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. 2022 Dec;241(6):1424-1440.
doi: 10.1111/joa.13756. Epub 2022 Sep 5.

Diphyodont tooth replacement of Brasilodon-A Late Triassic eucynodont that challenges the time of origin of mammals

Sergio F Cabreira  1 , Cesar L Schultz  2 , Lúcio R da Silva  1 , Luiz Henrique Puricelli Lora  3 , Cristiane Pakulski  4 , Rodrigo C B do Rêgo  5 , Marina B Soares  2   6 , Moya Meredith Smith  7   8 , Martha Richter  7
Affiliations

Diphyodont tooth replacement of Brasilodon-A Late Triassic eucynodont that challenges the time of origin of mammals

Sergio F Cabreira et al. J Anat. 2022 Dec.

Abstract

Two sets of teeth (diphyodonty) characterise extant mammals but not reptiles, as they generate many replacement sets (polyphyodonty). The transition in long-extinct species from many sets to only two has to date only been reported in Jurassic eucynodonts. Specimens of the Late Triassic brasilodontid eucynodont Brasilodon have provided anatomical and histological data from three lower jaws of different growth stages. These reveal ordered and timed replacement of deciduous by adult teeth. Therefore, this diphyodont dentition, as contemporary of the oldest known dinosaurs, shows that Brasilodon falls within a range of wide variations of typically mammalian, diphyodont dental patterns. Importantly, these three lower jaws represent distinct ontogenetic stages that reveal classic features for timed control of replacement, by the generation of only one replacement set of teeth. This data shows that the primary premolars reveal a temporal replacement pattern, importantly from directly below each tooth, by controlled regulation of tooth resorption and regeneration. The complexity of the adult prismatic enamel structure with a conspicuous intra-structural Schmelzmuster array suggests that, as in the case of extant mammals, this extinct species would have probably sustained higher metabolic rates than reptiles. Furthermore, in modern mammals, diphyodonty and prismatic enamel are inextricably linked, anatomically and physiologically, to a set of other traits including placentation, endothermy, fur, lactation and even parental care. Our analysis of the osteodental anatomy of Brasilodon pushes back the origin of diphyodonty and consequently, its related biological traits to the Norian (225.42 ± 0.37 myr), and around 25 myr after the End-Permian mass extinction event.

Keywords: Brasilodon; Late Triassic; diphyodonty; eucynodont; osteodental histology.

