Genomic data suggest parallel dental vestigialization within the xenarthran radiation

10.24072/pcjournal.303 - Peer Community Journal, Volume 3 (2023), article no. e75.

Get full text PDF Peer reviewed and recommended by PCI

The recent influx of genomic data has provided greater insights into the molecular basis for regressive evolution, or vestigialization, through gene loss and pseudogenization. As such, the analysis of gene degradation patterns has the potential to provide insights into the evolutionary history of regressed anatomical traits. We specifically applied these principles to the xenarthran radiation (anteaters, sloths, armadillos), which is characterized by taxa with a gradation in regressed dental phenotypes. Whether the pattern among extant xenarthrans is due to an ancient and gradual decay of dental morphology or occurred repeatedly in parallel is unknown. We tested these competing hypotheses by examining 11 core dental genes in most living species of Xenarthra, characterizing shared inactivating mutations and patterns of relaxed selection during their radiation. Here we report evidence of independent and distinct events of dental gene loss in the major xenarthran subclades. First, we found strong evidence of complete enamel loss in the common ancestor of sloths and anteaters, suggested by the inactivation of five enamel-associated genes (AMELX, AMTN, MMP20, ENAM, ACP4). Next, whereas dental regression appears to have halted in sloths, presumably a critical event that ultimately permitted adaptation to an herbivorous lifestyle, anteaters continued losing genes on the path towards complete tooth loss. Echoes of this event are recorded in the genomes of all living anteaters, being marked by a 2-bp deletion in a gene critical for dentinogenesis (DSPP) and a putative shared 1-bp insertion in a gene linked to tooth retention (ODAPH). By contrast, in the two major armadillo clades, genes pertaining to the dento-gingival junction and amelogenesis appear to have been independently inactivated prior to losing all or some enamel. These genomic data provide evidence for multiple pathways and rates of anatomical regression, and underscore the utility of using pseudogenes to reconstruct evolutionary history when fossils are sparse.

Published online:
DOI: 10.24072/pcjournal.303
Keywords: Armadillos, Anteaters, Sloths, Dental regression, Gene loss, Molecular evolution, Phylogenetics
Emerling, Christopher A 1, 2, 3; Gibb, Gillian C 4; Tilak, Marie-Ka 1; Hughes, Jonathan J 5; Kuch, Melanie 5; Duggan, Ana T 5; Poinar, Hendrik N 5; Nachman, Michael W 2; Delsuc, Frédéric 1

1 Institut des Sciences de l’Evolution de Montpellier (ISEM), Univ. Montpellier, CNRS, IRD – Montpellier, France
2 Museum of Vertebrate Zoology and Department of Integrative Biology, University of California – Berkeley, CA, USA
3 Biology Department, Reedley College – Reedley, CA, USA
4 School of Natural Sciences, Massey University – Palmerston North, New Zealand
5 McMaster Ancient DNA Centre, Department of Anthropology, McMaster University – Hamilton, ON, Canada
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Emerling, Christopher A and Gibb, Gillian C and Tilak, Marie-Ka and Hughes, Jonathan J and Kuch, Melanie and Duggan, Ana T and Poinar, Hendrik N and Nachman, Michael W and Delsuc, Fr\'ed\'eric},
     title = {Genomic data suggest parallel dental vestigialization within the xenarthran radiation},
     journal = {Peer Community Journal},
     eid = {e75},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.303},
     language = {en},
     url = {}
AU  - Emerling, Christopher A
AU  - Gibb, Gillian C
AU  - Tilak, Marie-Ka
AU  - Hughes, Jonathan J
AU  - Kuch, Melanie
AU  - Duggan, Ana T
AU  - Poinar, Hendrik N
AU  - Nachman, Michael W
AU  - Delsuc, Frédéric
TI  - Genomic data suggest parallel dental vestigialization within the xenarthran radiation
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.303
LA  - en
ID  - 10_24072_pcjournal_303
ER  - 
%0 Journal Article
%A Emerling, Christopher A
%A Gibb, Gillian C
%A Tilak, Marie-Ka
%A Hughes, Jonathan J
%A Kuch, Melanie
%A Duggan, Ana T
%A Poinar, Hendrik N
%A Nachman, Michael W
%A Delsuc, Frédéric
%T Genomic data suggest parallel dental vestigialization within the xenarthran radiation
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%R 10.24072/pcjournal.303
%G en
%F 10_24072_pcjournal_303
Emerling, Christopher A; Gibb, Gillian C; Tilak, Marie-Ka; Hughes, Jonathan J; Kuch, Melanie; Duggan, Ana T; Poinar, Hendrik N; Nachman, Michael W; Delsuc, Frédéric. Genomic data suggest parallel dental vestigialization within the xenarthran radiation. Peer Community Journal, Volume 3 (2023), article  no. e75. doi : 10.24072/pcjournal.303.

