Are there any teeth on the lower jaw of a frog

However, G. When going after big game, it may help to have lower teeth to secure squirming prey. But these fangs are pseudo-teeth—bony extensions of the mandible, lacking both dentin and enamel.

She believes that comparing the development of G. Paluh also hopes to do some developmental genetic work on the frog, but fresh embryos are not an option—a living G. While little is known about them, their numbers have dwindled as agriculture and logging devastate the cloud forests of Ecuador and Colombia.

Some fear the species is already extinct. However, the sudden rediscovery of a presumed extinct frog is not unprecedented.

In , for example, researchers found the horned marsupial frog Gastrotheca cornuta after failing to spot one for 13 years in the same Ecuadorian cloud forests where G. All rights reserved. But it has one even more puzzling trait: It possesses a full set of teeth. Share Tweet Email. Read This Next Wild parakeets have taken a liking to London. Animals Wild Cities Wild parakeets have taken a liking to London Love them or hate them, there's no denying their growing numbers have added an explosion of color to the city's streets.

India bets its energy future on solar—in ways both small and big. Phylogeny of frog species with a stochastic character map of dentition and the distribution of diet states with species tip labels.

Figure 5. Discussion Evolution of edentulism in jawed vertebrates With at least 22 independent origins of edentulism, frogs have completely lost teeth more times than any other vertebrate clade. Amphibian dentition and tooth loss in frogs Dentition is highly conserved in salamanders and caecilians with no identified cases of edentulism. Tooth loss in fossil amphibians To our knowledge, no stem tetrapods have been described as edentulous Ruta et al.

Molecular and developmental mechanisms of tooth loss Recent work has documented that several lineages of edentulous vertebrates have various states of molecular tooth decay in the genes that are critical for the formation of dentin and enamel with frameshift mutations and stop codons that result in nonfunctionalization mammals: Meredith et al.

Materials and methods Species sampling and scanning We collected data from high-resolution microCT scans of amphibian species, representing frog genera of total; AmphibiaWeb, , 65 salamander genera of 68 total , and 30 caecilian genera of 34 total.

Survey of amphibian dentition variation and ancestral state reconstructions We recorded the presence or absence of teeth on each dentigerous bone of the lower jaw, upper jaw, and palate for amphibian species Figure 1 ; Dataset S1.

Testing relationships among edentulism, diet, and body size We compiled dietary data for all sampled anuran species from the literature see Dataset S2 for references. Acknowledgements We thank all of the institutions, curators, and collection managers that loaned us specimens for this study. Funding Statement The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Additional information Competing interests No competing interests declared. Data curation, Investigation, Writing - review and editing. Additional files Transparent reporting form Click here to view. Data availability Computed tomography data tiff stacks and mesh files have been deposited in MorphoSource see Dataset 1. Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes. Reptile enamel matrix proteins: selection, divergence, and functional constraint.

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Although the location of teeth can vary from species to species, the same basic genetics likely underlies their development, and producing them on the lower jaw might be as simple as throwing a switch. Paluh plans on leveraging several genetic tools in the near future to map the contours of tooth development and evolution in frogs, but for G. DNA degrades over time in plants and animals stored in museum collections, and the scant number of aging G.

Journal Evolution. DOI Method of Research Experimental study. It remains unknown whether any anurans have lost enamel but retain teeth, which has occurred several times in mammals Meredith et al. No relationship was identified between complete edentulism and body size in the frog species sampled. The smallest known species of frog, P. We examined 25 taxa with an SVL of 15 mm or less: 13 were toothed and 12 were edentulous. Several of the smallest edentulous species in our dataset are microhylids, bufonids, and dendrobatids, and these clades have widespread tooth loss across a range of body sizes.

We identified only one case of edentulism in Brachycephaloidea, in the genus Brachycephalus , despite this neotropical radiation of over species containing many miniaturized lineages e. Within the genus Arthroleptis , several miniature species lack teeth Laurent, ; Blackburn, , suggesting that, in some cases, a reduction in body size and tooth loss may be linked. There are several large or gigantic species within the Bufonidae Womack and Bell, , but all true toads lack teeth regardless of size.

