Rampant tooth loss across 200 million years of frog evolution
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Curated by eLife
Evaluation Summary:
This manuscript will find a broad audience in the fields of evolutionary and developmental biology, especially herpetology, systematics, and those interested in the evolutionary history of vertebrate teeth. The expansive dataset presented by the authors has allowed for rigorous computational analyses yielding new insight into the evolutionary history of teeth in frogs, which is a topic that has received little attention from the scientific community. The resulting data largely support the key claims of the manuscript.
(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. The reviewers remained anonymous to the authors.)
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Abstract
Teeth are present in most clades of vertebrates but have been lost completely several times in actinopterygian fishes and amniotes. Using phenotypic data collected from over 500 genera via micro-computed tomography, we provide the first rigorous assessment of the evolutionary history of dentition across all major lineages of amphibians. We demonstrate that dentition is invariably present in caecilians and salamanders, but teeth have been lost completely more than 20 times in frogs, a much higher occurrence of edentulism than in any other vertebrate group. The repeated loss of teeth in anurans is associated with a specialized diet of small invertebrate prey as well as shortening of the lower jaw, but it is not correlated with a reduction in body size. Frogs provide an unparalleled opportunity for investigating the molecular and developmental mechanisms of convergent tooth loss on a large phylogenetic scale.
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Reviewer #2 (Public Review):
Paluh and colleagues have investigated the presence and absence of teeth in 523 species of amphibians spanning 515 genera. They have specifically utilized microCT scanning to identify the dentulous bones as well as those that may be missing teeth in all three modern orders of amphibians, with a particular focus on Anura (frogs and toads). It is known that many anurans are entirely edentulous, while frogs only have teeth in the bones of the upper jaw (with the exception of one species). Through Bayesian analysis, reconstruction of ancestral states, they've found that teeth have been completely lost at least 22 times in frogs. Remarkably, they also uncovered six reversals, back to a toothed state, although only in the upper jaw. They then attempt to find a correlation between tooth loss and the diet, jaw …
Reviewer #2 (Public Review):
Paluh and colleagues have investigated the presence and absence of teeth in 523 species of amphibians spanning 515 genera. They have specifically utilized microCT scanning to identify the dentulous bones as well as those that may be missing teeth in all three modern orders of amphibians, with a particular focus on Anura (frogs and toads). It is known that many anurans are entirely edentulous, while frogs only have teeth in the bones of the upper jaw (with the exception of one species). Through Bayesian analysis, reconstruction of ancestral states, they've found that teeth have been completely lost at least 22 times in frogs. Remarkably, they also uncovered six reversals, back to a toothed state, although only in the upper jaw. They then attempt to find a correlation between tooth loss and the diet, jaw morphology, and body size of the edentulous species. Through Bayesian analysis of an impressive, detailed dataset of dietary fact notes from the available scientific literature, the authors find a strong correlation between edentulous species and microphagy (eating ants, termites, other small arthropods). A subsequent phylogenetic logistic regression analysis reveals a significant relationship between edentulism and shortened lower jaws, while failing to find a similar correlation between edentulism and body size.
The major strengths of this paper are the sheer number of species analyzed (including diet data as well as jaw and SVL measurements), combined with up to date analytical methods. Additional strengths of the paper are the robust statistical confirmation obtained from the aforementioned methods.
While there are not many weaknesses, the one major weakness is the correlative nature of the results (e.g. edentulation and smaller lower jaws). While the authors are careful not to directly attribute smaller jaw to tooth loss, it is insinuated from the statistical significance of the analyses, when in reality, these two morphological features could both be independent results of adaptation to microphagy. This possibility should brought to the forefront of the discussion by the authors.
That said, the authors did achieve their goal of identifying how many times teeth were lost in frogs and how many times regained. This is the main aim of the manuscript and is a fascinating glimpse into the phenomenon of edentulation in one of the most speciose group of vertebrates on the planet. This information will allow both the herpetological community as well as the tooth evolution community to reassess some key aspect of their respective fields.
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Reviewer #1 (Public Review):
This study examines the evolution of tooth loss (endentulism) across amphibians, finding many cases of endentulism and the majority of losses in frogs and toads (Anura). The study is the first to characterize amphibian endentualism at this scale and the authors have collected an impressive dataset. The study shows correlations among endentulism, diet, and jaw length and discusses potential proximal and ultimate explanations for endentulism in anurans. There are important data provided in this manuscript (e.g. region-specific tooth loss - dentary, maxilla, premaxilla, palate), which could further illuminate developmental pathways responsible for endentulism as well as evolutionary correlates of region-specific tooth loss. The authors collated an impressive breadth of diet data but clearer documentation and …
Reviewer #1 (Public Review):
This study examines the evolution of tooth loss (endentulism) across amphibians, finding many cases of endentulism and the majority of losses in frogs and toads (Anura). The study is the first to characterize amphibian endentualism at this scale and the authors have collected an impressive dataset. The study shows correlations among endentulism, diet, and jaw length and discusses potential proximal and ultimate explanations for endentulism in anurans. There are important data provided in this manuscript (e.g. region-specific tooth loss - dentary, maxilla, premaxilla, palate), which could further illuminate developmental pathways responsible for endentulism as well as evolutionary correlates of region-specific tooth loss. The authors collated an impressive breadth of diet data but clearer documentation and examination of that data would allow readers to better evaluate the support for the relationship between diet and endentulism. Overall, this study reveals an interesting evolutionary pattern of endentulism, with the number of independent evolutionary cases of endentulism in amphibians (and anurans, in particular) dwarfing those found in other tetrapod clades.
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Evaluation Summary:
This manuscript will find a broad audience in the fields of evolutionary and developmental biology, especially herpetology, systematics, and those interested in the evolutionary history of vertebrate teeth. The expansive dataset presented by the authors has allowed for rigorous computational analyses yielding new insight into the evolutionary history of teeth in frogs, which is a topic that has received little attention from the scientific community. The resulting data largely support the key claims of the manuscript.
(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. The reviewers remained anonymous to the authors.)
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