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• W3022134496 abstract "In a new study, LeBlanc and co-workers have discovered an unusually complex dentition in a fossil relative of the modern-day tuatara that features compound occlusal surfaces, thick and prismatic enamel, and a novel enamel-to-bone tooth attachment. This finding suggests that complex dentitions arose independently in several reptilian lineages. In a new study, LeBlanc and co-workers have discovered an unusually complex dentition in a fossil relative of the modern-day tuatara that features compound occlusal surfaces, thick and prismatic enamel, and a novel enamel-to-bone tooth attachment. This finding suggests that complex dentitions arose independently in several reptilian lineages. The majority of reptilian jaws are equipped with blade-like, pointy, and similar-shaped teeth ideally suited to grasp and bite prey animals. These typical reptilian teeth are characterized by multiple generations of replacement teeth (polyphyodonty), similar-shaped tooth forms (homodonty), and pleurodont or acrodont modes of attachment (direct attachment to the jaw bone without a periodontal ligament). There are relatively few exceptions to this rule. Among the extant exceptions are a group of agamid lizards of the genus Uromastyx that feed on an herbivorous diet. Uromastyx teeth are characterized by thick and prismatic enamel, posterior to anterior tooth row extension, and the lack of a classic reptilian tooth-replacement regimen (Figure 1). Fossil exceptions from the reptilian-tooth stereotype include a group of herbivorous reptiles with transversely oriented, interlocking teeth from the North American Cretaceous, consisting of Polyglyphanodon sternbergi, Dicothodon moorensis, Bicuspidon numerosus, and Peniteius aquilonius [1Nydam R.L. Cifelli R.L. New data in the dentition of the scincomorphan lizard Polyglyphanodon sternbergi.Acta Paleontol. Pol. 2005; 50: 73-78Google Scholar]. Enamel-like tooth coverings have also been described in fossilized mammalian ancestors, including cynodonts and gorgonopsids [2Poole D.F.G. The structure of the teeth of some mammal-like reptiles.Q. Jl. Micr. Sci. 1956; 97: 303-312Google Scholar]. A clade of aquatic fossil reptiles, the mosasaurs, were distinguished by another exception from the reptilian-tooth stereotype: their multilayer pseudo-ligamentous mode of tooth attachment when compared to the attachment via a mineralized socket typically seen in reptiles [3Luan X. Walker C. Dangaria S. Ito Y. Druzinsky R. Jarosius K. Lesot H. Rieppel O. The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium.Evol. Dev. 2009; 11: 247-259Crossref PubMed Scopus (50) Google Scholar]. Even among archosaurs (a broad taxonomic classification including dinosaurs, reptiles and modern birds), the uniform dentition of modern crocodilians betrays their meandering evolutionary history, involving independent evolution of high-complexity dentitions at least three times [4Melstrom K.M. Irmis R.B. Repeated evolution of herbivorous crocodyliforms during the age of dinosaurs.Curr. Biol. 2019; 29: 2389-2395Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar]. Similarly, teeth of the modern tuatara Sphenodon punctatus — a distinct lineage of reptiles — with their aprismatic enamel and basal bone attachment are vastly different from the teeth covered with thick enamel reported in earlier studies in fossil relatives of the tuatara, the Sphenodontians Eilenodon robustus [5Jones M.E.H. Lucas P.W. Tucker A.S. Watson A.P. Sertich J.J.W. Foster J.R. Williams R. Garbe U. Bevitt J.J. Salvemini F. Neutron scanning reveals unexpected complexity in the enamel thickness of an herbivorous Jurassic reptile.J. R. Soc. Interface. 2018; 15: 20180039Crossref PubMed Scopus (14) Google Scholar] and Priosphenodon avelasi [6LeBlanc A.R.H. Apesteguía S. Larsson H.C.E. Caldwell M.W. Unique tooth morphology and prismatic enamel in Late Cretaceous sphenodontians from Argentina.Curr. Biol. 2020; 30: 1755-1761Abstract Full Text Full Text PDF Scopus (10) Google Scholar]. In a new study published in this issue of Current Biology, LeBlanc and colleagues report on the discovery of prismatic enamel layers with increased thickness and corresponding specialization of tooth form in herbivorous reptiles; a finding that goes far beyond the occasional histological oddity, but rather offers unique glimpses into the emergence of advanced morphological characters during the evolution of teeth. The occurrence of thick and prismatic enamel in mammals versus non-mammalian vertebrates, and the fact that human enamel is relatively thicker than chimpanzee or gorilla enamel, establish enamel thickness and organization as an important character in vertebrate evolution. There are considerable functional advantages associated with thick enamel as it protects teeth from microwear and abrasion due to dietary silicates [7Lucas P.W. van Casteren A. Al-Fadhalah K. Almusallam A.S. Henry A.G. Michael S. Watzke J. Reed D.A. Diekwisch T.G.H. Strait D.S. Atkins A.G. The role of dust, grit and phytoliths in tooth wear.Ann. Zool. Fennici. 