology from Qu et al., 2015 and Vaškaninová et al., 2020. Formal hierarchical categories indicated on right. Animal images from Trinajstic et al., 2013, except Callorhinchus, from Ryll et al., 2014, and Scyliorhinus, original.
Figure 2
Reconstructed ontogeny of the Lophosteus marginal jawbone relative to the development of the lateral line.
Block diagrams in antero-external view, aligned so that the biting margin maintains a fixed position (note that this causes the older parts of the bone to move away from the biting margin and rotate anticlockwise during growth). The founder ridges and the ornament-like tooth TR7-7 mark the labial rotation and drift of the tooth rows. (A) The initial odontodes are formed as founder ridges. (B) Isolated dermal odontodes and teeth are added sequentially in opposite direction, respectively attaining a stellate and conical morphology. The teeth are shed semi-basally, establishing replacement tooth positions. (C) Teeth are cyclically replaced at the positions set up by the first-generation teeth; the second-generation odontodes invade the oral domain lingually and form around the lateral line canal labially. Lines of resorption around the lateral line canal indicates bone remodeling (see Figure 4—figure supplement 6). Note, the replacement of teeth and the overgrowth of odontodes may have commenced before the addition of the ultimate first-generation teeth. (D) The ventral extension of the lateral line canal partially resorbs the second-generation odontodes at its ventral border; more tooth rows are overgrown by the third-generation odontodes after being rotated to the face; new tooth positions are inserted to compensate the embedded labial tooth positions. Curved arrows, examples of the adding or shedding of teeth or dermal odontodes. The buried part of teeth and dermal odontodes, the embedded resorption surfaces and bone mineralized at earlier stages become increasingly grey. The lateral line is represented by neuromasts and epithelial cells. The size and number of neuromasts is schematic and only represents their presence. Perspective view. Scale bar not applicable.
Figure 3 with 2 supplements
Gross morphology and digital disection of the Lophosteus marginal jawbone GIT 760–12.
(A) Photographs oriented with biting (presumed dorsal) margin at the top, in internal (left) and external (right) views. White box indicates region where internal structures have been fully modeled. (B) Antero-external view of a perspective block. (C) Antero-visceral view of a slab of the 3D histologic model through the midline of File 4. The most labial tooth positions have the shortest replacement history (TF5-3 has not been replaced); the marginal tooth positions have the longest replacement history (RC4-8 has been replaced 17 times), while the inserted tooth positions immediately labial to the marginal ones have the most recent history (TR4-10 has been replaced once).
Figure 3—figure supplement 1
Morphologic variation of the marginal jawbones in Lophosteus.
A, GIT 760–13; B, GIT 760–14; C, GIT 760–15; D, GIT 760–16; E, GIT 760–17; F, GIT 760–18; G, GIT 760–19; H, GIT 760–20; I, GIT 760–21; J, GIT 760–12; K, GIT 760–22; L, GIT 760–23; M, GIT 760–24; N, GIT 760–25; O, GIT 760–26; P, GIT 760–27; Q, GIT 760–28. 1, external view; 2, visceral view. l.l.g., lateral line groove, l.l.p., lateral line pore.
Figure 3—figure supplement 2
Virtual transverse sections between File 3 and 5.
Resorption surfaces are not highlighted in B to show the preservation and scan quality. Note, new positions are inserted into the marginal replacement column like a branch (TR4-10 into RC4-8 in A; TR3-10 into TR3-9 in B). Overgrowing odontodes that are deposited on top of a cusp have their pulp cavities squeezed (O3g-4, O3g-7) or divided (O3g-2), so the shape of the pulp cavities is not necessarily consistent with the crown. In the younger generations of facial odontodes, orthodentine is limited to the periphery, and the interior is filled by denteons, which turn into cellular osteons at the base (see Figure 4—figure supplements 2–6). In contrast, in the overgrowing odontodes on the oral lamina and the first-generation odontodes, pulp cavities are surrounded by acellular dentine, just as in the teeth. Dashed curve, putative extent of the jawbone when first mineralized, corresponding to the radiation center of feeder vessels in Figure 3C, and the large cuboidal osteocyte lacunae labeled in B and Figure 4—figure supplement 3. Dashed lines, sectioning planes of Figure 4—figure supplements 2–6. Asterisk, pulp cavity exposed by the extensive resorption during the development of the lateral line canal.