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100240

Conflict of interest of the recommender and peer reviewers:
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.

[1] Albalat, R.; Cañestro, C. Evolution by gene loss, Nature Reviews Genetics, Volume 17 (2016) no. 7, pp. 379-391 | DOI

[2] Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, Volume 30 (2014) no. 15, pp. 2114-2120 | DOI

[3] Burga, A.; Wang, W.; Ben-David, E.; Wolf, P. C.; Ramey, A. M.; Verdugo, C.; Lyons, K.; Parker, P. G.; Kruglyak, L. A genetic signature of the evolution of loss of flight in the Galapagos cormorant, Science, Volume 356 (2017) no. 6341 | DOI

[4] Casane, D. What does dental gene decay tell us about the regressive evolution of teeth in South American mammals?, Peer Community in Genomics (2023) | DOI

[5] Charles, C.; Solé, F.; Rodrigues, H. G.; Viriot, L. Under pressure? Dental adaptations to termitophagy and vermivory among mammals, Evolution, Volume 67 (2013) no. 6, pp. 1792-1804 | DOI

[6] Choo, S. W.; Rayko, M.; Tan, T. K.; Hari, R.; Komissarov, A.; Wee, W. Y.; Yurchenko, A. A.; Kliver, S.; Tamazian, G.; Antunes, A.; Wilson, R. K.; Warren, W. C.; Koepfli, K.-P.; Minx, P.; Krasheninnikova, K.; Kotze, A.; Dalton, D. L.; Vermaak, E.; Paterson, I. C.; Dobrynin, P.; Sitam, F. T.; Rovie-Ryan, J. J.; Johnson, W. E.; Yusoff, A. M.; Luo, S.-J.; Karuppannan, K. V.; Fang, G.; Zheng, D.; Gerstein, M. B.; Lipovich, L.; O'Brien, S. J.; Wong, G. J. Pangolin genomes and the evolution of mammalian scales and immunity, Genome Research, Volume 26 (2016) no. 10, pp. 1312-1322 | DOI

[7] Ciancio, M. R.; Vieytes, E. C.; Carlini, A. A. When xenarthrans had enamel: insights on the evolution of their hypsodonty and paleontological support for independent evolution in armadillos, Naturwissenschaften, Volume 101 (2014) no. 9, pp. 715-725 | DOI

[8] Ciancio, M. R.; Vieytes, E. C.; Castro, M. C.; Carlini, A. A. Dental enamel structure in long-nosed armadillos (Xenarthra: Dasypus) and its evolutionary implications, Zoological Journal of the Linnean Society, Volume 192 (2020) no. 4, pp. 1237-1252 | DOI

[9] Davit-Béal, T.; Tucker, A. S.; Sire, J.-Y. Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations, Journal of Anatomy, Volume 214 (2009) no. 4, pp. 477-501 | DOI

[10] Delsuc, F.; Superina, M.; Tilak, M.-K.; Douzery, E. J.; Hassanin, A. Molecular phylogenetics unveils the ancient evolutionary origins of the enigmatic fairy armadillos, Molecular Phylogenetics and Evolution, Volume 62 (2012) no. 2, pp. 673-680 | DOI

[11] Delsuc, F.; Gasse, B.; Sire, J.-Y. Evolutionary analysis of selective constraints identifies ameloblastin (AMBN) as a potential candidate for amelogenesis imperfecta, BMC Evolutionary Biology, Volume 15 (2015) no. 1 | DOI

