From Embryo to Adult: The Complete Development and Unusual Replacement of the Dentition of the Tammar Wallaby (Macropus eugenii)

Unlike their reptile-like ancestors with continuous tooth replacement, mammals have evolved to replace each tooth either only once, or not at all. In previous large-scale comparative studies, it has been suggested that this tooth replacement only occurs from a successional dental lamina produced lingually to the primary tooth. This study aims to document the complete tooth development and replacement pattern of the tammar wallaby (Macropus eugenii). The tammar wallaby is a diprotodont marsupial, a group defined by their two procumbent lower incisors. To provide a comprehensive documentation of the spatio-temporal pattern of tooth development, we used Lugol’s Iodine staining and microCT scanning (diceCT) of embryos and pouch young into adulthood, resulting in high resolution 3D models for both soft and mineralised stages of development for all tooth positions. Our results reveal that the eponymous lower incisors are the successional generation at the third incisor locus, where the primary dentition initiates but never erupts. Furthermore, we track the development of the only replacement tooth, the permanent third premolar (P3), from initiation to eruption, and found it develops from the primary dental lamina, mesial to the dP3. This is contrary to the conventional view of lingual replacement from successional lamina in mammals. Our findings indicate that no functional tooth replacement occurs in the tammar wallaby, and expands the diversity of tooth replacement patterns found in mammals. We also conclude that since almost all marsupial and placental mammals produce replacement teeth from the distalmost deciduous premolar, this tooth should be considered homologous in these two groups.

     

Dental fluctuating asymmetry in the Gullah: tests of hypotheses regarding developmental stability in deciduous vs. permanent and male vs. female teeth

In this investigation, deciduous teeth (canines, c; first molars, m1; second molars, m2) and their permanent successors (canines, C; first premolars, P1; second premolars, P2) were used to test two related hypotheses about fluctuating asymmetry (FA). First, based on the biology of the developing dentition, it was predicted that deciduous teeth would be more developmentally stable and thus exhibit less dimensional FA than their permanent successors. Second, based on sex differences in tooth development, it was predicted that female canines would have greater developmental stability (less FA) than male canines. Bucco-lingual measurements were made on dental casts from a single Gullah population. Using a repeated-measures study design (n = 3 repeated measures), we tested these hypotheses on sample sizes ranging from 63-82 antimeric pairs. Neither hypothesis was supported by our data. In most cases, Gullah deciduous teeth did not exhibit statistically significantly less FA than their permanent successors; indeed, statistically significant differences were found for only 3 of 12 deciduous vs. permanent contrasts, and in two cases, the deciduous tooth had greater FA. Female mandibular canines exhibited statistically significantly greater FA than those of males, while there was no statistically significant sex difference in FA for the maxillary canine. FA in these Gullah samples is high when compared to Archaic and late prehistoric Ohio Valley Native Americans, consistent with historical and archaeological evidence that environmental stress was relatively higher in the Gullah population. We suggest that when environmental stress in a population is high, the impact of differences in tooth formation time spans and developmental buffering upon FA may be minor relative to the effect of developmental noise.     

Incremental enamel development in modern human deciduous anterior teeth

This study reconstructs incremental enamel development for a sample of modern human deciduous mandibular (n = 42) and maxillary (n = 42) anterior (incisors and canines) teeth. Results are compared between anterior teeth, and with previous research for deciduous molars (Mahoney: Am J Phys Anthropol 144 (2011) 204-214) to identify developmental differences along the tooth row. Two hypotheses are tested: Retzius line periodicity will remain constant in teeth from the same jaw and range from 6 to 12 days among individuals, as in human permanent teeth; daily enamel secretion rates (DSRs) will not vary between deciduous teeth, as in some human permanent tooth types. A further aim is to search for links between deciduous incremental enamel development and the previously reported eruptionsequence. Retzius line periodicity in anterior teeth ranged between 5 and 6 days, but did not differ between an incisor and molar of one individual. Intradian line periodicity was 12 h. Mean cuspal DSRs varied slightly between equivalent regions along the tooth row. Mandibular incisors initiated enamel formation first, had the fastest mean DSRs, the greatest prenatal formation time, and based upon prior studies are the first deciduous tooth to erupt. Relatively rapid development in mandibular incisors in advance of early eruption may explain some of the variation in DSRs along the tooth row that cannot be explained by birth. Links between DSRs, enamel initiation times, and the deciduous eruption sequence are proposed. Anterior crown formation times presented here can contribute toward human infant age-at-death estimates. Regression equations for reconstructing formation time in worn incisors are given.     

