Continuous dental replacement in a hyper-chisel tooth digging rodent a,1 a b c d Helder Gomes Rodrigues , Pauline Marangoni , Radim Sumbera , Paul Tafforeau , Wim Wendelen , and Laurent Viriota,1 aTeam “Evo-Devo of Vertebrate Dentition,” Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Unité Mixte de Recherche 5242, Centre National de la Recherche Scientifique, Université Claude Bernard de Lyon 1, Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 07, France; bDepartment of Zoology, Faculty of Science, University of South Bohemia, Ceské Budejovice 37005, Czech Republic; cEuropean Synchrotron Radiation Facility, 38043 Grenoble Cedex, France; and dVertebrate Section, Zoology Department, Royal Museum for Central Africa, B-3080 Tervuren, Belgium Edited by David B. Wake, University of California, Berkeley, CA, and approved September 8, 2011 (received for review June 15, 2011) Contrary to their reptilian ancestors, which had numerous dental mechanisms leading to CDR, notably the occurrence of super- generations, mammals are known to usually develop only two numerary teeth in mammals (8, 9), remain to be determined. generations of teeth. However, a few mammal species have Here we report a case of CDR in a subterranean rodent, the acquired the ability to continuously replace their dentition by silvery mole-rat Heliophobius argenteocinereus, belonging to Af- the constant addition of supernumerary teeth moving secondarily rican mole-rats (Bathyergidae, Rodentia), which could signifi- toward the front of the jaw. The resulting treadmill-like replace- cantly contribute to the understanding of this rare phenomenon. ment is thus horizontal, and differs completely from the vertical The dental peculiarities of this species further underscore the dental succession of other mammals and their extinct relatives. De- interest of African mole-rats as models for examining topical spite the developmental implications and prospects regarding the issues, such as “eusociality” (10, 11), extreme longevity (12), and origin of supernumerary teeth, this striking innovation remains cancer resistance (13). We investigated Heliophobius dentition poorly documented. Here we report another case of continuous compared with Trichechus, P. concinna, and another African dental replacement in an African rodent, Heliophobius argenteo- mole-rat (the Cape mole-rat, Georychus capensis) to appraise the cinereus, which combines this dental system with the progressive main dental characteristics of this rodent on the one hand and to eruption of high-crowned teeth. The escalator-like mechanism of identify the specific traits relevant to improved knowledge of the EVOLUTION Heliophobius constitutes an original adaptation to hyper-chisel CDR mechanism on the other. tooth digging involving high dental wear. Comparisons between Heliophobius and the few mammals that convergently acquired Results and Discussion continuous dental replacement reveal that shared inherited traits, Original System of Dental Replacement Among Mammals Combining including dental mesial drift, delayed eruption, and supernumerary Hypsodonty and Continuous Dental Replacement. Heliophobius dis- molars, comprise essential prerequisites to setting up this dental plays four to seven cheek teeth (Fig. 1 A–C and Tables S1 and mechanism. Interestingly, these dental traits are present to a lesser S2), whereas the maximum cheek tooth number per dental extent in humans but are absent in mouse, the usual biological quadrant does not usually exceed five in rodents and four in model. Consequently, Heliophobius represents a suitable model African mole-rats. It is thus the only known rodent displaying so to investigate the molecular processes leading to the development many supernumerary cheek teeth. Although its abnormal tooth of supernumerary teeth in mammals, and the accurate description number has previously been reported (14), the underlying dental fi of these processes could be a signi cant advance for further appli- mechanism has never been properly interpreted. Heliophobius cations in humans, such as the regeneration of dental tissues. has single-rooted and bilophate hypsodont teeth. Tooth occlusal surfaces rapidly become flat and undergo a series of shape mole-rats | intensive burrowing activity | hypsodonty | abrasion | attrition transformations, finally resulting in upper heart-shaped and lower pear-shaped teeth (Fig. 1 A–C) that lack enamel to varying ost nonmammalian vertebrates continuously replace their degrees and are covered by cementum. Morphometric compar- Mdentition, entailing many generations of identical teeth. In isons between occlusal crown shapes observed from rear to front contrast, mammals develop a limited dentition composed at and virtual transverse slices