[12] Delsuc, F.; Kuch, M.; Gibb, G. C.; Hughes, J.; Szpak, P.; Southon, J.; Enk, J.; Duggan, A. T.; Poinar, H. N. Resolving the phylogenetic position of Darwin's extinct ground sloth (Mylodon darwinii) using mitogenomic and nuclear exon data, Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1878 | DOI

[13] DISCOVAR de novo: Large genome assembler (

[14] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | DOI

[15] Emerling, C. A.; Springer, M. S. Eyes underground: Regression of visual protein networks in subterranean mammals, Molecular Phylogenetics and Evolution, Volume 78 (2014), pp. 260-270 | DOI

[16] Emerling, C. A.; Huynh, H. T.; Nguyen, M. A.; Meredith, R. W.; Springer, M. S. Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1819 | DOI

[17] Emerling, C. A. Genomic regression of claw keratin, taste receptor and light-associated genes provides insights into biology and evolutionary origins of snakes, Molecular Phylogenetics and Evolution, Volume 115 (2017), pp. 40-49 | DOI

[18] Emerling, C. A.; Delsuc, F.; Nachman, M. W. Chitinase genes (CHIAs) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals, Science Advances, Volume 4 (2018) no. 5 | DOI

[19] Ferigolo, J. Evolutionary trends of the histological pattern in the teeth of Edentata (Xenarthra), Archives of Oral Biology, Volume 30 (1985) no. 1, pp. 71-82 | DOI

[20] Fisher, L. W. DMP1 and DSPP: Evidence for Duplication and Convergent Evolution of Two SIBLING Proteins, Cells Tissues Organs, Volume 194 (2011) no. 2-4, pp. 113-118 | DOI

[21] Foley, N. M.; Springer, M. S.; Teeling, E. C. Mammal madness: is the mammal tree of life not yet resolved?, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 371 (2016) no. 1699 | DOI

[22] Fong, D. W.; Kane, T. C.; Culver, D. C. Vestigialization and loss of nonfunctional characters, Annual Review of Ecology and Systematics, Volume 26 (1995) no. 1, pp. 249-268 | DOI

[23] Fouillen, A.; Dos Santos Neves, J.; Mary, C.; Castonguay, J.-D.; Moffatt, P.; Baron, C.; Nanci, A. Interactions of AMTN, ODAM and SCPPPQ1 proteins of a specialized basal lamina that attaches epithelial cells to tooth mineral, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[24] Freeman, P. W. Nectarivorous feeding mechanisms in bats, Biological Journal of the Linnean Society, Volume 56 (1995) no. 3, pp. 439-463 | DOI

[25] Ganss, B.; Abbarin, N. Maturation and beyond: proteins in the developmental continuum from enamel epithelium to junctional epithelium, Frontiers in Physiology, Volume 5 (2014) | DOI

[26] Gasse, B.; Silvent, J.; Sire, J.-Y. Evolutionary Analysis Suggests That AMTN is Enamel-specific and a Candidate for AI, Journal of Dental Research, Volume 91 (2012) no. 11, pp. 1085-1089 | DOI

[27] Gaudin, T. J.; Branham, D. G. The phylogeny of the Myrmecophagidae (Mammalia, Xenarthra, Vermilingua) and the relationship of Eurotamandua to the Vermilingua, Journal of Mammalian Evolution, Volume 5 (1998) no. 3, pp. 237-265 | DOI

[28] Gibb, G. C.; Condamine, F. L.; Kuch, M.; Enk, J.; Moraes-Barros, N.; Superina, M.; Poinar, H. N.; Delsuc, F. Shotgun Mitogenomics Provides a Reference Phylogenetic Framework and Timescale for Living Xenarthrans, Molecular Biology and Evolution, Volume 33 (2015) no. 3, pp. 621-642 | DOI

[29] Gullard, A.; Gluhak-Heinrich, J.; Papagerakis, S.; Sohn, P.; Unterbrink, A.; Chen, S.; MacDougall, M. MEPE Localization in the Craniofacial Complex and Function in Tooth Dentin Formation, Journal of Histochemistry & Cytochemistry, Volume 64 (2016) no. 4, pp. 224-236 | DOI

[30] Hautier, L.; Gomes Rodrigues, H.; Billet, G.; Asher, R. J. The hidden teeth of sloths: evolutionary vestiges and the development of a simplified dentition, Scientific Reports, Volume 6 (2016) no. 1 | DOI