Developmental origins and homologies of the hyracoid dentition

Understanding the origins of morphological specializations in mammals is a key goal in evolutionary biology. It can be accomplished by studying dental homology, which is at the core of most evolutionary and developmental studies. Here, we focused on the evolution and development of the specialized dentition of hyraxes for which dental homologies have long been debated, and could have implications on early placental evolution. Specifically, we analysed dental mineralization sequences of the three living genera of hyraxes and 17 fossil species using X‐ray computed microtomography. Our results point out the labile position of vestigial upper teeth on jaw bones in extant species, associated with the frequently unusual premolar shape of deciduous canines over 50 Ma of hyracoid evolution. We proposed two evolutionary and developmental hypotheses to explain these original hyracoid dental characteristics. (a) The presence of a vestigial teeth on the maxilla in front of a complex deciduous canine could be interpreted as extra‐teeth reminiscent of early placental evolution or sirenians, an order phylogenetically close to hyracoids and showing five premolars. (b) These vestigial teeth could also correspond to third incisors with a position unusually shifted on the maxilla, which could be explained by the dual developmental origin of these most posterior incisors and their degenerated condition. This integrative study allows discussion on the current evolutionary and developmental paradigms associated with the mammalian dentition. It also highlights the importance of nonmodel species to understand dental homologies.     

Homologies of the anterior teeth in Indriidae and a functional basis for dental reduction in primates

In a recent paper Schwartz ('74) proposes revised homologies of the deciduous and permanent teeth in living lemuriform primates of the family Indriidae. However, new evidence provided by the deciduous dentition ofAvahi suggests that the traditional interpretations are correct, specifically: (1) the lateral teeth in the dental scraper of Indriidae are homologous with the incisors of Lemuridae and Lorisidae, not the canines; (2) the dental formula for the lower deciduous teeth of indriids is 2.1.3; (3) the dental formula for the lower permanent teeth of indriids is 2.0.2.3; and (4) decrease in number of incisors during primate evolution was usually in the sequence I3, then I2, then I1. It appears that dental reduction during primate evolution occurred at the ends of integrated incisor and cheek tooth units to minimize disruption of their functional integrity.     

Innervation of the human upper primary dentition: Implications for understanding tooth initiation and rethinking growth and eruption patterns

Recent comparisons of humans with apes and early fossil hominids have prompted renewed interest in the study of sequences of dental growth and development. Such comparisons, however, rely on certain assumptions about tooth development and dental homology and the biological reality of distinguishing “deciduous” from “permanent” teeth. In light of earlier suggestions by Schwartz that there might be a correlation between nerves and the stem progenitors of tooth classes, and thus between nerve branch number and number of tooth classes, we studied a large sample of ～ 3 month fetuses to elucidate the nature of nerve branching patterns and the development of the primary dentition (i.e., the “deciduous” incisors, canine, and molars, and the first “permanent” molar). Contrary to expectation, variation in nerve branch patterning was the rule. If nerve fibers do have a role in tooth development, it can only be at the time of initiation, with definitive innervation occurring late in tooth development. In taking into consideration the entire span of tooth development—from initiation to innervation to eruption—and the process by which successional teeth arise (each from the external dental epithelium of a predecessor tooth), we suggest that dividing tooth growth and eruption into patterns of the “deciduous” teeth vs. those of the “permanent” is artificial and that a more meaningful approach would be the study of the entire dentition.     