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Figures

FIGURE 1
FIGURE 1
Geographic and stratigraphic positioning of Brasilodon quadrangularis. (a) Map with the location of Brasilodon records; (b) Chrono‐Biostratigraphic framework with the Allostratigraphic Sequences and Assemblage Zones (AZ) of the Brazilian Triassic, showing some of the probainognathian cynodonts that occur in each of these. Modified from Zerfass et al. (2003), Soares et al. (2011), Horn et al. (2014), Martinelli et al. (2016). Ages follow Cohen et al. (; Updated). Ind., Induan; Ole., Olenekian; Ani., Anisian; Lad., Ladinian; Car., Carnian; Nor., Norian; Rha., Rhaetian.
FIGURE 2
FIGURE 2
Brasilodon quadrangularis (a) skull of UFRGS‐PV‐0628‐T in left lateral view. (b) Post‐canine tooth row of the right dentary of ULBRA‐PV‐0284‐T in lingual view. atb, attachment bone; dp5, deciduous premolar5; m1, m2, molars 1 and 2; p2‐p4, premolars 2‐4; pcdia, post‐canine distema; pdt, post‐dentary through; prr, physiologic dental rhizolysis.
FIGURE 3
FIGURE 3
Diagenetic structures on a polished thin section of Brasilodon quadrangularis specimen ULBRA‐PVT‐0284‐T, a right dentary and teeth. All images are medial views. (a) in polarised light; (b) polarized under crossed nicols. (c) Normal transmitted light and (d) Same as (c), but under reflective light. (a) The medular cavities of the dentary bone and tooth roots are filled with diagenetic calcite (cac) that probable prolong throught the hard dental and osteal tissues. (b) The red dotted line (spfp) represents the subparallel crystallographic boundaries between apatite crystallites near the tooth roots and alveolar bone. (c) Post‐mortem fractures (pmf) on post‐canine crowns are indicated by white arrows. (d) A horizontal fracture affected the enamel and the dentine of the ‘a’ and ‘c’ cusps of m1 and m2, respectively. Diagenetic material fills up the pulpar cavity. a, principal cusp of m1; alb, alveolar bone; c, cuspid of m2; de, dentine; dim, diagenetic material; drt, dental root; e, enamel; llb, lamellar bone; m, permanent molar; mc, marrow cavity; pc, pulpar cavity, tth, tooth.
FIGURE 4
FIGURE 4
Photographs of dentary and teeth representing three development stages of Brasilodon (polarised light). (a) UFRGS‐PV‐0767‐T, neonate right dentary, showing large biradicular decidual molarifom‐like teeth arranged shoulder‐to‐shoulder. The dp5 is the largest dental unit. The m1 present thin dentine walls and a large pulp cavity. The yellow arrows indicate the birradicular divergent roots (b) Higher magnification of the post‐canine region shown in (a) showing the chondroid bone concentration penetrated by irregular calibre blood vessels. The large mass of intermediate transitional chondroid bone is surrounded by rows of small, pre‐hypertrophic chondroid‐like cells (phyc). Circumscribed within the yellow line there is a group of hypertrophic, chondroid‐like bone cell spaces separated by substantial intercellular spaces. This strongly suggests that at least in part, mandibular growth in Brasilodon would occur in association with the development of the post‐canine accessory cartilage. The dentinal exfoliative resorption radicular front (drrf) is observed on the mesial surface the dp1, which indicates that it was going through a physiological process of resorption, similarly to what happen to vestigial, post‐canine teeth in mammals. (c) Subadult specimen ULBRA‐PVT0284 in reflected light microphotograph. Note the pneumatisation internal to the diastema. The vdp1 was at nearly completely resorbed stage. (d) Juvenile left dentary UFRGS‐PV‐0825‐T with deciduous molariform‐like teeth grouped ‘shoulder‐to‐shoulder’. Observe the vdp1, still at a stage when it is not completely resorbed. (e) Higher magnification of (d). Note the thin and opaque, poorly developed enamel (pdone) and the thick layer of primary orthodentine (prde). atb, attachment bone; chipb, chondroid intermediary permanent bone; chitb, chondroid intermediary transitional bone; dim, diagenetic material; dp2 to dp5, deciduous premolars ; dw, dentinary wall; eabm2, empty alveolus for the unmineralised tooth germ of m2; edj, enamel‐ dentine junction; iavc, irregular anastomosed vascular canals; llb, lamelar bone; m1, permanent molar1; mdc, medular diastemal cavity; oes, outer enamel surface; p2 to p4, premolars 2 to 4; pcdia, post canine diastem; rddr, residual dentinary root; rrdp1, residual root of the vdp1; sde, secondary dentine; stsg, shoulder to shoulder teeth arrangement; vdp1, vestigial dp1.
FIGURE 5
FIGURE 5
Photomicrographs of specimen ULBRA‐PVT0284 (all but A under transmitted light microscopy). (a) Polished mandible showing developing teeth. The black dash lines indicate the lbsp5 tooth germ; the green one, the contour (outline) of the dental crypt. Yellow arrow indicates the sequential, rostro‐caudal replacement of the premolars. Red arrows indicate the caudal addition of molars. The horizontal dash line indicates the level of the low successional (yellow) and primary heights (red) of the dental lamina. The heterotopically high position of m1 reflects the post‐displaced heterochronous pattern of development of permanent molars (see Luckett, 1993). These programmed delays would allow the growth of dental bone at the base of the molars and the consequent development of Spee's Curvature in adult mammals (the partial formation of which is shown by the blue dashed line). (b) The translucent permanent enamel of p3 and p4 and the thin enamel of dp5, m1 and m2. The caudal concavity to the latter suggests the empty alveolus of bm3. The yellow dash line indicates the late bel stage tooth germ of the successional p5 (lbsp5). (c) Higher magnification of (a). Compare translucent enamel of successional p4 with the thin, underdeveloped, and opaque enamel of dp5. (d) The small progenic p4 and the deciduous molariform dp5 are separated by a conspicuous interdental battlement (idb), which indicates that both teeth derive from different successional and the primary segments of the dental lamina, respectively. dim, diagenetic material; dp5, deciduous premolar 5; dw, dentary wall; eabm3, empty alveolus for unmineralised m3 tooth germ; llb, lamellar bone; m, permanent molar; mdc, medular diastemal cavity; odcp5, osteodental crypt for lbsp5; p2 to p4, premolars 2 to 4; pdone, primary, opaque, poorly developed enamel; ppoe, primary, permanent opaque enamel; tspe, translucent permanent enamel.