of an erupting tooth belonging to the most of two generations of heteromorphous teeth, decreasing in same row lead to the conclusion that the various crown shapes number but generally increasing in shape complexity during result from an increasing degree of dental wear (Fig. 1D). All evolution (1, 2). This has contributed to the acquisition of a more teeth have an overall identical cone-like shape and only their efficient masticatory apparatus than reptile jaws (3) that allowed relative size is susceptible to change during life. We cannot say mammals to diversify their feeding habits (4) and to include whether the first erupting tooth is a premolar (Fig. S1), as in tough and abrasive plants in their diets. To withstand abrasive most African mole-rats, but all subsequent teeth are molars. intakes, many mammals acquired a more durable dentition by Most specimens of Heliophobius show either one erupting or way of diverse evolutionary trends (5). The most frequently ob- freshly erupted molar behind the functional tooth row. After served is the increase in tooth height (i.e., hypsodonty), which eruption, each tooth drifts from rear to front. Evidence of hor- leads in extreme cases to ever-growing teeth. Another trend to izontal movements is demonstrated by continual remodeling of improve durability is continuous dental replacement (CDR), an extremely rare phenomenon in mammals. CDR corresponds to a progressive replacement of the dentition by regular develop- Author contributions: W.W. and L.V. designed research; H.G.R., P.M., and P.T. performed research; H.G.R. and P.M. analyzed data; and H.G.R., P.M., R.S., P.T., W.W., and L.V. wrote ment of additional teeth, which move from the rear to the front the paper. ’ of the jaw throughout the animal s life. Among the ca. 5,500 The authors declare no conflict of interest. species of mammals, only the three manatee species (Trichechus, This article is a PNAS Direct Submission. Sirenia) and the pygmy-rock wallaby (Petrogale concinna, Mac- 1To whom correspondence may be addressed. E-mail: helder.gomes.rodrigues@ens-lyon. ropodiformes) are known to display this striking innovation (6, 7). fr or [email protected]. To date, this mechanism appears poorly documented. Further- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. more, the genetic etiology and the developmental and molecular 1073/pnas.1109615108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1109615108 PNAS Early Edition | 1of5 Downloaded by guest on September 27, 2021 are pushed out from the row alignment before being completely resorbed inside the bone (Figs. 1C and 2C). Because the molar progression is not synchronized between each quadrant, asym- metric dental rows occur (Fig. 1 A and B), as do rare cases of misalignment (Fig. S2B). Teeth also continue to grow and erupt vertically while moving to the front (Fig. 2 A and D). The orig- inality of the Heliophobius dental system relies on the superim- position of CDR over preexisting hypsodonty resulting in an escalator-like movement of teeth, constantly compensating for intensive dental wear. This dental replacement is not observed in other bathyergid rodents. Among other mammals, elephants present an analogous dental replacement, but their regular dentition develops sequentially, without the occurrence of any supplementary teeth. Unlike Heliophobius, Trichechus and P. concinna have low- crowned and bi- or trirooted cheek teeth but are bilophodont as well (Fig. 3 A and B). The replacement of their jugal dentition works like a simple treadmill in which each freshly developed molar erupts vertically at the rear of the row and then migrates horizontally toward the front (Fig. 3 C–F). A part of the regular dentition, including premolars (Fig. 3D), clearly develops before Fig. 1. Dental characteristics of H. argenteocinereus (RMCA96.036-M-5467). the system changes course, such that a single molar could be- (A) X-ray synchrotron microtomographic 3D rendering of upper jugal tooth come regularly ever-duplicated. Such an assumption relies on rows. (B) X-ray synchrotron microtomographic 3D rendering of lower jugal the fact that additional molars are identical to the second molars tooth rows. (C) Virtual cross-section of upper jugal tooth rows from syn- fi chrotron microtomographic data. (D) Morphological correspondences be- in manatees (6). The distal root is rst intensively resorbed, and tween virtual transverse slices of erupting lower molar and dental wear the crown breaks away from the mesial root when the tooth stages observed from the rear to front of the lower tooth row. D → M, distal- reaches the front of the row (Fig. 3 C–F). Even if the crown is to-mesial point. severely eroded during the drift, it is not resorbed and vertical readjustments