When excluding bufonids, reduction in body size was phylogenetically correlated with edentulism, indicating that further work is needed to investigate the interplay between edentulism, body size evolution, and paedomorphism across anurans. To our knowledge, no stem tetrapods have been described as edentulous Ruta et al.

Albanerpetontids, an extinct lineage of lissamphibians, had teeth on the premaxilla, maxilla, and dentary Daza et al. No teeth are visible in Triadobatrachus Ascarrunz et al. The dentary of Triadobatrachus lacks teeth, and the absence of dentition on the lower jaw is considered a synapomorphy of Salientia Milner, However, the clades Xenopodinomorpha and Pipinomorpha are not supported by molecular phylogenetic analyses of living pipids Irisarri et al.

All species of Xenopus and three of seven species of Pipa have teeth P. Teeth may have been lost several times in Pipa , but the relationships among species are poorly understood. The sister clade to Pipidae is Rhinophrynidae collectively forming the Pipoidea, Feng et al.

The fossil record of Rhinophrynidae is sparse Blackburn et al. The presence of teeth in Rhadinosteus supports the hypothesis that teeth were lost independently in pipids and rhinophrynids Figure 2 and indicates that edentulism may have evolved later in rhinophrynids.

Two edentulous, non-pipoid fossil frogs have been described from the Mesozoic of the Northern Hemisphere: Theatonius from the late Cretaceous of Wyoming Fox, and Tyrrellbatrachus from the late Cretaceous of Alberta Gardner, These two crown-group anurans have an uncertain placement in the frog tree of life but are likely distantly related to one another. Gardner, hypothesized that these two taxa likely represent two independent cases of tooth loss and possibly the oldest record of edentulism in nonpipid frogs.

The majority of living, edentulous frogs are neobatrachians Figure 2 ; in Hyloidea, Ranoidea, Myobatrachidae, and Nasikabatrachidae , but few fossil neobatrachians have been described as edentulous Gardner, Recent work has documented that several lineages of edentulous vertebrates have various states of molecular tooth decay in the genes that are critical for the formation of dentin and enamel with frameshift mutations and stop codons that result in nonfunctionalization mammals: Meredith et al.

The frameshift mutation rate of these loci can be used to estimate the timing of tooth loss in the fossil record Meredith et al. Whether edentulous frogs possess similar rates of molecular tooth decay in these loci, as demonstrated in amniotes, has yet to be tested. Recently, Lu et al. Based on selection intensity estimates and substitution rates, this gene likely became inactivated in the Bufonidae 40—60 million years ago Shaheen et al. We hypothesize that these tooth-specific genes have degenerated repeatedly across edentulous anurans by novel inactivating mutations, and the frameshift mutation rate will indicate that teeth were lost at several different geologic times during the evolution of frogs.

Anuran enamel matrix proteins may be operating under relaxed selection, compared to purifying selection in most mammals and reptiles Alazem and Abramyan, , due to the evolution of projectile tongue feeding, enabling the evolutionary lability of frog teeth. The developmental genetics of tooth formation in amphibians is almost entirely unexplored, especially when compared to our understanding of chondrichthyan, teleost, and amniote odontogenesis Fraser et al.

It is unknown if the genes critical for tooth formation in fishes and amniotes are also expressed during morphogenesis of teeth in amphibians, if all frog species retain a suppressed ancestral developmental pathway of tooth development on the lower jaw, or if the odontogenetic pathway has been disrupted via one or many mechanisms on the jaws of edentulous anurans. The loss of teeth on the lower jaw of frogs could be due to the loss of a single major signal that can orchestrate odontogenesis, comparable to the sole loss of odontogenic Bmp4 expression in living birds Chen et al.

If true, potential rudimentary structures, such as tooth buds or the early thickening of the odontogenic band, might be seen before the abortion of tooth development in the lower jaw of anurans.