[31] Jeffery, W. R. Regressive Evolution in Astyanax Cavefish, Annual Review of Genetics, Volume 43 (2009) no. 1, pp. 25-47 | DOI

[32] Jones, K. E.; Bielby, J.; Cardillo, M.; Fritz, S. A.; O'Dell, J.; Orme, C. D. L.; Safi, K.; Sechrest, W.; Boakes, E. H.; Carbone, C.; Connolly, C.; Cutts, M. J.; Foster, J. K.; Grenyer, R.; Habib, M.; Plaster, C. A.; Price, S. A.; Rigby, E. A.; Rist, J.; Teacher, A.; Bininda-Emonds, O. R. P.; Gittleman, J. L.; Mace, G. M.; Purvis, A. PanTHERIA: a species‐level database of life history, ecology, and geography of extant and recently extinct mammals, Ecology, Volume 90 (2009) no. 9, p. 2648-2648 | DOI

[33] Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; Thierer, T.; Ashton, B.; Meintjes, P.; Drummond, A. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data, Bioinformatics, Volume 28 (2012) no. 12, pp. 1647-1649 | DOI

[34] Kim, Y.; Lee, Y.; Kasimoglu, Y.; Seymen, F.; Simmer, J.; Hu, J.-C.; Cho, E.-S.; Kim, J.-W. Recessive Mutations in ACP4 Cause Amelogenesis Imperfecta, Journal of Dental Research, Volume 101 (2021) no. 1, pp. 37-45 | DOI

[35] Lagerström, M.; Dahl, N.; Nakahori, Y.; Nakagome, Y.; Bäckman, B.; Landegren, U.; Pettersson, U. A deletion in the amelogenin gene (AMG) causes X-linked amelogenesis imperfecta (AIH1), Genomics, Volume 10 (1991) no. 4, pp. 971-975 | DOI

[36] Lahti, D. C.; Johnson, N. A.; Ajie, B. C.; Otto, S. P.; Hendry, A. P.; Blumstein, D. T.; Coss, R. G.; Donohue, K.; Foster, S. A. Relaxed selection in the wild, Trends in Ecology & Evolution, Volume 24 (2009) no. 9, pp. 487-496 | DOI

[37] Lartillot, N.; Poujol, R. A Phylogenetic Model for Investigating Correlated Evolution of Substitution Rates and Continuous Phenotypic Characters, Molecular Biology and Evolution, Volume 28 (2010) no. 1, pp. 729-744 | DOI

[38] Lartillot, N.; Delsuc, F. Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model, Evolution, Volume 66 (2012) no. 6, pp. 1773-1787 | DOI

[39] Leal, F.; Cohn, M. J. Loss and Re-emergence of Legs in Snakes by Modular Evolution of Sonic hedgehog and HOXD Enhancers, Current Biology, Volume 26 (2016) no. 21, pp. 2966-2973 | DOI

[40] Lee, H.-K.; Ji, S.; Park, S.-J.; Choung, H.-W.; Choi, Y.; Lee, H.-J.; Park, S.-Y.; Park, J.-C. Odontogenic Ameloblast-associated Protein (ODAM) Mediates Junctional Epithelium Attachment to Teeth via Integrin-ODAM-Rho Guanine Nucleotide Exchange Factor 5 (ARHGEF5)-RhoA Signaling, Journal of Biological Chemistry, Volume 290 (2015) no. 23, pp. 14740-14753 | DOI

[41] Li, C.; Wu, X.-C.; Rieppel, O.; Wang, L.-T.; Zhao, L.-J. An ancestral turtle from the Late Triassic of southwestern China, Nature, Volume 456 (2008) no. 7221, pp. 497-501 | DOI

[42] Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform, Bioinformatics, Volume 25 (2009) no. 14, pp. 1754-1760 | DOI

[43] Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools, Bioinformatics, Volume 25 (2009) no. 16, pp. 2078-2079 | DOI

