Getting out of a mammalian egg: the egg tooth and caruncle of the echidna
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Evaluation Summary:
This paper addresses the development, fate and homology of the egg tooth and caruncle of the short-beaked echidna (Tachyglossus aculeatus) and will be of broad interest to workers in the fields of vertebrate evolutionary/developmental biology, comparative anatomy and palaeontology. This manuscript features high quality histological and tomographic data from an unprecedented developmental series of pre- and post-hatching echidna stages. The study is well-organised and clearly reported, though additional image data would strengthen the authors' conclusions.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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Evaluation Summary:
This paper addresses the development, fate and homology of the egg tooth and caruncle of the short-beaked echidna (Tachyglossus aculeatus) and will be of broad interest to workers in the fields of vertebrate evolutionary/developmental biology, comparative anatomy and palaeontology. This manuscript features high quality histological and tomographic data from an unprecedented developmental series of pre- and post-hatching echidna stages. The study is well-organised and clearly reported, though additional image data would strengthen the authors' conclusions.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
This paper reports features of the development (and subsequent loss) of the egg tooth of the short-beaked echidna (T. aculeatus) at the histological level. Based on these features, the authors then consider the homology of the egg tooth/caruncle of the echidna with those of avian and non-avian reptiles. The authors report that while the echidna egg tooth is first apparent as a Shh-expression epithelial placode, the tooth then takes shape by evagination, rather than invagination, of that placode. This is reminiscent of the first teeth of some reptiles. The authors also find that the echidna egg tooth is anchored directly to the bone of the premaxilla (again, reminiscent of the mechanism of attachment of some reptilian teeth, and unlike the thecodonty seen in mammalian teeth). The caruncle also forms near the …
Reviewer #1 (Public Review):
This paper reports features of the development (and subsequent loss) of the egg tooth of the short-beaked echidna (T. aculeatus) at the histological level. Based on these features, the authors then consider the homology of the egg tooth/caruncle of the echidna with those of avian and non-avian reptiles. The authors report that while the echidna egg tooth is first apparent as a Shh-expression epithelial placode, the tooth then takes shape by evagination, rather than invagination, of that placode. This is reminiscent of the first teeth of some reptiles. The authors also find that the echidna egg tooth is anchored directly to the bone of the premaxilla (again, reminiscent of the mechanism of attachment of some reptilian teeth, and unlike the thecodonty seen in mammalian teeth). The caruncle also forms near the premaxillary bone and is associated with a prematurely differentiated and cornified epithelium. Finally, the authors find that the egg tooth is lost via a combination of resorption (by multinucleated TRAP-positive clast cells) and by cell death within the egg tooth pulp, and that the caruncle is lost at some undetermined point between 11- and 50-days post-hatching. Taken together, these findings indicate that the only tooth (albeit a transient one) in the otherwise edentulate echidna more closely resembles the teeth of reptiles than those of eutherian mammals, indicative of remarkable conservation of dental features in monotremes and reptiles from the last common ancestor of amniotes.
Strengths
We commend the authors on acquiring a unique and impressive series of embryonic and post-embryonic echidna specimens, and on making the most of these precious specimens by sequentially imaging them for microCT, followed by processing for paraffin histochemistry and/or immunofluorescence. The quality of the histology and image data presented here is high, and the authors effectively use their various data types (CT and section) in combination to provide good and clear anatomical context for their observations. This histochemical stainings presented here are very clear, and easily allows the reader to distinguish tissue types and connectively between elements (e.g., between the dentine of the egg tooth and the premaxilla, and between the os caruncle and the premaxilla).
Furthermore, by framing their work in a comparative context, the authors can propose homologies between the egg tooth of the echidna and the first forming teeth of some lizards and crocodilians. Monotremes possess a fascinating melange of anatomical features classically regarded as "mammalian" or "reptilian", but these are extremely difficult to study developmentally. This work is a significant contribution in this regard and highlights the importance of monotreme developmental data when reconstructing the nature of the last common ancestor of amniotes.
Weaknesses
The introduction of the paper is a bit too long (and, at times, unfocused). Given the succinct nature of the results, the paper would benefit from a more focused and streamlined introduction.
While the embryonic samples studied here are understandably limited (and sample sizes necessarily small), there are nevertheless claims made here that are not fully supported by the figures. In most instances, this is a case of a lack of high-magnification panels in the plates illustrating, for example, the features of the odontoblast layer, the ameloblast-like cells at the tip of the tooth, etc. These features are discussed, but not shown.
The story around the caruncle isn't fully developed. It is introduced as though there has been some debate about whether the element forms as a distinct condensation from the premaxilla, but then this is not revisited. Also, the rationale for the choice of molecular markers used to characterise the epithelial component of the caruncle isn't entirely clear. The authors state that Loricrin is a marker of "terminal differentiation" - but does this mean that the loricrin-expressing epithelium adjacent to the caruncle skeleton is just farther along in its development relative to adjacent epidermis? Or is loricrin a specific marker of "cornified epithelia"? And if the latter, has loricrin expression been examined in the developing caruncles of avian or non-avian reptiles?
Finally, the evolutionary synthesis presented here seems reasonable with respect to the egg tooth but remains a bit less clear with respect to the caruncle. The authors conclude that the os caruncle may be a novelty of monotremes, but that the epithelial caruncle may be homologous between monotremes and reptiles - but then suggest that the last common ancestor of amniotes had both structures? It is difficult to follow this logic. I think that that paper would benefit from a more nuanced "final model" or hypothesis of homology of egg teeth and caruncles across amniotes.
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Reviewer #2 (Public Review):
The authors made a genuine effort to describe the cellular process implicated in the life cycle of the echidna egg tooth. The authors were able to collect new echidna specimens of high quality and thus could use modern staining and 3D imaging techniques. Typically only museum specimens are available. The rarity of the echidna embryonic, fetal and post natal material is of interest to evolutionary developmental biologists and those interested in tooth development. However, the data as presented is incomplete and does not capture the full developmental sequence and postnatal loss of the egg tooth.
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Reviewer #3 (Public Review):
The manuscript by Fenelon et al., documents the development and loss of dental egg tooth and cornified egg tooth of the short-beaked Echidna (Tachyglossus aculeatus). The authors use a variety of techniques (histology, microCT, immunofluorescence) and evidence to showcase the understudied set of morphologies common to egg-laying animals, but unique to monotreme mammals. I understand that this is a rare set of embryonic stages and the authors may have had very limited access to material, but there is little in the way of data concerned with tooth markers (only SHH). Overall, this is a brief, yet interesting morphological report on a fascinating mammal. This is a well written description of the mainly histological development of the osseous/cornified caruncle and the dental egg tooth. This work serves to …
Reviewer #3 (Public Review):
The manuscript by Fenelon et al., documents the development and loss of dental egg tooth and cornified egg tooth of the short-beaked Echidna (Tachyglossus aculeatus). The authors use a variety of techniques (histology, microCT, immunofluorescence) and evidence to showcase the understudied set of morphologies common to egg-laying animals, but unique to monotreme mammals. I understand that this is a rare set of embryonic stages and the authors may have had very limited access to material, but there is little in the way of data concerned with tooth markers (only SHH). Overall, this is a brief, yet interesting morphological report on a fascinating mammal. This is a well written description of the mainly histological development of the osseous/cornified caruncle and the dental egg tooth. This work serves to advance our knowledge of the development of an enigmatic group of mammals.
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