Figure 4 with 6 supplements
3D external view of the scanned area.
For three-dimensional curvature, see Figure 3. (A) External morphology with individually modeled structures highlighted in color. White arrowheads point to ornament-like teeth with side-cusps in the uncolored area. Bars in lavender and mint green indicate the putative gradient of the oral and dermal signal spheres, and the shift of the oral-dermal boundary during deposition of the first-generation (1g), second-generation (2g) and third-generation (3g) odontodes. (B) Overgrowing odontodes and bone matrix rendered invisible to show a consistent alternate pattern between replacement teeth, first-generation teeth and dermal odontodes dorsal to the lateral line canal. The replacement teeth at the inserted positions are not shown. Because the lingual rows of first-generation teeth are obscured by the labial rows of replacement teeth in this view, these rows are not shown (for all tooth rows, see Figure 5B). For optimal visibility, the most lingual rows of replacement teeth are represented by their pulp cavities. (C) Diagram of the alternate organization based on B. Solid lines, transverse files; numbers of files mark the putative level of the ossification center. Dashed lines, longitudinal rows; colored parts of the dashed lines indicate the range of the founder ridges. Dots denote positions of the structures in the particular colors. Note, the second-generation odontodes situated along the lingual border of the lateral line canal (O2g-3–2, O2g-7–2) have their labial ridgelets truncated, in order not to intrude on the canal sulcus. The alternate positions that are supposed to form the next row are suppressed (null signs), but the same alternate pattern develops properly on the other side of the canal (see Figure 4—figure supplement 1B). The dorsal edge of the odontodes at the ventral border of the canal is resorbed, leaving their pulp cavities open to the canal (asterisk; see Figure 3, O2g-3–3; Figure 4—figure supplement 1B, OP3-3, OP7-3; Figure 4—figure supplement 4). The ridgelets of the third-generation odontodes at both borders of the canal are also compressed (O3g-4, O3g-7).
Figure 4—figure supplement 1
3D external views (same as Figure 4) of the vascular system and the organization of facial ornament.
(A) All canals in the modeled area. Asterisk, exposed pulp cavity in Figures 2D and 4A. Dashed arrows, canals in yellow joining the radial vessels of preexisting odontodes is presumably from the epithelium, which indicates the development of an upcoming odontode at OP6-7, see B. (B) Radial vessels and pulp cavities of the overgrowing odontodes and replacement teeth are removed to expose the pulp cavities that are laid down directly on the basal bone. The labeled numbers indicate the non-overgrowing odontodes and teeth are organized in the same alternate files. The labial founder ridge possesses both odd- and even-number positions (see Figure 4—figure supplement 2); the first-generation odontode row (Row 1) crosses all the even-number files, taking every second position (0, 2, 4, 6); the second-generation odontodes only occupy every second odd-number position (1, 5 and 3, 7) in Row 2–4 and every second even-number position (2, 6) in Row 5; the third-generation odontodes occupy every third odd-number position (3, 9) in Row 6, with Row 7 predicted to occupy every third even-number position, including OP6-7. TR and TF, ranges of tooth replacement columns and first-generation teeth, indicating the putative drift of the oral epithelium. O1g, O2g, and O3g, ranges of the first, second, and third generations of dermal odontodes, indicating the expansion of the dermal epithelium. NB, new bone margin. Dashed oval, the next odontode predicted to be added at the new ventral margin. Arrows, the directions of the feeder vessels as they penetrate the bony plate from the ossification center, through the pulp cavities, to the openings on the internal surface and the lingual edge, see Figure 5A.
Figure 4—figure supplement 2
Slideshow of serial virtual thin sections — Slice A.
Sectioning planes are indicated by dashed line A in Figure 3—figure supplement 2B.
Figure 4—figure supplement 3
Slideshow of serial virtual thin sections — Slice B.
Sectioning planes are indicated by dashed line B in Figure 3—figure supplement 2B.
Figure 4—figure supplement 4
Slideshow of serial virtual thin sections — Slice C.
Sectioning planes are indicated by dashed line C in Figure 3—figure supplement 2B.
Figure 4—figure supplement 5
Slideshow of serial virtual thin sections — Slice D.
Sectioning planes are indicated by dashed line D in Figure 3—figure supplement 2B.
Figure 4—figure supplement 6
Slideshow of serial virtual thin sections — Slice E.