Investigation of the developmental genetics of tooth formation in the upper and lower jaws of frogs will fill a large gap in our understanding of vertebrate evolution and development and may elucidate the mechanisms of repeated tooth loss and putative cases of the re-evolution of lost teeth in one of the most diverse vertebrate orders.

We collected data from high-resolution microCT scans of amphibian species, representing frog genera of total; AmphibiaWeb, , 65 salamander genera of 68 total , and 30 caecilian genera of 34 total. One recently described frog species was not microCT scanned but included in the dataset because it is the only member of its genus with teeth U.

All genera are represented by one species except for nine anuran genera Arthroleptis , Cacosternum , Engystomops , Gastrotheca , Physalaemus , Pipa , Telmatobius , Uperodon , Uperoleia with two sampled lineages that represent known dental variation within these genera Dataset S1. All scans were run using a kv X-ray tube containing a diamond-tungsten target, with the voltage, current, and detector capture time adjusted for each scan to maximize absorption range for each specimen.

We conducted ancestral state reconstructions of dentition two states: toothed, edentulous in extant amphibians using the data collected from species representing genera and all 77 families using the phylogeny of Jetz and Pyron, The models were assigned an equal prior probability using a uniform set-partitioning prior, and the root state frequencies were estimated using a flat Dirichlet prior.

The rates of gain and loss of dentition were drawn from an exponential distribution with a mean of 10 expected character state transitions over the tree. The MCMC was run for 22, iterations, the first iterations were discarded as burn-in, and samples were logged every 10 iterations. We conducted additional Bayesian ancestral state reconstructions using RevBayes to model the evolutionary history of dentition presence or absence on individual dentigerous elements Figure 2—figure supplements 3 — 6.

To test if vomerine tooth loss always precedes complete edentulism in frogs, we compared discrete character evolution models using fitMk in phytools for three dental states fully toothed, toothed upper jaw with vomerine tooth loss, edentulous in species of frogs.

The only two species that putatively possess vomerine teeth while lacking upper jaw teeth R. Six models were compared equal-rates, single-rate ordered, symmetric ordered, unsymmetric ordered, symmetric unordered, all-rates-different using the AIC and AICw Figure 3—figure supplement 1. The ordered models enforced vomerine tooth loss as an intermediate state between fully toothed and edentulous states.

To estimate the posterior probabilities for all nodes and the number of transitions between these three character states, we used stochastic character mapping MCMC sampling of character histories from their posterior probability distribution; Huelsenbeck et al. We compiled dietary data for all sampled anuran species from the literature see Dataset S2 for references. Species were classified as generalists if the majority of their diet by number or volume consists of other invertebrate groups or vertebrates.

Only 10 of anuran genera are known to contain both edentulous and toothed species Arthroleptis , Cacosternum , Engystomops , Glyphoglossus , Mini , Physalaemus , Pipa , Telmatobius , Uperodon , Uperoleia. Due to the disparity in existing ecological data available across all anurans, the dietary records ranged from singular reports one prey item in one individual to detailed studies investigating the stomach contents of hundreds of individuals. We measured SVL tip of the snout to the rear of the ischium , skull length occiput to tip of the snout , and mandible length posterior to anterior tip of the lower jaw for all sampled specimens using the linear measurement tools in VG StudioMax and MeshLab Cignoni et al.

We calculated relative jaw length mandible length divided by skull length for each specimen: a jaw length value greater than 1 indicates a posteriorly shifted jaw joint lower jaw is longer than the head and a value less than 1 indicates an anteriorly shifted jaw joint lower jaw is shorter than the head.

We used phylogenetic comparative methods to test for evolutionary correlations among dentition, diet, and body size in frogs. We compiled diet records for taxa, representing genera and 52 anuran families: species in the dentition dataset had published diet records and the remaining lineages are represented by genus-level diet data.

We excluded the remaining anuran species in the dentition dataset 55 edentulous, toothed from the diet analyses due to the lack of known diet records at the species or genus level. The stepping stone sampler for marginal likelihood reconstructions was used with stones and iterations.