FIGURE 6
FIGURE 6
Photomicrographs of polished thin‐section of the left dentary ULBRA‐PVT0284 (a, b under polarised light, and c, d under reflected light microscopy). (a) Note the differences between the enamel of the primary lbsp5 and m1. The thin, opaque and poorly developed enamel of dp5 indicates an early onset and an early offset stage. The highest positioned m1, shows a semi‐translucent enamel that indicates a late offset in relation to dp5. Advanced stage of substitution (replacement) of dp5 by its respective (still immature) successional p5. (b) Immature lbsp5 has a thick, undeveloped immature not yet translucent radial enamel. The apex, in the phase of secretion and enamel maturation, shows two lines (ilemf) that indicate the active mineralization front. This shows that the lbsp5 bud would not have reached the end of the bell stage at the time of the specimen's death. (d) and (e). Deciduous tooth dp5 at the stage of being physiologically replaced (region encircled in red line). The yellow arrows indicate the coronal region and the distal part of the radicular dentinal walls, which remained after the process of physiological rhizolysis of the dp5 tooth. abdl, connecting lines indicating the fusion between the distal radicular dentine and alveolar bone; alb, alveolar bone; cvvc, cribriform vascular canals of Volkmann; dcc, dentinoclast cavities; de, dentine; dim, diagenetic material; dp5, deciduous premolar5; e, enamel; edj, enamel dentine junction; lbsp5, late bell stage tooth germ of successional p5; m, permanent molar; p5, premolar5; pc, pulp cavity; pdone, primary, opaque, poorly developed enamel; pe, prismatic enamel; ppoe, primary permanent opaque enamel; rdw, radicular dentinary wall.
FIGURE 7
FIGURE 7
Photomicrographs of polished thin‐section of the left dentary ULBRA‐PVT0284 under polarised light. (a) The first molar, m1, shows a more developed irregular prismatic enamel (iapl) in the most cervical part of the mesial side of the cusp ‘a’, within the area marked with a yellow rectangle. (b) Higher magnification of (a). The delayed offset of the m1 is indicated by its complex enamel, showing Schmelzmuster multi‐layered enamel, including radial (rel), irregular angled prismatic enamel (iapl) and an aprismatic external layer (plex). (c) Higher magnification of (b). Note that groups of six enamel prisms appear vertically arranged from the edj, and simultaneously bend at positive angles toward the coronal apex. Further to the right of this area, the enamel prisms run parallel to the outer surface of the enamel (oes) and their individual limits become almost indistinguishable. a, principal cusp; b, accessory cusp b; de, dentine; dmt, dentinary mantle; edj, enamel dentine junction; iapl, irregular angled prismatic enamel;; m1, permanent molar1; oes, outer enamel surface; plex, aprismatic external layer; rel, radial enamel layer.
FIGURE 8
FIGURE 8
Hypothetical schematic interpretation of the eutherian dental replacement pattern (DRP) of Brasilodon. (a) Hypothetical embryonic stage. The caudo‐rostral induction of the primary lamina starts with the appearance of the dp5 tooth germ, and the tooth germ of m1, induced at a later ontogenetic stage delayed through a heterochronic process typical of eutherians. (b) Note that the primary lamina produces large deciduous molarifoms, arranged shoulder‐to‐shoulder, a vestigial vdp1 and the delayed development of m1. (C–E) Juvenile stages; (C) observe the induction of p2 and consequent resorption of dp2, as well as the late eruption and elevated position of m1. (d) Total eruption of p2 and root resorption starts for dp3. The m2 erupts beyond its bony crypt, not yet into the adult occlusal plane. (e) The tooth germs of m3 (delayed development in the primary dental lamina), p4, and p5 are initiated (as from secondary dental laminae), while eruption of p3 and development of p4, triggers the resorption of dp4. (f) Adult stage. p4 and p5 have already erupted and the m3 tooth germ is added caudally. c, canine; dp, deciduous premolar; i, deciduous incisive; m, permanent premolar; rrvdp1, residual root of the deciduous premolar1; vdp1, vestigial premolar1.
FIGURE 9
FIGURE 9
Reconstruction of Brasilodon quadrangularis with litter in their environment during the Late Triassic in southern Brazil (art by Humphrey Bangham), where all the known specimens have been found. Note the suggested parental care and size difference as mammalian features, as well as inferred fur, and a below ground burrow (see text for dento‐anatomical support for these inferences). The palaeoenvironmental interpretations of the late Triassic Candelaria Sequence (within the Santa Maria Supersequence) follow Zerfass et al. (2003) and Soares et al. (2014).
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