Brief communication: enamel thickness trends in the dental arcade of humans and chimpanzees

In addition to evidence for bipedality in some fossil taxa, molar enamel thickness is among the few characters distinguishing (thick-enameled) hominins from the (thin-enameled) African apes. Despite the importance of enamel thickness in taxonomic discussions and a long history of scholarship, measurements of enamel thickness are performed almost exclusively on molars, with relatively few studies examining premolars and anterior teeth. This focus on molars has limited the scope of enamel thickness studies (i.e., there exist many fossil hominin incisors, canines, and premolars). Increasing the available sample of teeth from which to compare enamel thickness measurements from the fossil record could substantially increase our understanding of this aspect of dental biology, and perhaps facilitate greater taxonomic resolution of early hominin fossils. In this study, we report absolute and relative (size-scaled) enamel thickness measurements for the complete dentition of modern humans and chimpanzees. In accord with previous studies of molars, chimpanzees show lower relative enamel thickness at each tooth position, with little overlap between the two taxa. A significant trend of increasing enamel thickness from anterior to posterior teeth is apparent in both humans and chimpanzees, indicating that inter-taxon comparisons should be limited to the same tooth position in order to compare homologous structures. As nondestructive imaging techniques become commonplace (facilitating the examination of increasing numbers of fossil specimens), studies may maximize available samples by expanding beyond molars.     

Behavioral correlates of tooth eruption in Madagascar lemurs

Observations on the sequence and timing of gingival tooth eruption are reported for six species of Madagascar lemurs. Complete sequences of eruption were obtained for the deciduous dentition, and partial to complete sequences were recorded for the permanent dentition. In Cheirogaleus medius and in four species of the genus Lemur, the deciduous teeth erupt in front-to-back sequence, with the toothcomb emerging near birth as an integrated complex. In Propithecus verreauxi the same pattern is exhibited, but the small peglike lower canine and dp₃ erupt last. Eruption of the permanent dentition in Lemur species takes place in two distinct stages. In the first stage the upper incisors, toothcomb, and first two molars penetrate the gingiva. After an interval of 3 to 4 months, the remaining permanent teeth erupt. Deciduous premolars erupt when young animals are being weaned. The eruption of the deciduous toothcomb appears unrelated to feeding or grooming behavior. In L. catta and L. fulvus, the first stage of permanent tooth eruption occurs at approximately 6 months of age, when the growth rate slows down and (in wild populations) the rainy season is ending. This suggests that eruption of the anterior molars is timed to coincide with a shift from a more frugivorous to a more folivorous dietary regime, which occurs during the dry season. No further tooth eruption occurs until approximately 1 year of age, when the growth rate increases and the rainy season returns for wild populations. Thus, the second wave of permanent tooth eruption in these species again appears linked to changing climatic conditions which lead to a shift in dietary preferences.     

A new spalacolestine mammal from the Early Cretaceous Jehol Biota and implications for the morphology,phylogeny, and palaeobiology of Laurasian ‘symmetrodontans’

‘Symmetrodontans’ are extinct mammals characterized by having a reversed‐triangle molar pattern in which three main cusps define a triangular molar crown. This dental morpholgy has been regarded as being intermediate between the ‘triconodont’ tooth and the tribosphenic pattern characterizing therians; it is a key feature in taxonomy of Mesozoic mammals and one to understand mammalian evolution and palaeobiology. Here we report a new genus and species of ‘symmetrodontan’ mammal, Lactodens sheni, from the Early Cretaceous Jehol Biota, represented by a partial skeleton with dentary and upper and lower teeth with dental morphologies well‐preserved. The new species has a dental formula of three upper incisors, one canine, three premolars, and six molars/three lower incisors, one canine, five premolars and six lower molars, double‐rooted canines, extremely low‐crowned and transversely thin premolars, and acute angled molars. The dental morphologies of molars and peculiar deciduous premolars are similar to those of Spalacolestes from North America. The associated upper and lower dentitions from one individual animal helped to clarify tooth identification of some spalacotheriids represented only by fragmentary material. Phylogenetic analyses indicate a close relationship of the new species to North American spalacolestines and faunal interchanges between Eurasia and North America, thus supporting the notion that small‐bodied spalacotheriids were diverse and had a pan‐Laurasian distribution during the Early Cretaceous. Absence of the Meckelian groove suggests acquisition of the definitive mammalian middle ear in spalacolestines, and deciduous canines and premolars in the slim and extremely long dentary imply a faunivorous diet.     