[44] Liang, T.; Wang, S.-K.; Smith, C.; Zhang, H.; Hu, Y.; Seymen, F.; Koruyucu, M.; Kasimoglu, Y.; Kim, J.-W.; Zhang, C.; Saunders, T. L.; Simmer, J. P.; Hu, J. C.-C. Enamel defects in Acp4R110C/R110C mice and human ACP4 mutations, Scientific Reports, Volume 12 (2022) no. 1 | DOI

[45] Martin, B. E. Tooth development in dasypus novemcinctus, Journal of Morphology, Volume 27 (1916) no. 3, pp. 647-691 | DOI

[46] McKenna, M.; Wyss, A.; Flynn, J. Paleogene Pseudoglyptodont Xenarthrans from Central Chile and Argentine Patagonia, American Museum Novitates, Volume 3536 (2006) no. 1 | DOI

[47] McKnight, D. A.; Fisher, L. W. Molecular evolution of dentin phosphoprotein among toothed and toothless animals, BMC Evolutionary Biology, Volume 9 (2009) no. 1 | DOI

[48] Meredith, R. W.; Gatesy, J.; Murphy, W. J.; Ryder, O. A.; Springer, M. S. Molecular Decay of the Tooth Gene Enamelin (ENAM) Mirrors the Loss of Enamel in the Fossil Record of Placental Mammals, PLoS Genetics, Volume 5 (2009) no. 9 | DOI

[49] Meredith, R. W.; Gatesy, J.; Cheng, J.; Springer, M. S. Pseudogenization of the tooth gene enamelysin (MMP20) in the common ancestor of extant baleen whales, Proceedings of the Royal Society B: Biological Sciences, Volume 278 (2010) no. 1708, pp. 993-1002 | DOI

[50] Meredith, R. W.; Janecka, J. E.; Gatesy, J.; Ryder, O. A.; Fisher, C. A.; Teeling, E. C.; Goodbla, A.; Eizirik, E.; Simao, T. L. L.; Stadler, T.; Rabosky, D. L.; Honeycutt, R. L.; Flynn, J. J.; Ingram, C. M.; Steiner, C.; Williams, T. L.; Robinson, T. J.; Burk-Herrick, A.; Westerman, M.; Ayoub, N. A.; Springer, M. S.; Murphy, W. J. Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification, Science, Volume 334 (2011) no. 6055, pp. 521-524 | DOI

[51] Meredith, R. W.; Gatesy, J.; Springer, M. S. Molecular decay of enamel matrix protein genes in turtles and other edentulous amniotes, BMC Evolutionary Biology, Volume 13 (2013) no. 1 | DOI

[52] Meredith, R. W.; Zhang, G.; Gilbert, M. T. P.; Jarvis, E. D.; Springer, M. S. Evidence for a single loss of mineralized teeth in the common avian ancestor, Science, Volume 346 (2014) no. 6215 | DOI

[53] Mu, Y.; Huang, X.; Liu, R.; Gai, Y.; Liang, N.; Yin, D.; Shan, L.; Xu, S.; Yang, G. ACPT gene is inactivated in mammalian lineages that lack enamel or teeth, PeerJ, Volume 9 (2021) | DOI

[54] Nakayama, Y.; Holcroft, J.; Ganss, B. Enamel Hypomineralization and Structural Defects in Amelotin-deficient Mice, Journal of Dental Research, Volume 94 (2015) no. 5, pp. 697-705 | DOI

[55] Nowak, R. Walker’s Mammals of the World, Vol. 1, 6th ed., John Hopkins University Press, Baltimore, Maryland., 1999

[56] Parry, D. A.; Brookes, S. J.; Logan, C. V.; Poulter, J. A.; El-Sayed, W.; Al-Bahlani, S.; Al Harasi, S.; Sayed, J.; Raïf, E. M.; Shore, R. C.; Dashash, M.; Barron, M.; Morgan, J. E.; Carr, I. M.; Taylor, G. R.; Johnson, C. A.; Aldred, M. J.; Dixon, M. J.; Wright, J. T.; Kirkham, J.; Inglehearn, C. F.; Mighell, A. J. Mutations in C4orf26, Encoding a Peptide with In Vitro Hydroxyapatite Crystal Nucleation and Growth Activity, Cause Amelogenesis Imperfecta, The American Journal of Human Genetics, Volume 91 (2012) no. 3, pp. 565-571 | DOI

