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.     

Platyrrhine dental eruption sequences

To determine dental eruption sequences of extant platyrrhines, 367 mandibles and maxillae of informative juvenile specimens from all 16 genera were scored for presence of permanent teeth including three intermediate eruption stages following Harvati (Am J Phys Anthropol 112 (2000) 69-85). The timing of molar eruption relative to that of the anterior dentition is variable in platyrrhines. Aotus is precocious, with all molars erupting in succession before replacement of any deciduous teeth, while Cebus is delayed in M2-3 eruption relative to I1-2. Callitrichines have a distinct tendency toward delayed canine and premolar development. Platyrrhine eruption sequences presented here show some evidence of conformity to Schultz's Rule, with relatively early replacement of deciduous dentition in "slower"-growing animals. The relationship of dental eruption sequences to degree of folivory, body mass, brain mass, and dietary quality is also examined. The early eruption of molars relative to anterior teeth in Pithecia, Chiropotes, and Cacajao, in comparison to genera such as Ateles, Lagothrix, and Alouatta, showing relatively later eruption of the molars, appears to be consistent with current phylogenetic hypotheses. Schultz (Am J Phys Anthropol 19 (1935) 489-581) postulated early relative molar eruption as the primitive dental eruption schedule for primates. The extremely early molar eruption of Aotus versus Callicebus (where both incisors erupt before M2 and M3, with M3 usually last) may lend support to the status of Aotus as a basal taxon. The early relative molar eruption of the fossil platyrrhine species Branisella boliviana is also consistent with this hypothesis (Takai et al.: Am J Phys Anthropol 111 (2000) 263-281).     

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.     

Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history

The ring-tailed lemurs at Beza Mahafaly Special Reserve, Madagascar, exhibit a high frequency of severe wear and antemortem tooth loss. As part of a long-term study, we collected dental data on 83 living adult ring-tailed lemurs during 2003 and 2004. Among these individuals, 192 teeth were scored as absent. The most frequently missing tooth position is M1 (24%). As M1 is the first tooth to erupt, its high frequency of absence (primarily a result of wear) is not remarkable. However, the remaining pattern of tooth loss does not correlate with the sequence of eruption. We suggest that this pattern is a function of 1) feeding ecology, as hard, tough tamarind fruit is a key fallback food of ring-tailed lemurs living in gallery forests; 2) food processing, as tamarind fruit is primarily processed in the P3-M1 region of the mouth; and 3) tooth structure, as ring-tailed lemurs possess thin dental enamel. The incongruity between thin enamel and use of a hard, tough fallback food suggests that ring-tailed lemurs living in riverine gallery forests may rely on resources not used in the past. When comparing dental health in the same individuals (n=50) between 2003 and 2004, we found that individual tooth loss can show a rapid increase over the span of one year, increasing by as much as 20%. Despite this rapid loss, individuals are able to survive, sometimes benefiting from unintentional assistance from conspecifics, from which partially processed tamarind fruit is obtained. Although less frequent in this population, these longitudinal data also illustrate that ring-tailed lemurs lose teeth due to damage and disease, similar to other nonhuman primates. The relationship between tooth loss, feeding ecology, dental structure, and individual life history in this population has implications for interpreting behavior based on tooth loss in the hominid fossil record.     

Dental fast track: Prenatal enamel growth,incisor eruption,and weaning in human infants

Correlation between the timing of permanent first molar eruption and weaning age in extant primates has provided a way to infer a life history event in fossil species, but recent debate has questioned whether the same link is present in human infants. Deciduous incisors erupt at an age when breast milk can be supplemented with additional foods (mixed feeding), and weaning is typically complete before permanent first molars erupt. Here, I use histological methods to calculate the prenatal rate by which enamel increases in thickness and height on human deciduous incisors, canines, and molars (n = 125). Growth trajectories for each tooth type are related to the trimesters and assessed against the eruption sequence and final crown height. Analyses show that central incisors initiate early in the second trimester with significantly faster secretion rates relative to canines and second molars, which initiate closer to birth. Even though initial extension rates were correlated with crown height and scaled with positive allometry within each tooth class, the relatively short incisors still increased in height at a significantly faster rate than the taller canines and molars. The incisor prenatal “fast track” produces a greater proportion of the crown before birth than all other tooth types. This growth mechanism likely facilitates early incisor eruption at a time when the mixed feeding of infants can be initiated as part of the weaning process. Findings provide a basis from which to explore new links between developmental trends along the tooth row and mixed feeding age in other primates. Am J Phys Anthropol 156:407–421, 2015. © 2014 Wiley Periodicals, Inc.     