The taming of the shrew milk teeth

SUMMARY A characteristic feature of mammalian dentition is the evolutionary reduction of tooth number and replacement. Because mice do not replace teeth, here we used Sorex araneus , the common shrew, as a model to investigate the loss of tooth replacement. Historically, shrews have been reported to initiate the development of several, milk or deciduous teeth but these soon become rudimentary and only the replacement teeth erupt. Shrews thus offer a living example of a derived mammalian pattern where the deciduous tooth development is being suppressed. Based on histological and gene expression analyses of serial sections, we suggest that S. araneus has discernible tooth replacement only in the premolar 4 (P4) position. Both generations of teeth express Shh in the enamel knot and in the inner enamel epithelium. Nevertheless, the deciduous P4 (dP4) is reduced in size during embryogenesis and is eventually lost without becoming functional. Analysis of growth shows that P4 replaces the dP4 in a "double-wedge" pattern indicative of competitive replacement where the suppression of the deciduous tooth coincides with the initiation of its replacement. Because activator–inhibitor mechanisms have been implicated in adjacent mouse molars and in transgenic mice with continuous tooth budding, we suggest that evolutionary suppression of deciduous teeth may involve early activation of replacement teeth, which in turn begin to suppress their deciduous predecessors.     

Premaxillary-maxillary suture asymmetry in a juvenile Gorilla. Implications for understanding dentofacial growth and development

A specimen of juvenile gorilla was found that had the premaxillary-maxillary suture coursing between the lateral deciduous incisor and deciduous canine on one side of the jaw, but between the central and lateral deciduous incisors on the other; in the latter, the suture also separates the alveolus of the lateral deciduous incisor from the crypt of the growing successional lateral incisor. Rather than dismiss this exception to the traditional dictum of tooth identification--which is based on the position to teeth relative to this suture--as some inconsequential anomaly, an attempt is made to understand how this can occur within the confines of present understanding of dentofacial growth and development and developmental theory. An hypothesis relating tooth and tooth class identification is presented in the context of ectomesenchymally predifferentiated stem progenitors and subsequent tooth class proliferation.     

Changes in the Distribution of Periodontal Nerve Fibers during Dentition Transition in the Cat

The periodontal ligament has a rich sensory nerve supply which originates from the trigeminal ganglion and trigeminal mesencephalic nucleus. Although various types of mechanoreceptors have been reported in the periodontal ligament, the Ruffini ending is an essential one. It is unknown whether the distribution of periodontal nerve fibers in deciduous teeth is identical to that in permanent teeth or not. Moreover, morphological changes in the distribution of periodontal nerve fibers during resorption of deciduous teeth and eruption of successional permanent teeth in diphyodont animals have not been reported in detail. Therefore, in this study, we examined changes in the distribution of periodontal nerve fibers in the cat during changes in dentition (i.e., deciduous, mixed and permanent dentition) by immunohistochemistry of protein gene product 9.5. During deciduous dentition, periodontal nerve fibers were concentrated at the apical portion, and sparsely distributed in the periodontal ligament of deciduous molars. During mixed dentition, the periodontal nerve fibers of deciduous molars showed degenerative profiles during resorption. In permanent dentition, the periodontal nerve fibers of permanent premolars, the successors of deciduous molars, increased in number. Similar to permanent premolars, the periodontal nerve fibers of permanent molars, having no predecessors, increased in number, and were densely present in the apical portion. The present results indicate that the distribution of periodontal nerve fibers in deciduous dentition is almost identical to that in permanent dentition although the number of periodontal nerve fibers in deciduous dentition was low. The sparse distribution of periodontal nerve fibers in deciduous dentition agrees with clinical evidence that children are less sensitive to tooth stimulation than adults.     

Frugivorous and animalivorous bats (Microchiroptera): dental and cranial adaptations

The most derived fruit-eating bats have small canines, wide palates and molars with a distinctive labial rim. Paracone and metacone have moved from a dilambdodont position in the middle of the tooth to the labial side of the tooth where they form the labial cutting edge. Along with the well-developed and close fitting labial cutting edges of the premolars and canines, this cutting edge skirts nearly the entire perimeter of the palate. The labial rim of the lower teeth fit inside the labial rim of the upper teeth like two cookie cutters nesting one inside the other. Frugivores have a greater allocation of tooth area at the anterior end of the toothrow, while animalivorous species have more at the posterior end of the toothrow. The area occupied by canines of predators of struggling prey is greater than that for bats that eat non-struggling prey like fruit. In addition, frugivores have wider palates than long while many carnivores have longer palates than wide. Omnivores appear to have a more equal allocation of space to more kinds of teeth, particularly the incisors and non-molariform premolars, on the toothrow than do frugivores or animalivores. The mechanical nature of different food items is discussed and the suggestion made that describing foods in terms of their texture may be more important in tooth design than whether they are fruit or insect or vertebrate.     