2014; 51: 43-152Crossref Scopus (93) Google Scholar], and the organization of enamel into rods and prisms prevents crack extension toward the vital pulp and dissipates fracture energy. The majority of the lepidosaurs and archosaurs with complex dentitions and thickened enamel described here evolved together with mammals and many other dead-end lineages at the beginning of the Mesozoic, a time period characterized by the recovery from the great Permian extinction [8Luo Z.X. Transformation and diversification in early mammal evolution.Nature. 2007; 450: 1011-1019Crossref PubMed Scopus (376) Google Scholar]. At that time, competition for food sources pressured organisms to occupy unique ecological niches and to evolve characters with diverse apomorphies [8Luo Z.X. Transformation and diversification in early mammal evolution.Nature. 2007; 450: 1011-1019Crossref PubMed Scopus (376) Google Scholar]. In such a competitive ecological environment, thickened enamel coverings with increased fracture resistance facilitated access to yet un-explored food sources and thus provided a survival advantage. Compared to the narrow tooth shapes and thin enamel coverings of their carnivorous counterparts, herbivorous species with their broad occlusal surfaces and patterned enamel have distinct advantages when it comes to food diversity. Earlier studies in insects, cichlids, and Darwin’s finches demonstrated that the availability of underexploited food resources is an important prerequisite for the evolution of new species, allowing them to allocate more time and energy for reproduction and less investment into searching for prey and feeding on nutritious diets [9Stewart T.A. Albertson R.C. Evolution of a unique predatory feeding apparatus: functional anatomy, development and a genetic locus for jaw laterality in Lake Tanganyika scale-eating cichlids.BMC Biol. 2010; 8: 8Crossref PubMed Scopus (57) Google Scholar, 10Borges I. Soares A.O. Magro A. Hemptinne J.L. Prey availability in time and space is a driving force in life history evolution of predatory insects.Evol. Ecol. 2011; 25: 1307-1319Crossref Scopus (32) Google Scholar, 11Lamichhane B.R. Persoon G.A. Leirs H. Musters C.J.M. Subedi N. Gairhe K.P. Pokhera C.P.I. Poudel S. Mishra R. Dhakal M. et al.Are conflict-causing tigers different? Another perspective for understanding human-tiger conflict in Chitwan National Park, Nepal.Glob. Ecol. Conserv. 2017; 11: 177-187Crossref Scopus (12) Google Scholar]. For example, studies in primates have linked the presence of long shearing crests to folivorous diets, whereas intermediate crest lengths correspond to frugivorous diets, and relatively flat, blunt molar teeth are ideal to partition fruits, nuts, flowers, and buds, but also suitable to cope with an omnivorous diet [12Teaford M.F. Ungar P.S. Diet and the evolution of the earliest human ancestors.Proc. Natl. Acad. Sci. USA. 2000; 97: 13506-13511Crossref PubMed Scopus (291) Google Scholar]. The molecular basis responsible for the changes in enamel structure that occurred during the evolution of herbivorous sphenodonts, squamates, and archosaurs remains to be discovered. The majority of the proteins that contribute to enamel crystal formation and elongation are structural proteins such as amelogenin, ameloblastin, and enamelin, or enzymes such as MMP20 and KLK4. These proteins are thought to contribute to the physical spacing between enamel crystals, enamel crystal nucleation, or apatite crystal growth [13Pandya M. Diekwisch T.G.H. Enamel biomimetics—fiction or future of dentistry.Int. J. Oral Sci. 2019; 11: 8Crossref PubMed Scopus (56) Google Scholar]. The major protein in the developing enamel matrix is amelogenin, which comprises approximately 90% of all enamel proteins by volume. Amelogenins contain a polyproline repeat motif that preferentially binds to apatite versus carbonate and promotes apatite crystal elongation [14Gopinathan G. Jin T. Liu M. Li S. Atsawasuwan P. Galang M.T. Allen M. Luan X. Diekwisch T.G.H. The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation.Front. Physiol. 