Sectioning planes are indicated by dashed line E in Figure 3—figure supplement 2B.
Figure 5
Occlusal view of the oral lamina.
(A-B) Numbering of tooth positions (TP). (A) Pulp cavities of the first-generation teeth and dermal odontodes. Arrows indicate the directions of the feeder vessels radiating from the ossification center. The feeder vessels in blue run longitudinally only beneath the first-generation teeth, but never do it labially, and these longitudinal feeder vessels may have penetrated the old oral lamina at the early stage. The horizontal vascular mesh in pink, which represents the new oral lamina beyond the first-generation teeth, supports the lingual replacement columns in the interval that lacks feeder vessels. (B) Pulp cavities of replacement teeth and overgrowing odontodes are added. For the feeder vessels, only those newly incorporated at the jaw margin are shown. Note, RC2-6 is covered by O3g-1, and RC6-6 is covered by O3g-5. Dashed oval, an example of the discontinuity of the pulp cavities between a first-generation tooth and its successive replacement teeth, which suggests the replacement of the first-generation tooth has been delayed, but the drift of the delayed replacement teeth still follows the same file. All inserted positions are also aligned with the tooth files of preexisting positions. (C-E) Comparison between the tooth replacement of File 2–3 and File 4–5. C is aligned to A. The successive resorption surfaces of RC2-4, which are similar to those of RC4-8, are not shown, except the last and the first basal resorption surface and the semi-basal resorption surface. Note, the resorption surfaces of RC4-8 gradually change in orientation and density. (F) Antero-occlusal view of the lingual founder ridge and the first-generation teeth showed in C, showing the transition from no resorption, via semi-basal resorption, to basal resorption, as the tooth rows increasingly overlap.
Figure 6
Postero-occlusal view of the tooth field invaded by overgrowing odontodes.
(A) First-generation teeth are shown. They are perfectly conical. (B) The final replacement teeth that will be buried by second-generation overgrowing odontodes are shown. They are still perfectly conical. (C) The final replacement teeth that will be buried by third-generation overgrowing odontodes are shown. They are more or less ornament-like, probably because of the approach of the dermal epithelium, which is represented by the second-generation overgrowing odontodes, during the tooth development. (D) The final replacement teeth of the inserted positions are shown. They are ornament-like, probably because of the approach of the dermal epithelium that generate the third-generation overgrowing odontodes. The dermal odontodes overgrowing the oral lamina do not develop a fully stellate morphology, only with few uncrenulated ridgelets. The most lingual ones tend to become longitudinally compressed, contrary to the longitudinal elongation of those on the facial lamina. Their side-cusps only develop labially and main cusps incline lingually. Note, since the invasive front line of the ornament (the oral-dermal boundary) is undulating, tooth morphology is not correlated with rows or generations, but with the proximity of dermal odontodes. (E) Spatial relationship between the pulp cavities of overgrowing odontodes and the teeth buried right below. Note, the labial positions function at the earlier stages, depending on how soon they are overgrown by ornament, and thus the final replacement teeth of the labial tooth rows are smaller than those of the lingual ones. Each position, even if in the same row, has a different replacement history, which can be revealed by the shape of pulp cavity; in a long-life position, the first-generation tooth and all its replacement teeth have their pulp cavities fused into a mushroom-like shape.
Videos
Video 1
Tooth addition and replacement of two alternate files.
Perspective view. The order of the structures appearing in the video is not strictly consistent with that in life. However, the sequence of developmental events can be inferred: except for the most labial ones, each first-generation tooth had been resorbed before the next, more lingual, tooth was added to the file. As the successive tooth positions in a file increasingly overlap, at a point, semi-basal resorption becomes completely basal, and the successive teeth in a file now take on the appearance of a replacement column. The marginal position is drifting and tilting lingually, with the basal resorption surfaces become increasingly tighter. 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. The former process constructs tooth files from the positions set up by the founder ridges via semi-basal resorption, and the latter builds replacement columns at each position via basal resorption. The replacement cycles of the labial positions are terminated by the overgrowth of ornament. But where space allows, a new position can be inserted into the marginal replacement column, substituting the overgrown positions.
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The developmental relationship between teeth and dermal odontodes in the most primitive bony fish Lophosteus
eLife 9:e60985.
https://doi.org/10.7554/eLife.60985