How do genes make teeth to order through development?

This introduction to new patterning theories for the vertebrate dentition outlines the historical concepts to explain graded sequences in tooth shape in mammals (incisors, canines, premolars, molars) which change in evolution in a linked manner, constant for each region. The classic developmental models for shape regulation, known as the 'regional field' and 'dental clone' models, were inspired by the human dentition, where it is known that the last tooth in each series is the one commonly absent. The mouse, as a valuable experimental model, has provided data to test these models and more recently, based on spatial-temporal gene expression data, the 'dental homeobox code' was proposed to specify regions and regulate tooth shape. We have attempted to combine these hypotheses in a new model of the combinatorial homeobox gene expression pattern with the clone and field theories in one of 'co-operative genetic interaction'. This also explains the genetic absence of teeth in humans ascribed to point mutations in mesenchymally expressed genes, which affect tooth number in each series.     

Size and placement of developing anterior teeth in immature Neanderthal mandibles from Dederiyeh Cave,Syria: Implications for emergence of the modern human chin

Evolutionary and functional significance of the human chin has long been explored from various perspectives including masticatory biomechanics, speech, and anterior tooth size. Recent ontogenetic studies have indicated that the spatial position of internally forming anterior teeth partially constrains adult mandibular symphyseal morphology. The present study therefore preliminarily examined the size and placement of developing anterior teeth in immature Neanderthal mandibles of Dederiyeh 1 and 2, compared with similarly‐aged modern humans (N = 16) and chimpanzees (N = 7) whose incisors are comparatively small and large among extant hominids, respectively. The Dederiyeh 1 mandible is described as slightly presenting a mental trigone and attendant mental fossa, whereas Dederiyeh 2 completely lacks such chin‐associated configurations. Results showed that, despite symphyseal size being within the modern human range, both Dederiyeh mandibles accommodated overall larger anterior dentition and displayed a remarkably wide bicanine space compared to those of modern humans. Dederiyeh 2 had comparatively thicker deciduous incisor roots and more enlarged permanent incisor crypts than Dederiyeh 1, but both Dederiyeh individuals exhibited a total dental size mostly intermediate between modern humans and chimpanzees. These findings potentially imply that the large deciduous/permanent incisors collectively distended the labial alveolar bone, obscuring an incipient mental trigone. It is therefore hypothesized that the appearance of chin‐associated features, particularly of the mental trigone and fossa, can be accounted for partly by developmental relationships between the sizes of the available mandibular space and anterior teeth. This hypothesis must be, however, further addressed with more referential samples in future studies. Am J Phys Anthropol 156:482–488, 2015. © 2014 Wiley Periodicals, Inc.     

Enamel hypoplasias as indicators of developmental stress in pongids and hominids

This paper reports the results from a study of enamel hypoplasia in the deciduous dentition of free-living Liberian chimpanzees (Pan troglodytes verus). The entire study collection includes 280 specimens (278 skulls plus two unassociated mandibles), of which 70 are young enough to retain some decidous teeth. Among the subsample of infants, the total frequency of hypoplasia summed over all teeth in any individual reaches 80%, being expressed in the form of pits rather than transverse lines. Hypoplasia of a linear form was common in the permanent dentition, attaining a frequency of 46.7% on maxillary central incisors and 69.7% on mandibular canines.     