Human Life History Evolution Explains Dissociation between the Timing of Tooth Eruption and Peak Rates of Root Growth

We explored the relationship between growth in tooth root length and the modern human extended period of childhood. Tooth roots provide support to counter chewing forces and so it is advantageous to grow roots quickly to allow teeth to erupt into function as early as possible. Growth in tooth root length occurs with a characteristic spurt or peak in rate sometime between tooth crown completion and root apex closure. Here we show that in Pan troglodytes the peak in root growth rate coincides with the period of time teeth are erupting into function. However, the timing of peak root velocity in modern humans occurs earlier than expected and coincides better with estimates for tooth eruption times in Homo erectus. With more time to grow longer roots prior to eruption and smaller teeth that now require less support at the time they come into function, the root growth spurt no longer confers any advantage in modern humans. We suggest that a prolonged life history schedule eventually neutralised this adaptation some time after the appearance of Homo erectus. The root spurt persists in modern humans as an intrinsic marker event that shows selection operated, not primarily on tooth tissue growth, but on the process of tooth eruption. This demonstrates the overarching influence of life history evolution on several aspects of dental development. These new insights into tooth root growth now provide an additional line of enquiry that may contribute to future studies of more recent life history and dietary adaptations within the genus Homo.     

Developmental stage of the dentition and speech sound production in a series of first-grade schoolchildren.

This study was undertaken to investigate the effect of developmental stage of the dentition on speech sound production in children with and without articulatory speech disorders. In the whole sample, there were 281 subjects, mean age 7.5 years (SD 0.4). The stage of the eruption of the permanent incisors was calculated as the percentage height of each tooth of the mean crown height of the corresponding tooth in a group of 252 young adults. Eruptional stage of the first permanent molars was classified into three categories. Articulatory disorders were diagnosed by one experienced speech therapist and phoniatrician using the Remes Articulation Test [Remes, 1975] for the Finnish language. The results showed a wide interindividual variation in developmental stage of the dentition in a group of 7-year-old children with a tendency of the first permanent molars but not the incisors to erupt earlier in girls than in boys. Boys had a higher frequency of misarticulations estimated to need treatment than did girls. The present results indicate that during eruption of permanent teeth it is more important to draw attention to symmetrical eruption and to individual timing pattern rather than to the mean values of tooth eruption in subjects of the same age. The findings also suggest a decreasing risk of faulty speech sound production with advancing eruption of some permanent teeth still present in 7-year-old children.     

Dental eruption sequence among colobine primates

Dental development is one aspect of growth that is linked to diet and to life history but has not been investigated among colobines since the work of Schultz [1935]. This study establishes the dental eruption sequence for several colobine species and compares it to that of other catarrhines. The mandibles and maxillae of two hundred and four juvenile colobine specimens were scored for presence or absence of permanent teeth and for stages of partial eruption. Eruption was defined as ranging between tooth emergence (any part of a tooth crown above the alveolar margin) and full occlusion, with three intermediate levels manifest between these boundaries. In African colobines, represented by C. guereza, C. angolensis and P. badius, M2 erupts before I2, and in C. angolensis it also erupts before I1. The canine is delayed, erupting after the premolars in females and after M3 in males. Asian colobines show greater diversity in eruption sequences. Nasalis shows no early eruption of the molars and is very similar to Macaca. In Trachypithecus and Pygathrix M(2) erupts before I(2). The canine in Trachypithecus is delayed, erupting after the premolars and, in some males, after M3. In Presbytis M2 erupts before both incisors; M3 erupts before C in both sexes, and often before both premolars. Although the actual timing of eruption is unknown, all colobine species examined except N. larvatus showed some degree of relatively early eruption of M2 and M3. The lack of this tendency in Nasalis sets this genus apart from all other colobines represented in this study. Dental eruption sequence is thought to reflect life history patterns. Early molar eruption in colobines was thought by Schultz (1935) to be a primitive character reflecting shorter life history. Faster growth rates found in folivorous primates have been interpreted as being related to an adaptation to folivory (Leigh 1994), and early eruption of molars may be part of this dietary specialization. The relationships between dental development and both diet and life history are investigated.     