[57] Prasad, M.; Laouina, S.; El Alloussi, M.; Dollfus, H.; Bloch-Zupan, A. Amelogenesis Imperfecta, Journal of Dental Research, Volume 95 (2016) no. 13, pp. 1457-1463 | DOI

[58] Poulter, J. A.; Murillo, G.; Brookes, S. J.; Smith, C. E. L.; Parry, D. A.; Silva, S.; Kirkham, J.; Inglehearn, C. F.; Mighell, A. J. Deletion of ameloblastin exon 6 is associated with amelogenesis imperfecta, Human Molecular Genetics, Volume 23 (2014) no. 20, pp. 5317-5324 | DOI

[59] Rajpar, M. H. Mutation of the gene encoding the enamel-specific protein, enamelin, causes autosomal-dominant amelogenesis imperfecta, Human Molecular Genetics, Volume 10 (2001) no. 16, pp. 1673-1677 | DOI

[60] Randall, J. G.; Gatesy, J.; Springer, M. S. Molecular evolutionary analyses of tooth genes support sequential loss of enamel and teeth in baleen whales (Mysticeti), Molecular Phylogenetics and Evolution, Volume 171 (2022) | DOI

[61] Reiss, K. Z. Using Phylogenies to Study Convergence: The Case of the Ant-Eating Mammals, American Zoologist, Volume 41 (2001) no. 3, pp. 507-525 | DOI

[62] Renaud, G.; Stenzel, U.; Kelso, J. leeHom: adaptor trimming and merging for Illumina sequencing reads, Nucleic Acids Research, Volume 42 (2014) no. 18 | DOI

[63] Rosenberg, H. I.; Richardson, K. C. Cephalic morphology of the honey possum, Tarsipes rostratus (Marsupialia: Tarsipedidae); an obligate nectarivore, Journal of Morphology, Volume 223 (1995) no. 3, pp. 303-323 | DOI

[64] Saarinen, J.; Karme, A. Tooth wear and diets of extant and fossil xenarthrans (Mammalia, Xenarthra) – Applying a new mesowear approach, Palaeogeography, Palaeoclimatology, Palaeoecology, Volume 476 (2017), pp. 42-54 | DOI

[65] Seymen, F.; Kim, Y. J.; Lee, Y. J.; Kang, J.; Kim, T.-H.; Choi, H.; Koruyucu, M.; Kasimoglu, Y.; Tuna, E. B.; Gencay, K.; Shin, T. J.; Hyun, H.-K.; Kim, Y.-J.; Lee, S.-H.; Lee, Z. H.; Zhang, H.; Hu, J. C.-C.; Simmer, J. P.; Cho, E.-S.; Kim, J.-W. Recessive Mutations in ACPT , Encoding Testicular Acid Phosphatase, Cause Hypoplastic Amelogenesis Imperfecta, The American Journal of Human Genetics, Volume 99 (2016) no. 5, pp. 1199-1205 | DOI

[66] Sharma, V.; Hecker, N.; Roscito, J. G.; Foerster, L.; Langer, B. E.; Hiller, M. A genomics approach reveals insights into the importance of gene losses for mammalian adaptations, Nature Communications, Volume 9 (2018) no. 1 | DOI

[67] Simpson, G. Enamel on the teeth of an Eocene edentate, American Museum Novitates, Volume 4 (1932), pp. 1-4

[68] Sire, J.-Y.; Delgado, S. C.; Girondot, M. Hen's teeth with enamel cap: from dream to impossibility, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | DOI

[69] Smith, C. E.; Murillo, G.; Brookes, S. J.; Poulter, J. A.; Silva, S.; Kirkham, J.; Inglehearn, C. F.; Mighell, A. J. Deletion of amelotin exons 3–6 is associated with amelogenesis imperfecta, Human Molecular Genetics, Volume 25 (2016) no. 16, pp. 3578-3587 | DOI

[70] Smith, C. E. L.; Poulter, J. A.; Antanaviciute, A.; Kirkham, J.; Brookes, S. J.; Inglehearn, C. F.; Mighell, A. J. Amelogenesis Imperfecta; Genes, Proteins, and Pathways, Frontiers in Physiology, Volume 8 (2017) | DOI