Dental formulae and dental eruption patterns in Parapithecidae (Primates, Anthropoidea)

The eruption sequence for the lower teeth of Apidium phiomense based on 18 juvenile specimens is dP3, dP4, M1, M2, P2, P4, (P3, M3), C. Only five specimens of Parapithecus grangeri show developing lower teeth. P2, M1, and M2 all erupted before P3 and P4; C and M3 were the last cheek teeth to erupt. Late eruption of the lower canines in parapithecids is a possible shared derived resemblance linking these species with Anthropoidea and Adapidae and distinguishing both from Omomyidae, Tarsiidae, and tooth-combed lemurs. Late eruption of M3 in parapithecids is a shared derived resemblance with Anthropoidea alone. The lower dental formula of Apidium phiomense is confirmed as 2 X 1 X 3 X 3 by additional specimens which show the incisors. Based in part on tooth socket counts, the deciduous lower dental formula was 2 X 1 X 3. New specimens of Parapithecus grangeri now demonstrate an adult mandibular dental formula of 0 X 1 X 3 X 3 (not 2 X 1 X 3 X 3 as previously thought) and a juvenile formula of 1 X 1 X 3. The number of incisors possessed by Parapithecus fraasi is again open to debate. Material is insufficient to judge whether this species had a pair of incisors in each lower jaw quadrant, by analogy with Apidium, or had undergone reduction to just one incisor. In any event, the presence of two incisors in another parapithecid Apidium shows anterior tooth reduction of Parapithecus grangeri occurred independent of, and should not be considered a shared derived similarity with, Tarsiidae, as was once thought.     

The deciduous dentition and dental replacement in the Eocene bat Palaeochiropteryx tupaiodon from Messel: The primitive condition and beginning of specialization of milk teeth among Chiroptera

The deciduous dentition and tooth replacement pattern of Palaeochiropteryx tupaiodon from the early Middle Eocene of Messel, near Frankfurt, Germany, are described. Ontogenetic states include fetuses to subadults. The posterior portion of the deciduous dentition (dP3-4) still shows the primitive eutherian condition of molarization, while the anterior part (dI-dC) was already engaged in the evolution of the highly derived condition found in living bats for clinging to the mother's fur. A styliform and sharp anterior dentition is considered a prerequisite in earliest chiropteran evolution. The greatly modified milk teeth of all living bats developed in different clades by parallel evolution under high selective pressure. The tiny and, at initial stages, poorly calcified teeth are substantiated by a newly developed microradiographic technique which is described in detail.     

Traumatic injury to the incisive bones and maxillary dentition in a male gray wolf (Canis lupus L.) from Slovakia

The paper presents the skull of a male gray wolf shot in the region of Snina, eastern Slovakia. Age at death of the wolf was estimated at 6 years. The skull was characterized by the almost-complete absence of the alveolar processes of the incisive bones and multiple dental abnormalities that were attributed to a severe trauma. All maxillary incisors and both maxillary first premolars were missing. In addition, both maxillary canines were fractured with only tooth fragments being left. The pulp exposure associated with the crown fractures of the maxillary canines had caused pulp necrosis and periapical lesions, as evidenced on radiographs. The right P², P³, and P⁴ were fractured, with only the remaining tooth structure of the second and third premolars being left. In the right P⁴ and the left M¹, periapical bone resorption was diagnosed radiologically. In the mandibular dentition, the right I₂ and left P₁ had been lost in life. The mandibular canines exhibited distinct wear facets that were caused by contact with the maxillary third incisors, which were subsequently lost. The fact that all fractured teeth showed signs of wear indicates that the trauma had occurred some time before the wolf was shot.     

MANDIBULAR DENTAL ONTOGENY OF RINGED SEALS (PHOCA HISPIDA)

X-rays of mandibles from ringed seal fetuses ( n = 15), newborns ( n = 12), and young-of-the-year ( n = 11), collected up to early June, were examined for the presence, location, and eruption patterns of deciduous and permanent teeth. The presence of a neonatal line and cementum in permanent canines was determined microscopically. Fetuses sampled in October-November had only unerupted, deciduous tooth germs, but by late January there were robust, deciduous teeth at il-2 pc2-4 and small permanent teeth at 11-2 Cl PCl-5. In newborns collected in early April, 109 of 143 (76%) deciduous teeth were resorbed completely. The remaining 34 deciduous teeth were partially resorbed; six (18%) had erupted and likely would be shed. By late April young-of-the-year had no deciduous teeth remaining. In newborns 54% of the permanent teeth (102/188) were erupted < 2 mm, and by late May the permanent dentition was erupted fully. The neonatal line first appeared in the canine teeth of young-of-the-year collected in mid-April and was 100% present after early May. There was no cementum apparent on any canine collected up to early June. Two seals were missing one and two permanent incisors, respectively. No supernumerary teeth or morphological variants were observed.