Human tooth development,tooth length and eruption; a study of British archaeological dentitions

Abstract

Human teeth erupt during root growth but few studies report the relationship between fractions of root development and eruption levels. The aim of this study was to assess root stages of deciduous and early erupting permanent teeth (maxillary and mandibular central incisors and first molars) at eruption levels and relate this to root fraction and tooth length. The sample consisted of 620 modern human skeletal remains with developing teeth. Tooth stage (based on Moorrees crown and root stages) and eruption levels of all developing teeth were assessed where possible. Tooth length of isolated teeth was measured. The distribution of root stage at eruption levels was calculated. Results showed that root stage at alveolar eruption was less variable than at partial eruption. Most teeth (72% of 138) at alveolar eruption were at root a quarter (R¼) whereas teeth at partial eruption were at R¼ or root half (R½) (38 and 50% of 128 respectively). These findings suggest that the active phase of eruption is probably a rapid process and occurs during the first half of root growth.     

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.     

Growth changes in endocranial capacity in the Cercopithecoidea and Hominoidea

On the basis of examination of 2588 skulls representing 15 genera (56 species) from the Cercopithecoidea, together with 973 skulls representing six genera (10 species) of the Hominoidea, grouped according to stages of dental development, the pattern of postnatal growth change in endocranial volume has emerged as constant throughout Old World Primates. The brain attains 80% of its adult size by the time the deciduous dentition is fully established; 90% by the time the first permanent molars erupt; 95% during the period of eruption of the premolars and second molars; and some 98 % by the time the last permanent teeth are erupting. This constancy in timing of postnatal endocranial growth contrasts with a progressive variation in parameters associated with brain weight-body weight relationship.     

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.     

Relationships between age and dental attrition in Australian aboriginals

Tooth wear scores (ratios of exposed dentin to total crown area) were calculated from dental casts of Australian Aboriginal subjects of known age from three populations. Linear regression equations relating attrition scores to age were derived. The slope of the regression line reflects the rate of tooth wear, and the intercept is related to the timing of first exposure of dentin. Differences in morphology between anterior and posterior teeth are reflected in a linear relationship between attrition scores and age for anterior teeth but a logarithmic relationship for posterior teeth. Correlations between age and attrition range from less than 0.40 for third molars (where differences in the eruption and occlusion of the teeth resulted in different patterns of wear) to greater than 0.80 for the premolars and first molars. Because of the generally high correlations between age and attrition, it is possible to estimate age from the extent of tooth wear with confidence limits of the order of +/- 10 years.     

Dental Ontogeny in Macroscelides proboscideus (Afrotheria) and Erinaceus europaeus (Lipotyphla)

We investigated the state of dental eruption in specimens of Macroscelides proboscideus and Erinaceus europaeus of known age. When M. proboscideus reaches adult size and sexual maturity, few or none of its replaced permanent cheek teeth have erupted. The approximate sequence of upper tooth eruption is P1, [I3, C, M1], [I1–2], M2, P4, [P2, P3]. Chronologically, E. europaeus erupts its molars and most premolars prior to M. proboscideus; but its first two upper incisors erupt after those of M. proboscideus, and its canines erupt around the same time. The approximate sequence of upper tooth eruption in E. europaeus is [M1, M2, P2, I3], C, M3, P4, P3, I2, I1. Unlike M. proboscideus, E. europaeus does not reach adult size until all permanent teeth except for the anterior incisors have erupted. While not unique among mammals, the attainment of adult body size prior to complete eruption of the permanent cheek teeth is particularly common among macroscelidids and other afrotherians.     

Evidence of strong stabilizing effects on the evolution of boreoeutherian (Mammalia) dental proportions

