From teeth to pad: tooth loss and development of keratinous structures in sirenians

Abstract

Sirenians are a well-known example of morphological adaptation to a shallow-water grazing diet characterized by a modified feeding apparatus and orofacial morphology. Such adaptations were accompanied by an anterior tooth reduction associated with the development of keratinized pads, the evolution of which remains elusive. Among sirenians, the recently extinct Steller's sea cow represents a special case for being completely toothless. Here, we used μ-CT scans of sirenian crania to understand how motor-sensor systems associated with tooth innervation responded to innovations such as keratinized pads and continuous dental replacement. In addition, we surveyed nine genes associated with dental reduction for signatures of loss of function. Our results reveal how patterns of innervation changed with modifications of the dental formula, especially continuous replacement in manatees. Both our morphological and genomic data show that dental development was not completely lost in the edentulous Steller's sea cows. By tracing the phylogenetic history of tooth innervation, we illustrate the role of development in promoting the innervation of keratinized pads, similar to the secondary use of dental canals for innervating neomorphic keratinized structures in other tetrapod groups.

Keywords: Steller's sea cow; dental pseudogenes; keratinous pad; sirenians; tooth loss.

Figure 1.

Ontogenetic evidence of the association of dorsal canaliculi to tooth alveoli, vestigial or not, and dental pad. (a–d) 3D models of the mandibles of sirenian fetuses ((a) Trichechus manatus NHMUK 1865-4-28-9; (b) Dugong dugon IRSNB 5386, mirror image) and adults ((c) Trichechus manatus NHMUK 1950-1-23-1; (d) Dugong dugon NHMUK 2005-51) in lateral views. (a,b) Arrows indicate the location of vestigial tooth loci (but see also electronic supplementary material, figure S4). Bone is transparent. Orange = dorsal canaliculi; purple = mental branches; cyan = mandibular canal; dark blue = teeth; green = tooth alveoli. Scale bars: 1 cm.

Figure 2.

Comparison of the internal mandibular morphology in (a) Trichechus manatus (NHMUK 1885-6-30-2), (b) Dugong dugon (NHMUK 2023.66) and (C) Hydrodamalis gigas (UMZC C1021), showing the link between dorsal canaliculi, teeth and keratinous pad (same colour code as figure 1; keratinized pad is in yellow). Bone is transparent. Vertical line in (c) represents post-scanning combination of separate scans of anterior and posterior parts of the jaw. Orange = dorsal canaliculi; purple = mental branches; cyan = mandibular canal; dark blue = teeth; green = tooth alveoli; yellow = keratinous pad. Upper left corner of each panel: small mandible silhouettes representing dental replacement systems: green arrows indicate dental drift; red arrows indicate molar loss; yellow lines indicate the position of the keratinous pad. Electronic supplementary material provides detailed anatomical descriptions of the intraspecific variation of the internal anatomy in each of these species (figures S2 and S3). Scale bars: 1 cm.

Figure 3.

Evolution of dorsal canaliculi linked to tooth reduction in five paleogene and four neogene sirenian species (including two extant ones). Timetree (according to [22]) with corresponding 3D reconstructions of the internal mandibular morphology. Orange = dorsal canaliculi; purple = mental branches; cyan = mandibular canal; dark blue = teeth; green = tooth alveoli; yellow = keratinous pad. Scale bars: 1 cm. Paintings by Michelle S. Fabros.

Figure 4.

(a) Summary of dental gene functionality in three sirenian species and their most recent common ancestors. (b) DNA sequence alignments of five dental genes derived from four sirenian genome assemblies, highlighting putative inactivating mutations. Grey bars at the top of whole gene assemblies indicate coding exons. Paintings by Michelle S. Fabros.