What does dental gene decay tell us about the regressive evolution of teeth in South American mammals?
Genomic data suggest parallel dental vestigialization within the xenarthran radiation
Recommendation: posted 03 August 2023, validated 07 August 2023
Casane, D. (2023) What does dental gene decay tell us about the regressive evolution of teeth in South American mammals?. Peer Community in Genomics, 100240. 10.24072/pci.genomics.100240
A group of mammals, Xenathra, evolved and diversified in South America during its long period of isolation in the early to mid Cenozoic era. More recently, as a result of the Great Faunal Interchange between South America and North America, many xenarthran species went extinct. The thirty-one extant species belong to three groups: armadillos, sloths and anteaters. They share dental degeneration. However, the level of degeneration is variable. Anteaters entirely lack teeth, sloths have intermediately regressed teeth and most armadillos have a toothless premaxilla, as well as peg-like, single-rooted teeth that lack enamel in adult animals (Vizcaíno 2009). This diversity raises a number of questions about the evolution of dentition in these mammals. Unfortunately, the fossil record is too poor to provide refined information on the different stages of regressive evolution in these clades. In such cases, the identification of loss-of-function mutations and/or relaxed selection in genes related to a character regression can be very informative (Emerling and Springer 2014; Meredith et al. 2014; Policarpo et al. 2021). Indeed, shared and unique pseudogenes/relaxed selection can tell us to what extent regression has occurred in common ancestors and whether some changes are lineage-specific. In addition, the distribution of pseudogenes/relaxed selection on the branches of a phylogenetic tree is related to the evolutionary processes involved. A much higher density of pseudogenes in the most internal branches indicates that degeneration took place early and over a short period of time, consistent with selection against the presence of the morphological character with which they are associated, while pseudogenes distributed evenly in many internal and external branches suggest a more gradual process over many millions of years, in line with relaxed selection and fixation of loss-of-function mutations by genetic drift.
In this paper (Emerling et al. 2023), the authors examined the dynamics of decay of 11 dental genes that may parallel teeth regression. The analyses of the data reported in this paper clearly point to xenarthran teeth having repeatedly regressed in parallel in the three clades. In fact, no loss-of-function mutation is shared by all species examined. However, more genes should be studied to confirm the hypothesis that the common ancestor of extant xenarthrans had normal dentition. There are distinct patterns of gene loss in different lineages that are associated with the variation in dentition observed across the clades. These patterns of gene loss suggest that regressive evolution took place both gradually and in relatively rapid, discrete phases during the diversification of xenarthrans. This study underscores the utility of using pseudogenes to reconstruct evolutionary history of morphological characters when fossils are sparse.
Emerling CA, Gibb GC, Tilak M-K, Hughes JJ, Kuch M, Duggan AT, Poinar HN, Nachman MW, Delsuc F. 2023. Genomic data suggest parallel dental vestigialization within the xenarthran radiation. bioRxiv, 2022.12.09.519446, ver 2, peer-reviewed and recommended by PCI Genomics. https://doi.org/10.1101/2022.12.09.519446
Emerling CA, Springer MS. 2014. Eyes underground: Regression of visual protein networks in subterranean mammals. Molecular Phylogenetics and Evolution 78: 260-270. https://doi.org/10.1016/j.ympev.2014.05.016
Meredith RW, Zhang G, Gilbert MTP, Jarvis ED, Springer MS. 2014. Evidence for a single loss of mineralized teeth in the common avian ancestor. Science 346: 1254390. https://doi.org/10.1126/science.1254390
Policarpo M, Fumey J, Lafargeas P, Naquin D, Thermes C, Naville M, Dechaud C, Volff J-N, Cabau C, Klopp C, et al. 2021. Contrasting gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals. Molecular Biology and Evolution 38: 589-605. https://doi.org/10.1093/molbev/msaa249
Vizcaíno SF. 2009. The teeth of the “toothless”: novelties and key innovations in the evolution of xenarthrans (Mammalia, Xenarthra). Paleobiology 35: 343-366. https://doi.org/10.1666/0094-8373-35.3.343
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
This research was supported by a European Research Council consolidator grant (ConvergeAnt ERC-2015-CoG-683257; FD); the Centre National de la Recherche Scientifique (CNRS; FD); the Scientific Council of the Université de Montpellier (FD); Investissements d’Avenir grants managed by Agence Nationale de la Recherche (CEBA: ANR-10-LABX-25-01; CEMEB: ANR-10-LABX-0004; FD); a National Science Foundation Postdoctoral Research Fellowship in Biology (award no. 1523943; CAE); a National Science Foundation Postdoctoral Fellow Research Opportunities in Europe award (CAE); the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA grant agreement no. PCOFUND-GA-2013-609102, through the PRESTIGE programme coordinated by Campus France (CAE); the France-Berkeley Fund (FD and MWN); and the Natural Sciences and Engineering Research Council of Canada (NSERC, no. RGPIN04184-15) and the Canada Research Chairs program (HNP).
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.12.09.519446
Version of the preprint: 1
Author's Reply, 01 Aug 2023
Decision by Didier Casane, posted 31 Jan 2023, validated 01 Feb 2023
Three reviewers gave very positive feedback on this manuscript. They also suggest that some changes be made to improve its readability and understanding of the results by most readers. I suggest that the most important ones be done. Many minor concerns should also be considered too.
1) The authors assembled a dataset of 11 dental genes: nine genes having well-characterized functions and/or expression patterns tied to tooth development and frequently pseudogenized in edentulous and enamelless taxa, and two other genes expressed in teeth but do not have the same patterns of inactivation. I understand this selection that makes sense, but I was wondering if it could be possible to enlarge the set of genes, for example by looking for pseudogenes in xenarthran genomes and checking those involved in teeth development using mammal gene expression databases. I was wondering if these 11 genes represent a small or a large subset of teeth specific genes. If it is a small subsets and if the ancestral branch is small compared to the xenarthran tree, even if some pseudogenes are shared by all xenarthrans, because there are few of them we need a large gene set to find those that appeared in the common ancestor. Thus, no common loss of function mutations in tooth specific genes could be the consequence of a too small number of genes examined and not evidence of normal teeth and gingiva in the common ancestor.
2) A reviewer wrote: Regarding the methodology, although I understand that they accomplish the goal of getting the sequence of the genes using different approaches, adding a schematic figure showing which method was used for which species would help to understand more easily. Another reviewer wrote: this data collection might also be one of the few limitations of the paper: even with such a broad effort, a lot of genetic information is missing from the final dataset. Except for the few fully sequenced analyzed, it is unclear whether the missing exons of various genes are the reflection of a biological reality or rather of the incomplete molecular sampling due to imperfect amplification or capture and/or lack of depth in the sequencing. This difficulty is exemplified by the DMP1 and MEPE datasets (see below). Since these missing pieces of genes might themselves be involved in the identification of inactivated genes, it slightly blurs the general message. The limited completeness of the dataset for this marker (and the others too) should be directly accessible from the main text to be obvious to help contextualize the interpretation.
Thus, for the 11 genes examined, a clear description of the data completeness is necessary.
3) A reviewer wrote: I also like the evolutionary rationale behind reconstructing dN/dS values and when the inactivation process occurred in the xenarthran phylogeny. I recommend creating a schematic figure showing the rationale. Being more didactic will open the paper to a broader audience.
I agree, although crafting such a figure may not be an easy task.