Phylogenetic memory of developing mammalian dentition

Structures suppressed during evolution can be retraced due to atavisms and vestiges. Atavism is an exceptional emergence of an ancestral form in a living individual. In contrast, ancestral vestige regularly occurs in all members of an actual species. We surveyed data about the vestigial and atavistic teeth in mammals, updated them by recent findings in mouse and human embryos, and discussed their ontogenetic and evolutionary implications. In the mouse incisor and diastema regions, dental placodes are transiently distinct being morphologically similar to the early tooth primordia in reptiles. Two large vestigial buds emerge in front of the prospective first molar and presumably correspond to the premolars eliminated during mouse evolution. The incorporation of the posterior premolar vestige into the lower first molar illustrates the putative mechanism of evolutionary disappearance of the last premolar in the mice. In mutant mice, devious development of the ancestral tooth primordia might lead to their revivification and origin of atavistic supernumerary teeth. Similarity in the developmental schedule between three molars in mice and the respective third and fourth deciduous premolar and the first molar in humans raises a question about putative homology of these teeth. The complex patterning of the vestibular and dental epithelium in human embryos is reminiscent of the pattern of "Zahnreihen" in lower vertebrates. A hypothesis was presented about the developmental relationship between the structures at the external aspect of the dentition in mammals (oral vestibule, pre-lacteal teeth, paramolar cusps/teeth), the tooth glands in reptiles, and the earliest teeth in lower vertebrates.     

Heterochrony in the development of vestigial and functional deciduous incisors in rabbits (Oryctolagus cuniculus L.)

Foetal and postnatal development of vestigial and functional deciduous incisors was reexamined using routine serial histological sections of maxillae and mandibles at daily intervals from day 16 postconception to postnatal day 15. It was found that the development of the maxillary and mandibular vestigial incisor teeth was more rapid than that of the functional incisors and that, of the functional incisors, the maxillary posterior deciduous incisors were the slowest to develop. It appeared from this study that a basic morphogenetic requirement for unfolding structure, ie, developmental timing, was not critical in generating hypsodont or brachydont teeth. A proposition has been made that originally juvenile stages of odontogenesis represent a continuously growing system, which during evolution has successively become typical for adult descendants.     

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.     

Ontogeny and homology of the dentition in dasyurid marsupials: Development inSminthopsis virginiae

Histological analysis of an ontogenetic series of the dasyurid marsupial,Sminthopsis virginiae, from birt to 60 days old, was undertaken to assess the developmental homologies of the deciduous and successional teeth. This period covers the time from the initiation of all teeth as epithelial buds up until the time of early eruption of some teeth. In addition, two older specimens, aged 81 and 97 days, were examined to provide additional information on the state of differentiation of the unerupted third premolar. In the postcanine dentition, only a single tooth position, dP3, was characterized by the later development of a replacing successional tooth (P3), following developmental pathways identical to those in eutherian mammals. In contrast, the anterior dentition is characterized by the formation of rudimentary, nonerupting deciduous incisors and canines, and by the accelerated development of normal, erupting successional incisors and canines in both jaws. Comparison of relative developmental stages for each tooth position throughout its preeruptive ontogeny suggests thatheterochrony (both developmental acceleration and retardation) has played an important role in the evolutionary history of the dasyurid dentition. Differing aspects of this phenomenon are identified and discussed for the anterior dentition, the anterior two premolars, P3, and the lower molars. Further evidence is presented to corroborate the identification of the anterior two premolars in the adult as dP1 and dP2, based on the relative retardation of their initiation and their lack of successor tooth germs. This developmental heterochrony has probably occurred in all three-premolared marsupials.     

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.     

Dentition development and budding morphogenesis

The development of functional teeth in the mouse has been widely used as a model to study general mechanisms of organogenesis. Compared with other mammals, in which three incisors, one canine, four premolars, and three molars may occur even in each dental quadrant, the mouse functional dentition is strongly reduced. It comprises only one incisor separated from three molars by a toothless gap diastema at the location of the missing teeth. However, mouse embryos also develop transient vestigial dental primordia between the incisor and molar germs in both the upper and lower jaws. These rudimental structures regress, and epithelial apoptosis is involved in this process. The existence of the vestigial dental structures allowed a better assessment of the periodicity in the mouse dentition, which extends opportunities for the interpretation of molecular data on tooth development. We compared the dentition development with tentative models of budding morphogenesis in other epithelial appendages lungs and feathers. We suggested how developmental control by signaling molecules, including bone morphogenetic protein (Bmp), sonic hedgehog (Shh), and fibroblast growth factor (Fgf), can be similarly involved during budding morphogenesis of dentition and other epithelial appendages. We propose that epithelial apoptosis plays an important role in achieving specific features of dentition, whose development involves both budding and its more complex variant branching. The failure of segregation of the originating buds supports the participation of the concrescence of several tooth primordia in the evolutionary differentiation of mammalian teeth.     