The branch lengths were scaled to have a mean of 0. Models were run using the complete taxon dataset, a reduced taxon dataset excluding genus-level diet data, and a reduced taxon dataset excluding genus-level diet data and species-level diet data based on a small sample size less than five individuals.

Because diet data are lacking for many anuran genera, we additionally tested for a phylogenetic correlation between dentition and the relative length of the jaw as a morphological proxy for diet. The body size analysis was run using the complete taxon dataset and a reduced taxon dataset excluding bufonid toads. Computed tomography data tiff stacks and mesh files have been deposited in MorphoSource see Dataset 1. Our editorial process produces two outputs: i public reviews designed to be posted alongside the preprint for the benefit of readers; ii feedback on the manuscript for the authors, including requests for revisions, shown below.

We also include an acceptance summary that explains what the editors found interesting or important about the work. This manuscript will find a broad audience in the fields of herpetology, systematics, as well as 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. Thank you for submitting your article "Rampant tooth loss across million years of frog evolution" for consideration by eLife. Your article has been reviewed by 2 peer reviewers, and the evaluation has been overseen by Patricia Wittkopp as the Senior and Reviewing Editor.

The reviewers have opted to remain anonymous. The reviewers have discussed their reviews with one another, and the Reviewing Editor has drafted this to help you prepare a revised submission. Please address the suggestions from both reviewers provided below, which detail recommended changes to improve the presentation of this work. Abstract: The term "broadly maintained" in the abstract is a bit vague. Results: There is a missed opportunity to examine the evolution of each regional tooth "type" in this study, which would greatly increase the study's impact and help draw conclusions about developmental hypotheses proposed in the discussion.

For example, in the discussion it is mentioned that "Vomerine teeth are not coordinated with dentition on the upper jaw in frogs" and this could be tested and shown here.

Are teeth types lost in any particular order? Or are other non-vomerine tooth types lost in a coordinated fashion? These analyses would be incredibly beneficial, even if just in supplemental materials. Given the range of reliability in the diet data e. Line The relationship between the loss of mineralized structures and delayed ossification has been posited to explain the rampant loss of other skull structures frequently lost in anuran clades — most notably the loss of middle ear structures see Pererya et al.

It would be worth mentioning this here, given it suggests this could be a more common phenomena. Line mentions that direct development may provide an opportunity to alter dental development but you provide no evidence that direct development is associated with shifts in dentition. This would be interesting and easy to examine with your current dataset.

But if you feel it is beyond the scope of this paper, I would at least mention whether there appears to be a correlation based on existing data. Line the paragraph discussing regains does a great job pointing out that some teeth may be present but very small and that regains may or may not have occurred — we can never know based on these meshes alone.

It would be worth adding that even if teeth are truly and completely lost in many microhylids, teeth could simply have been lost more times and never regained. This alternative scenario could be quantified by restricting ancestral state reconstructions to not allow regains, or simply stated as a possibility.

Line Please change "despite that this new world radiation of over 1, species contains" to "despite this new world radiation of over 1, species containing.. Please also consider removing "new world" and "old world" from the manuscript. These terms, although widely used and accepted, are inherently colonial in their perspective.

The section on tooth loss in fossil frogs provides some really interesting and relevant information about tooth loss in this clade. Are these crown-group fossil frogs just adding clades of tooth loss? Do they change any interpretations or assumptions about the analysis on extant taxa?

As written, a general audience may struggle to make these connections if not familiar with these extinct and extant taxonomic groups. Is there any chance for error in dentition survey? Could teeth be present but very unmineralized and not recognized during segmentation? You mention that some microhylids that would appear to lack teeth do have "true teeth" that are very small.

How likely is this across frogs more generally? Is there histological evidence that shows a true lack of teeth in any species? This seems important to discuss more generally and not only in the context of microhylid regains. Diet data are incredibly tough to attain from the literature for most amphibian species.

The authors have done a great job and service compiling the data for this study. The authors point out the range in data that they drew their microphagy versus generalist categorizations from — "singular reports one prey item in one individual to detailed studies investigating the stomach contents of dozens of individuals through space and time".