2014; 5: 430Crossref PubMed Scopus (16) Google Scholar]. This polyproline repeat region is expanded by 5–7 tripeptide inserts in ruminants such as cows and goats and is either lost or irregular in modern amphibians and reptiles. Alteration of this polyproline repeat element in a mouse model that overexpresses a frog amelogenin resulted in a loss of enamel prism structure and disorganized enamel [15Jin T. Ito Y. Luan X. Dangaria S. Walker C. Allen M. Kulkarni A. Gibson C. Braatz R. Liao X. Diekwisch T.G. Elongated polyproline motifs facilitate enamel evolution through matrix subunit compaction.PLoS Biol. 2009; 7e1000262Crossref PubMed Scopus (44) Google Scholar], underscoring the importance of the amelogenin polyproline repeat region for prismatic enamel in mammals. The importance of amelogenin for a higher-order enamel structure has been further illustrated by an ameloblastin-rich enamel mouse model in which the amelogenin matrix protein was genetically removed, resulting in short, thick, and randomly oriented enamel crystals and a lack of enamel prisms [16Lu X. Ito Y. Kulkarni A. Gibson C. Luan X. Diekwisch T.G.H. Ameloblastin-rich enamel matrix favors short and randomly oriented apatite crystals.Eur. J. Oral Sci. 2011; 119: 254-260Crossref PubMed Scopus (15) Google Scholar]. Another enamel gene, Enamelin, has been associated with changes in enamel thickness in response to diet [17Kelley J.L. Swanson W.J. Dietary change and adaptive evolution of enamelin in humans and among primates.Genetics. 2008; 178: 1595-1603Crossref PubMed Scopus (38) Google Scholar], confirming a direct relationship between ecological niches and tooth shape. Whereas enamel matrix proteins immediately contribute to enamel crystal size and habit, the timing and quantity of enamel matrix protein secretion is tightly regulated by transcription factors such as FoxO1, Msx2, and Dlx3. These transcription factors control the secretion of enamel proteins and the movement of enamel matrix-secreting cells, the ameloblasts, by regulating the promoter regions of downstream genes. Such enamel-organ transcriptional networks and underlying structural genes are subject to change during vertebrate evolution. One of the likely factors contributing to the changes in transcription factors and structural genes during evolution are epigenetic mechanisms such as cytosine DNA methylation. Epigenetic factors have profound influence on gene regulation and morphogenesis, and also affect phenotypic plasticity as it contributes to epigenetic inheritance of traits [18Kronholm I. Collins S. Epigenetic mutations can both help and hinder adaptive evolution.Mol. Ecol. 2016; 25: 1856-1868Crossref PubMed Scopus (98) Google Scholar, 19Guerrero-Bosagna C. From epigenotype to new genotypes: Relevance of epigenetic mechanisms in the emergence of genomic evolutionary novelty.Semin. Cell Dev. Biol. 2020; 97: 86-92Crossref PubMed Scopus (11) Google Scholar, 20Sarkies P. Molecular mechanisms of epigenetic inheritance: Possible evolutionary implications.Semin. Cell Dev. Biol. 2020; 97: 106-115Crossref PubMed Scopus (32) Google Scholar]. As a result, it is likely that environmental influences such as changes in diet affect enamel and jaw evolution through yet-to-be determined epigenetic mechanisms. Even without genetic or epigenetic context, LeBlanc’s report of Late Cretaceous sphenodont teeth gives plenty of insights into the evolution of tooth enamel and tooth attachment. Priosphenodon’s organized and thick enamel layer, in conjunction with a lateral mode of tooth attachment and replacement, is one of several fossil forbearers of mammalian tooth complexity that evolved in multiple non-mammalian Mesozoic lineages. Moreover, Priosphenodon with its herbivore-type dentition is as much a testimony to Mesozoic species diversification as it illustrates the distinct survival advantages of specialized and sophisticated jaws and teeth in competitive ecological environments. Unique Tooth Morphology and Prismatic Enamel in Late Cretaceous Sphenodontians from ArgentinaLeBlanc et al.Current BiologyMarch 26, 2020In BriefLeBlanc et al. describe the unique dentition of an extinct reptile Priosphenodon avelasi from the Cretaceous period of Argentina. Using histology and CT data, they describe its cone-in-cone dentition, where each tooth develops as a half-cone that anchors to a neighboring tooth. P. avelasi also evolved a tough, mammal-like enamel. 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• W3022134496 title "Evolution: Herbivore-Type Teeth in a Cretaceous Tuatara Relative" @default.
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