Coordinated labio-lingual asymmetries in dental and bone development create a symmetrical acrodont dentition

Abstract

Organs throughout the body develop both asymmetrically and symmetrically. Here, we assess how symmetrical teeth in reptiles can be created from asymmetrical tooth germs. Teeth of lepidosaurian reptiles are mostly anchored to the jaw bones by pleurodont ankylosis, where the tooth is held in place on the labial side only. Pleurodont teeth are characterized by significantly asymmetrical development of the labial and lingual sides of the cervical loop, which later leads to uneven deposition of hard tissue. On the other hand, acrodont teeth found in lizards of the Acrodonta clade (i.e. agamas, chameleons) are symmetrically ankylosed to the jaw bone. Here, we have focused on the formation of the symmetrical acrodont dentition of the veiled chameleon (Chamaeleo calyptratus). Intriguingly, our results revealed distinct asymmetries in morphology of the labial and lingual sides of the cervical loop during early developmental stages, both at the gross and ultrastructural level, with specific patterns of cell proliferation and stem cell marker expression. Asymmetrical expression of ST14 was also observed, with a positive domain on the lingual side of the cervical loop overlapping with the SOX2 domain. In contrast, micro-CT analysis of hard tissues revealed that deposition of dentin and enamel was largely symmetrical at the mineralization stage, highlighting the difference between cervical loop morphology during early development and differentiation of odontoblasts throughout later odontogenesis. In conclusion, the early asymmetrical development of the enamel organ seems to be a plesiomorphic character for all squamate reptiles, while symmetrical and precisely orchestrated deposition of hard tissue during tooth formation in acrodont dentitions probably represents a novelty in the Acrodonta clade.

X-ray microtomography imaging of craniofacial hard tissues in selected reptile species with different types of dentition

“…For this study, we enlarged the list of scanned model species, which have been used for the purpose of our previously published studies focused on tooth development [ 7 , 8 , 13 , 14 ], by species possessing further unique features among reptiles. As a source of information for the selection of key reptilian specimens, we used a detailed review discussing the different aspects of the tooth to bone relationship across amniotes [ 2 ].…”

“…There is visible heterogeneity in tooth shape along the jaw, ranging from smaller teeth in the very rostral part of the jaw to tricuspid teeth in the caudal area, where teeth are also noticeably larger. A number of publications have described chameleon dentition in detail, with micro-CT used as one of the key methods [ 7 , 8 , 14 ]. In these studies, mostly the embryos were used to describe the process of odontogenesis.…”

“…In these studies, mostly the embryos were used to describe the process of odontogenesis. Therefore, so far, we know that chameleon teeth germs develop asymmetrically, closely recalling pleurodont implantation [ 8 ]. Also, the patterning of the tooth germ initiation is precisely coordinated, with the first calcified tooth appearing caudally followed by next teeth placed rostrally [ 15 ].…”

“…The acquired data could be helpful in the study of different types of tooth-bone attachment and implantations, which is, according to recent publications, a broadly studied topic [ 8 , 10 , 11 , 21–24 ] that varies across species. Another interesting feature concerning teeth is the analysis of tooth spacing, which we addressed using a specific tool in VG studio Max that allows the jaw to be "unrolled" to display all the teeth at once.…”

“…In chameleons, which are strictly monophydont with only 1 tooth generation, teeth are firmly attached to the jawbone, and if the tooth is lost owing to injury or during a fight, the jawbone is extensively damaged [ 7 ]. Also, the whole process of odontogenesis across individual developmental stages is peculiar, especially because of asymmetrically developing tooth germ giving rise to symmetrically ankylosed teeth [ 8 ]. However, most reptiles (e.g., geckos, Anolis , skinks, Ameiva , iguanas, and snakes) possess an unlimited and lifelong supply of new tooth generations.…”