Dental developmental pattern of the Neanderthal child from Roc de Marsal: a high-resolution 3D analysis

The assessment of the degree of similarity or difference between Neanderthals and modern humans in their patterns of dental development remains a controversial matter. Here we report results from the microtomographic-based (SR-μCT) high-resolution structural investigation of the maxilla and mandible of the Neanderthal child from Roc de Marsal, Dordogne, France (likely from OIS 5a). Following their virtual extraction and 3D rendering, we assessed the maturational stage of each of the 41 dental elements (20 deciduous and 21 permanent) forming its mixed dentition. By using a Bayesian approach, we calculated the probability that its deciduous and permanent mandibular sequences are found within the extant human variation as illustrated by a tomographic CT-based sub-sample of 32 children (deciduous dentition) and a panoramic radiographic- and CT-based whole sample of 343 living children (permanent dentition). Results show that neither the deciduous nor the permanent mandibular sequences displayed by Roc de Marsal are precisely found within our modern comparative files. In both sequences, the most influential factor is represented by a slight discrepancy in the Neanderthal child between the stage of mineralization of the first molar, which is proportionally advanced, and the maturational level reached by its incisors, which are proportionally delayed. Following a quantitative volumetric analysis of the deciduous teeth, we suggest that this characteristic may be related to differences between Neanderthals and modern humans in absolute dental size and relative size proportions between front and cheek teeth, as well as to structural differences in dental tissue proportions.     

Pattern and pace of dental eruption in Tarsius

This article uses data on the dental eruption pattern and life history of Tarsius to test the utility of Schultz's rule. Schultz's rule claims a relationship between the relative pattern of eruption and the absolute pace of dental development and life history and may be useful in reconstructing life histories in extinct primates. Here, we document an unusual eruption pattern in Tarsius combining early eruption (relative to molars) of anterior replacement teeth (P2 and incisors) and relatively late eruption of the posterior replacement teeth (C, P3, and P4). This eruption pattern does not accurately predict the "slow" pace of life documented for Tarsius [Roberts: Int J Primatol 15 (1994) 1-28], nor aspects of life history directly associated with dental development as would be expected using Schultz's rule. In Tarsius, the anterior teeth and M1 erupt at an early age and therefore are not only fast in a relative sense but also fast in an absolute sense. This seems to be related to a developmental anomaly in the deciduous precursor teeth, which are essentially skipped. This decoupling among dental eruption pattern, dental eruption pace, and life history pace in Tarsius undermines the assumptions that life histories can accurately be described as "fast" or "slow" and that dental eruption pattern alone can be used to infer overall life history pace. The relatively and absolutely early eruption of the anterior dentition may be due to the utility of these front teeth in early food acquisition rather than with the pace of life history.     

Homologies of the anterior teeth in indriidae

Schwartz ('74) proposed revised homologies of the deciduous and permanent anterior teeth in living lemuriform primates of the family Indriidae. Gingerich ('77) described a juvenile specimen of Avahi and emphasized the importance of functional integrity in controlling the pattern of dental reduction in primates, neither of which supports Schwartz's interpretation. Schwartz ('78) recently reiterated his position without adequately discussing the Avahi evidence and the functional basis that probably controls dental reduction. Avahi has a deciduous dentition intermediate in morphology between that of Lemuridae and Indriidae, and similar to both. Thus the lower deciduous dental formula of Indriidae is probably 2.1.3, which is the typical and maximum deciduous complement known in living and fossil lemuriform primates. The formula of the lower permanent dentition in Indriidae is thus 2.0.2.3.     

Formation of anterior maxillary teeth in 0-3-year-old children with cleft lip and palate and prenatal risk factors for delayed development

Formation of deciduous and permanent maxillary incisors and canines was studied in 361 children with cleft lip and palate. Altogether, 704 occlusal X rays of the children aged from 2 weeks to 41 months were assessed using a 13-stage scale. The early timing of tooth development was in both dentitions close to that reported for healthy children. However, developmental asymmetry was noted between contralateral teeth on the cleft and noncleft sides. In the unilateral cleft lip and palate group, every tenth cleft-side deciduous central incisor, deciduous canine, and permanent central incisor was delayed compared to the corresponding contralateral tooth. The formation timing was also compared within 11 prenatal and hereditary variables. Risk factors for delayed development were low placental weight, short gestation, mother's use of drugs during pregnancy, first in birth order, cleft with multiple additional malformations, and relatives having malformations other than oral clefts. However, the associations between a risk factor and tooth development were weak.     