The dentition is an extremely important organ in mammals with variation in timing and sequence of eruption, crown morphology, and tooth size enabling a range of behavioral, dietary, and functional adaptations across the class. Within this suite of variable mammalian dental phenotypes, relative sizes of teeth reflect variation in the underlying genetic and developmental mechanisms. Two ratios of postcanine tooth lengths capture the relative size of premolars to molars (premolar–molar module, PMM), and among the three molars (molar module component, MMC), and are known to be heritable, independent of body size, and to vary significantly across primates. Here, we explore how these dental traits vary across mammals more broadly, focusing on terrestrial taxa in the clade of Boreoeutheria (Euarchontoglires and Laurasiatheria). We measured the postcanine teeth of N = 1,523 boreoeutherian mammals spanning six orders, 14 families, 36 genera, and 49 species to test hypotheses about associations between dental proportions and phylogenetic relatedness, diet, and life history in mammals. Boreoeutherian postcanine dental proportions sampled in this study carry conserved phylogenetic signal and are not associated with variation in diet. The incorporation of paleontological data provides further evidence that dental proportions may be slower to change than is dietary specialization. These results have implications for our understanding of dental variation and dietary adaptation in mammals.     

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.     

The timing of eruption of the primary dentition in Nigerian children

The objectives of this study were to clarify the eruption time and sequence for primary teeth in Nigerian children. It also investigated the effect of sex and socioeconomic status on the timing and sequence of eruption. A random sample of 1,657 children from ages of 3-40 months were examined--921 (55.6%) males and 736 (44.4%) females. The age of eruption of the teeth was estimated using probit regression. The results show that there was no effect of sex, socioeconomic status or breastfeeding status on the timing of eruption and pattern of teeth eruption in Nigerian children. Left and right teeth had similar eruption times. Eruption times of the lateral incisor, canine, and molars were similar for upper and lower teeth. Interpopulation studies however showed that though the sequence of eruption of primary teeth in Nigerian population is similar to that of their peers in other compared populations, there are observable sex differences in the timing of tooth eruption.     

The role of epithelial remodelling in tooth eruption in larval zebrafish

Based on light and transmission electron-microscopic observations on erupting first-generation teeth in the zebrafish, Danio rerio, we propose a biphasic mechanism for tooth eruption: (1). formation of an epithelial crypt prior to eruption of the tooth, possibly as a result of constraints in the epithelium resulting from the growth of adjacent tooth germs, and (2). detachment of cellular interdigitations both within the pharyngeal epithelium, at the pharyngeal epithelium/enamel organ boundary, and between the outer and inner dental epithelium, resulting in the exposure of the tooth tip in the crypt, immediately after tooth ankylosis. Later, further detachment of interdigitations between the inner and the outer enamel epithelium unfolds the epithelium even more and leads to a more pronounced exposure of the tooth tip. The presence of small patches of non-collagenous matrix on the outer surface of the tooth close to where it merges with the attachment bone is interpreted as a device to prevent complete detachment of the enamel organ. The biphasic nature of the mechanism for tooth eruption is supported by observations on in vitro cultured heads. First-generation teeth develop normally and crypts are formed, as under in vivo conditions, but the teeth fail to erupt. Taken together, our observations suggest that epithelial remodelling plays a crucial role in eruption of the teeth in this model organism.     

Masculinization of the eruption pattern of permanent mandibular canines in opposite sex twin girls

The aim of this study is to explore the effect of prenatal androgenization on the clinical eruption of permanent teeth expressing dimorphism and bimaturism. The eruption curves of permanent teeth (except third molars), including those that make up the canine complex (permanent canines, lower first premolars), are compared among opposite sex twins (OS twins) relative to single‐born boys and girls. The comparisons are made with regard to three phases of eruption (pierced mucosa, half‐ erupted, and completely erupted) from a cross‐sectional sample of dental casts, using Kaplan–Meier survival and Cox regression analyzes. The casts were collected from 2159 school children from the US Collaborative Perinatal Project, including 39 pairs of OS‐twins, of which 12 pairs (30.8%) were Euro‐Americans and 27 pairs (69.2%) were of African‐American ancestry. The eruption patterns of the incisors, upper first molars, and lower canines were found to be significantly masculinized (delayed) among OS twin girls. The differences in most other teeth were either not significant, or the number of observations of active eruption phases were too few, such as in the upper first molars and incisors, to yield strong evidence and meaningful results. The masculinization of the tooth eruption pattern in OS twin girls is intriguing because of the lower canine responses during puberty, as well as canine primordial formation during early fetal androgenization of their co‐twin during the 8th to 14th gestational weeks. The present results offer a challenge for future research exploring tooth eruption mechanisms, and may also highlight some cases of delayed or ectopic canines, which are biased toward females. Am J Phys Anthropol 151:566–572, 2013. © 2013 Wiley Periodicals, Inc.