[71] Springer, M. S.; Starrett, J.; Morin, P. A.; Lanzetti, A.; Hayashi, C.; Gatesy, J. Inactivation of C4orf26 in toothless placental mammals, Molecular Phylogenetics and Evolution, Volume 95 (2016), pp. 34-45 | DOI

[72] Springer, M. S.; Emerling, C. A.; Gatesy, J.; Randall, J.; Collin, M. A.; Hecker, N.; Hiller, M.; Delsuc, F. Odontogenic ameloblast-associated (ODAM) is inactivated in toothless/enamelless placental mammals and toothed whales, BMC Evolutionary Biology, Volume 19 (2019) no. 1 | DOI

[73] Spurgin, A. M. Enamel in the teeth of an embryo edentate (Dasypus novemcinctus linn), American Journal of Anatomy, Volume 3 (1904) no. 1, pp. 75-84 | DOI

[74] Sreenath, T.; Thyagarajan, T.; Hall, B.; Longenecker, G.; D'Souza, R.; Hong, S.; Wright, J. T.; MacDougall, M.; Sauk, J.; Kulkarni, A. B. Dentin Sialophosphoprotein Knockout Mouse Teeth Display Widened Predentin Zone and Develop Defective Dentin Mineralization Similar to Human Dentinogenesis Imperfecta Type III, Journal of Biological Chemistry, Volume 278 (2003) no. 27, pp. 24874-24880 | DOI

[75] Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics, Volume 30 (2014) no. 9, pp. 1312-1313 | DOI

[76] Stenzel, U. Network-aware-bwa (accessed 5.9.17), 2017 (

[77] Sun, Y.; Chen, L.; Ma, S.; Zhou, J.; Zhang, H.; Feng, J. Q.; Qin, C. Roles of DMP1 Processing in Osteogenesis, Dentinogenesis and Chondrogenesis, Cells Tissues Organs, Volume 194 (2011) no. 2-4, pp. 199-204 | DOI

[78] Toyosawa, S.; Fujiwara, T.; Ooshima, T.; Shintani, S.; Sato, A.; Ogawa, Y.; Sobue, S.; Ijuhin, N. Cloning and characterization of the human ameloblastin gene, Gene, Volume 256 (2000) no. 1-2, pp. 1-11 | DOI

[79] Ungar, P. Mammal teeth: Origin, evolution and diversity, John Hopkins University Press, Baltimore, Maryland, 2010

[80] Vizcaíno, S. F. The teeth of the “toothless”: novelties and key innovations in the evolution of xenarthrans (Mammalia, Xenarthra), Paleobiology, Volume 35 (2009) no. 3, pp. 343-366 | DOI

[81] Wazen, R.; Moffatt, P.; Ponce, K.; Kuroda, S.; Nishio, C.; Nanci, A. Inactivation of the Odontogenic ameloblast-associated gene affects the integrity of the junctional epithelium and gingival healing, European Cells and Materials, Volume 30 (2015), pp. 187-199 | DOI

[82] Xiao, S.; Yu, C.; Chou, X.; Yuan, W.; Wang, Y.; Bu, L.; Fu, G.; Qian, M.; Yang, J.; Shi, Y.; Hu, L.; Han, B.; Wang, Z.; Huang, W.; Liu, J.; Chen, Z.; Zhao, G.; Kong, X. Dentinogenesis imperfecta 1 with or without progressive hearing loss is associated with distinct mutations in DSPP, Nature Genetics, Volume 27 (2001) no. 2, pp. 201-204 | DOI

[83] Yang, Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution, Molecular Biology and Evolution, Volume 15 (1998) no. 5, pp. 568-573 | DOI

[84] Yang, Z.; Nielsen, R. Synonymous and nonsynonymous rate variation in nuclear genes of mammals, Journal of Molecular Evolution, Volume 46 (1998) no. 4, pp. 409-418 | DOI

[85] Yang, Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood, Molecular Biology and Evolution, Volume 24 (2007) no. 8, pp. 1586-1591 | DOI

[86] Zoonomia Consortium A comparative genomics multitool for scientific discovery and conservation, Nature, Volume 587 (2020) no. 7833, pp. 240-245 | DOI

Cited by Sources: