Development of the egg tooth – The tool facilitating hatching of squamates: Lessons from the grass snake Natrix natrix

Hermyt, Mateusz; Kaczmarek, Paweł; Kowalska, Magdalena; Rupik, Weronika

doi:10.1016/j.jcz.2016.11.001

Cited by 24 publications

(31 citation statements)

References 52 publications

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“…Given the underlying fibrous network of the mosasaurid (Figs ) and snake (Savitsky, ; Hermyt et al. ; Figs and ) periodontal tissues, squamate tooth attachment tissue development should be re‐examined under the evolutionary and developmental paradigms we propose here.…”

Section: Discussionmentioning

confidence: 99%

Mosasaurs and snakes have a periodontal ligament: timing and extent of calcification, not tissue complexity, determines tooth attachment mode in reptiles

LeBlanc

Lamoureux

2017

Journal of Anatomy

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Squamates present a unique challenge to our understanding of dental evolution in amniotes because they are the only extant tooth-bearing group for which a ligamentous tooth attachment is considered to be absent. This has led to the assumption that mammals and crocodilians have convergently evolved a ligamentous tooth attachment, composed of root cementum, periodontal ligament, and alveolar bone, whereas squamates are thought to possess a single bone of attachment tissue that fuses teeth to the jaws. The identity and homology of tooth attachment tissues between squamates, crocodilians, and mammals have thus been a focal point of debate for decades. We provide a novel interpretation of the mineralized attachment tissues in two focal taxa in this debate, mosasaurids and snakes, and compare dental tissue histology with that of the extant crocodilian Caiman sclerops. We identify a periodontal ligament in these squamates that usually exists temporarily as a soft connective tissue anchoring each tooth to the alveolar bone. We also identify two instances where complete calcification of the periodontal ligament does not occur: in a durophagous mosasaur, and in the hinged teeth of fossil and modern snakes. We propose that the periodontal ligament rapidly calcifies in the majority of mosasaurids and snakes, ankylosing the tooth to the jaw. This gives the appearance of a single, bone-like tissue fusing the tooth to the jaw in ankylosed teeth, but is simply the end stage of dental tissue ontogeny in most snakes and mosasaurids.

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Section: Discussionmentioning

confidence: 99%

Mosasaurs and snakes have a periodontal ligament: timing and extent of calcification, not tissue complexity, determines tooth attachment mode in reptiles

LeBlanc

Lamoureux

2017

Journal of Anatomy

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“…Transverse section series were cut at 7 μm using a Leica rotary microtome (Leica RM2125RT). Paraffin sections were stained using the AZAN method, after Heidenhain [60], and with Ehrlich’s haematoxylin and eosin [61, 62]. All histological sections (7-μm thick) were sequentially photographed, using a light microscope OLYMPUS BX60 with an OLYMPUS DP12 digital camera, and archived as TIFF files, using CellSens Standard software.…”

Section: Methodsmentioning

confidence: 99%

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

2017

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BackgroundSnakes are considered to be vomerolfaction specialists. They are members of one of the most diverse groups of vertebrates, Squamata. The vomeronasal organ and the associated structures (such as the lacrimal duct, choanal groove, lamina transversalis anterior and cupola Jacobsoni) of adult lizards and snakes have received much anatomical, histological, physiological and behavioural attention. However, only limited embryological investigation into these structures, constrained to some anatomical or cellular studies and brief surveys, has been carried out thus far. The purpose of this study was, first, to examine the embryonic development of the vomeronasal organ and the associated structures in the grass snake (Natrix natrix), using three-dimensional reconstructions based on histological studies, and, second, to compare the obtained results with those presented in known publications on other snakes and lizards.ResultsFive major developmental processes were taken into consideration in this study: separation of the vomeronasal organ from the nasal cavity and its specialization, development of the mushroom body, formation of the lacrimal duct, development of the cupola Jacobsoni and its relation to the vomeronasal nerve, and specialization of the sensory epithelium. Our visualizations showed the VNO in relation to the nasal cavity, choanal groove, lacrimal duct and cupola Jacobsoni at different embryonic stages. We confirmed that the choanal groove disappears gradually, which indicates that this structure is absent in adult grass snakes. On our histological sections, we observed a gradual growth in the height of the columns of the vomeronasal sensory epithelium and widening of the spaces between them.ConclusionsThe main ophidian taxa (Scolecophidia, Henophidia and Caenophidia), just like other squamate clades, seem to be evolutionarily conservative at some levels with respect to the VNO and associated structures morphology. Thus, it was possible to homologize certain embryonic levels of the anatomical and histological complexity, observed in the grass snake, with adult conditions of certain groups of Squamata. This may reflect evolutionary shift in Squamata from visually oriented predators to vomerolfaction specialists. Our descriptions offer material useful for future comparative studies of Squamata, both at their anatomical and histological levels.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0188-y) contains supplementary material, which is available to authorized users.

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“…6,10,13 This suggests that this process is not a universal feature of snakes and that large egg teeth can be created using different mechanisms. This therefore suggests that fusion of tooth germs is a conserved mechanism used by a wide variety of snakes to create a single large tooth.…”

Section: Discussionmentioning

confidence: 99%

“…1,4,5,8 In some lizards, two developing egg teeth have been reported, with one tooth degenerating to leave one remaining tooth germ, which goes on to form the final egg tooth. 6,10 We wished to further study formation of the egg tooth in snakes. 1 In the skink, Lygosoma, however, the single egg tooth appears to develop from a single medially developing tooth germ.…”

Section: Introductionmentioning

confidence: 99%

Getting out of an egg: Merging of tooth germs to create an egg tooth in the snake

Fons

Gaete

Zahradnicek

et al. 2019

Developmental Dynamics

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Background:The egg tooth is a vital structure allowing hatchlings to escape from the egg. In squamates (snakes and lizards), the egg tooth is a real tooth that develops within the oral cavity at the top of the upper jaw. Most squamates have a single large midline egg tooth at hatching, but a few families, such as Gekkonidae, have two egg teeth. In snakes the egg tooth is significantly larger than the rest of the dentition and is one of the first teeth to develop. Results: We follow the development of the egg tooth in four snake species and show that the single egg tooth is formed by two tooth germs. These two tooth germs are united at the midline and grow together to produce a single tooth. In culture, this merging can be perturbed to give rise to separate smaller teeth, confirming the potential of the developing egg tooth to form two teeth. Conclusions: Our data agrees with previous hypotheses that during evolution one potential mechanism to generate a large tooth is through congrescence of multiple tooth germs and suggests that the ancestors of snakes could have had two egg teeth. K E Y W O R D Scongrescence theory, dentition, egg tooth, fusion, snake Juan M. Fons and Marcia Gaete contributed equally.

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Development of the egg tooth – The tool facilitating hatching of squamates: Lessons from the grass snake Natrix natrix

Cited by 24 publications

References 52 publications

Mosasaurs and snakes have a periodontal ligament: timing and extent of calcification, not tissue complexity, determines tooth attachment mode in reptiles

Mosasaurs and snakes have a periodontal ligament: timing and extent of calcification, not tissue complexity, determines tooth attachment mode in reptiles

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Getting out of an egg: Merging of tooth germs to create an egg tooth in the snake

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