Evolutionary and developmental dynamics of the dentition in Muroidea and Dipodoidea (Rodentia, Mammalia)

SUMMARY When it comes to mouse evo‐devo, the fourth premolar–first molar (P4–M1) dental complex becomes a source of longstanding controversies among paleontologists and biologists. Muroidea possess only molar teeth but with additional mesial cusps on their M1. Developmental studies tend to demonstrate that the formation of such mesial cusps could result from the integration of a P4 germ into M1 during odontogenesis. Conversely, most Dipodoidea conserve their fourth upper premolars and those that lost these teeth can also bear additional mesial cusps on their first upper molars. The aim of this study is to assess this developmental model in both Muroidea and Dipodoidea by documenting the morphological evolution of the P4–M1 complex across 50 Ma. Fourteen extinct and extant species, including abnormal and mutant specimens were investigated. We found that, even if their dental evolutionary pathways strongly differ, Dipodoidea and Muroidea retain common developmental characteristics because some of them can present similar dental morphological trends. It also appears that the acquisition of a mesial cusp on M1 is independent from the loss of P4 in both superfamilies. Actually, the progressive decrease of the inhibitory effect of P4, consequent to its regression, could allow the M1 to lengthen and mesial cusps to grow in Muroidea. Apart from these developmental explanations, patternings of the mesial part of first molars are also deeply constrained by morpho‐functional requirements. As there is no obvious evidence of such mechanisms in Dipodoidea given their more variable dental morphologies, further developmental investigations are needed.     

Toothcomb homology and toothcomb function in extant strepsirhines

Contrary to some recent assertions, there are no persuasive ways for determining the homologies of indriid toothcomb teeth and the resulting dental formulas. Most of the presumably distinctive features of procumbent “canines” are also seen in incisors, and vice versa. Thus, there are at least three plausible dental formulas for indriid deciduous teeth and two for the permanent dentition. All formulas are compatible with the distribution of teeth in fossil strepsirhines. Similar arguments apply to strepsirhine toothcombs as a whole, but the absence of three-incisored ancestors in the fossil record strongly supports the conclusion that the dental formula of nonindriids is 2.1.3.3. for the lower dentition. There are also alternative interpretations of the original function of the toothcomb. Recent arguments which purport to demonstrate that the toothcomb evolved originally as a sap-feeding adaptation fail that purpose. The ontogeny of infant lemur behavior suggests that the original function involved grooming rather than feeding if the data are interpreted in a Haeckelian context.     

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.     

The study of animal bones from archaeological sites. By Raymond E. Chaplin. ix + 170 pp., figures,tables, bibliography,index. Seminar press,London. 1971. $5.75 (cloth)

A review of the literature reveals a long history of disagreement on the interpretation of the lower deciduous and permanent dentition of the Indriidae. This disagreement has centered on the existence and/or replacement of a canine as a member of the indriid toothcomb. The presence of a pair of canines in the toothcomb of lemurids and lorisids has rarely been questioned, and there is no evidence to indicate that this interpretation is incorrect. There has, however, been no consistency nor substantiating evidence presented for any interpretation of the indriid toothcomb. By comparing the morphology of the teeth of the lemurid, lorisid, and indriid toothcomb, both deciduous and permanent, comparing the mode of dental development in these three families, identifying the indriid lower deciduous dentition, and by relating the data to an ontogenetic and phylogenetic framework, this study proposes: (1) in all three families, the lateral teeth of the toothcomb are canines, (2) the dental formula for the lower deciduous teeth of indriids is 1.1.4, (3) the dental formula for the lower permanent teeth of indriids is 1.1.2.3, and (4) that decrease in number of incisors during primate evolution was most likely I1 to I2 to I3.     

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.     

A discussion of dental homology with reference to primates

The inconsistencies which exist when the traditional tooth-to-bony-landmark/tooth-to-occlusal-relationship criteria of identification of teeth are maintained are discussed. It is pointed out how these (e.g., "the canine is the tooth behind the premaxillary-maxillary suture") can be falsified. It is also suggested that some mammals, including Tarsius and Homo sapiens, develop homologies of three sets of "teeth," and that the "adult" antemolar dentition of a mammal may be composed of retained deciduous teeth as well as permanent teeth. Following a revision of dental homologies in most primates, an approach to reevaluating dental homologies is proposed, and a model of tooth "loss" presented.     

Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions

Functional dental theory predicts that tooth shape responds evolutionarily to the mechanical properties of food. Most studies of mammalian teeth have focused on qualitative measures of dental anatomy and have not formally tested how the functional components of teeth adapt in response to diet. Here we generated a series of predictions for tooth morphology based on biomechanical models of food processing. We used murine rodents (Old World rats and mice) to test these predictions for the relationship between diet and morphology and to identify a suite of functional dental characteristics that best predict diets. One hundred and five dental characteristics were extracted from images of the upper and lower tooth rows and incisors for 98 species. After accounting for phylogenetic relationships, we showed that species evolving plant‐dominated diets evolved deeper incisors, longer third molars, longer molar crests, blunter posteriorly angled cusps, and more expanded laterally oriented occlusal cusps than species adapting to animal‐dominated diets. Measures of incisor depth, crest length, cusp angle and sharpness, occlusal cusp orientation, and the lengths of third molars proved the best predictors of dietary adaptation. Accounting for evolutionary history in a phylogenetic discriminant function analysis notably improved the classification accuracy. Molar morphology is strongly correlated with diet and we suggest that these dental traits can be used to infer diet with good accuracy for both extinct and extant murine species.     

Deciduous dental morphology and the biological affinities of a late Chalcolithic skeletal series from western India

Morphological variations of the dental crown and roots provide valuable data for determining the genetic affinities and evolutionary adaptedness of prehistoric human skeletal populations. This paper documents morphological variations of a sample of deciduous teeth from the late Chalcolithic farming village of Inamgaon (1600-700 B.C.) in western India. Hanihara's (1963) grading system of deciduous dental traits was employed in assessing the degree of expression of shovel-shape of incisors, cusp number of upper and lower first molars, hypocone variation, Carabelli's trait, cusp number of lower second molars and the protostylid. Turner's (1970) classification was used to determine presence and size of accessory cusps: entoconulid (C-6) and metaconulid (C-7). Comparative evaluation of the Inamgaon deciduous dental data is hampered by the absence of data for dental features of living and prehistoric South Asian populations. Many of the traits observed in the Inamgaon series exhibit a frequency of occurrence intermediate between figures characteristic of the "Mongoloid" dental complex and the "Caucasoid" dental complex.     

Developmental palaeontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives

The study of fossilized ontogenies in mammals is mostly restricted to postnatal and late stages of growth, but nevertheless can deliver great insights into life history and evolutionary mechanisms affecting all aspects of development. Fossils provide evidence of developmental plasticity determined by ecological factors, as when allometric relations are modified in species which invaded a new space with a very different selection regime. This is the case of dwarfing and gigantism evolution in islands. Skeletochronological studies are restricted to the examination of growth marks mostly in the cement and dentine of teeth and can provide absolute age estimates. These, together with dental replacement data considered in a phylogenetic context, provide life-history information such as maturation time and longevity. Palaeohistology and dental replacement data document the more or less gradual but also convergent evolution of mammalian growth features during early synapsid evolution. Adult phenotypes of extinct mammals can inform developmental processes by showing a combination of features or levels of integration unrecorded in living species. Some adult features such as vertebral number, easily recorded in fossils, provide indirect information about somitogenesis and hox-gene expression boundaries. Developmental palaeontology is relevant for the discourse of ecological developmental biology, an area of research where features of growth and variation are fundamental and accessible among fossil mammals.     

The anatomy and systematic position of the early Miocene proconsulid from Meswa Bridge, Kenya

A small collection of fossil catarrhines was recovered from the early Miocene locality of Meswa Bridge in western Kenya between 1978 and 1980. The associated fauna from Meswa Bridge indicates an age older than 20 Ma. Much of the material has been briefly described previously, and its taxonomic status considered. The material can be assigned to a minimum of four individuals, all of which are infants or juveniles. Although the specimens were shown to belong to a distinct species of Proconsul, the taxon was not named, primarily because many of the specimens belonged to immature individuals. Nevertheless, the combined morphological features of the deciduous and permanent teeth allow the diagnosis of a new species of Proconsul, which is formally named here as P. meswae. It is a large-sized species, similar in dental size to P. nyanzae. The main features distinguishing it from all other previously named species of Proconsul are: incisors and deciduous incisors relatively low crowned; upper deciduous canines relatively higher crowned and more robust; molars and deciduous premolars relatively broader and higher crowned, with a more pronounced degree of buccolingual flare and better developed cingula; size differential between molars not as marked; dP₄ with a longer mesial fovea and smaller hypoconulid and distal fovea; P₄ relatively broader, with a better developed buccal cingulum; lower molars less rectangular with a longer mesial fovea, smaller distal fovea, more restricted talonid basin, and a tendency for a smaller hypoconulid; dP⁴ and upper molars with strongly buccolingually splayed roots; mandibular corpus in infants relatively deeper and more slender; maxilla with a well developed canine jugum and fossa. The broader and more flared molars with better developed cingula indicate that the Meswa Bridge species is more primitive than other species of Proconsul. The inference that it is a stem member of the Proconsul clade is consistent with the estimated age of the material.