What molars contribute to an emerging understanding of lateral enamel formation in Neandertals vs. modern humans

Two hypotheses, based on previous work on Neandertal anterior and premolar teeth, are investigated here: (1) that estimated molar lateral enamel formation times in Neandertals are likely to fall within the range of modern human population variation, and (2) that perikymata (lateral enamel growth increments) are distributed across cervical and occlusal halves of the crown differently in Neandertals than they are in modern humans. To investigate these hypotheses, total perikymata numbers and the distribution of perikymata across deciles of crown height were compared for Neandertal, northern European, and southern African upper molar mesiobuccal (mb) cusps, lower molar mesiobuccal cusps, and the lower first molar distobuccal (db) cusp. Sample sizes range from five (Neandertal M(1)db) to 29 (southern African M(1)mb). Neandertal mean perikymata numbers were found to differ significantly from those of both modern human samples (with the Neandertal mean higher) only for the M(2)mb. Regression analysis suggests that, with the exception of the M(2)mb, the hypothesis of equivalence between Neandertal and modern human lateral enamel formation time cannot be rejected. For the M(2)mb, regression analysis strongly suggests that this cusp took longer to form in the Neandertal sample than it did in the southern African sample. Plots of perikymata numbers across deciles of crown height demonstrate that Neandertal perikymata are distributed more evenly across the cervical and occlusal halves of molar crowns than they are in the modern human samples. These results are integrated into a discussion of Neandertal and modern human lateral enamel formation across the dentition, with reference to issues of life history and enamel growth processes.     

Variation in modern human premolar enamel formation times: implications for Neandertals

A recent study demonstrated that variation in enamel cap crown formation in the anterior teeth is greater than that in the molars from two geographically distinct populations: native indigenous southern Africans and northern Europeans. Eighty southern African and 69 northern European premolars (P3 and P4) were analyzed in the present study. Cuspal, lateral, and total enamel formation times were assessed. Although cuspal enamel formation times were not consistently different between the two populations, both lateral and total enamel formation times generally were. Bonferroni-corrected t-tests showed that southern Africans had significantly shorter lateral enamel formation time for five of the six cusps, as well as significantly shorter total enamel formation time for these same cusps. An analysis of covariance performed on the lingual cusps of the upper third and fourth premolars showed that differences in enamel formation times between these populations remained when crown height was statistically controlled. A further goal of this study was to ascertain, based on perikymata counts, what Neandertal periodicities would have to be in order for their teeth to have lateral enamel formation times equivalent to either southern Africans or northern Europeans. To this end, perikymata were counted on 32 Neandertal premolars, and the counts were inserted into regression formulae relating perikymata counts to periodicity for each population and each tooth type. Neandertal enamel formation times could be equivalent to those of southern Africans or northern Europeans only if their hypothetical periodicities fall within the range of periodicities for African apes and modern humans (i.e., 6-12 days). The analysis revealed that both populations could encompass Neandertal timings, with hypothetical periodicities based on the southern African population necessitating a lower range of periodicity (6-8 days) than those based on the northern European population (8-11 days).     

Variation in modern human enamel formation times

Most of what we know about the timing of human enamel formation comes from radiographic studies on children of known age. Here, we present new longitudinal data derived from a histological analysis of tooth enamel. Two samples, one from southern Africa and one from northern Europe, contained all anterior and molar tooth types. Two further samples contained only one tooth type: canines from a medieval Danish sample and third molars from a modern North American sample. Data were collected on 326 molars and 352 anterior teeth. Each tooth was sectioned and prepared for polarized light microscopy. We used daily enamel cross striations to determine cuspal enamel formation time, recorded the periodicity of long-period striae in the lateral enamel, and used this value to calculate enamel formation times for each decile of crown length. We present data that reveal some of the processes whereby differences in enamel formation times arise between our samples. Mean cuspal enamel formation times were similar in southern African and northern European anterior teeth, but differed in certain molar cusps. All the southern African anterior teeth completed enamel formation earlier. The greatest difference in mean chronological age at enamel completion was 5.2 vs. 6.2 years of age in lower canines. However, enamel completion times in the molar teeth showed few differences between the samples, with mean times for the longest forming cusps all falling between 3.0 years and 3.45 years. Our data suggest fewer differences between samples and smaller ranges of variation than in many radiographic studies and present a more realistic picture of worldwide variation in enamel formation times.     

Did the lateral enamel of Neandertal anterior teeth grow differently from that of modern humans?

The formation of lateral enamel in Neandertal anterior teeth has been the subject of recent studies. When compared to the anterior teeth of modern humans from diverse regions (Point Hope, Alaska; Newcastle upon Tyne, England; southern Africa), Neandertal anterior teeth appear to fall within the modern human range of variation for lateral enamel formation time. However, the lateral enamel growth curves of Neandertals are more linear than those of these modern human samples. Other researchers have found that the lateral enamel growth curves of Neandertals are more linear than those of Upper Paleolithic and Mesolithic modern humans as well. The statistical significance of this apparent difference between Neandertal and modern human lateral enamel growth curves is analyzed here. The more linear Neandertal enamel growth curves result from the smaller percentage of total perikymata located in the cervical halves of their teeth. The percentage of total perikymata in the cervical halves of teeth is therefore compared between the Neandertal sample (n=56 teeth) and each modern human population sample: Inuit (n=65 teeth), southern African (n=114 teeth), and northern European (n=115 teeth). There are 18 such comparisons (6 tooth types, Neandertals vs. each of the three modern human populations). Eighteen additional comparisons are made among the modern human population samples. Statistically significant differences are found for 16 of the 18 Neandertal vs. modern human comparisons but for only two of the 18 modern human comparisons. Statistical analyses repeated for subsamples of less worn teeth show a similar pattern. Because surface curvature is thought to affect perikymata spacing, we also conducted measurements to assess surface curvature in thirty teeth. Our analysis shows that surface curvature is not a factor in this lateral enamel growth difference between Neandertals and modern humans.     

Functional implications of primate enamel thickness.

Recent evolutionary interpretations of Hominoidea have postulated functional relationships between tooth form, diet and masticatory biomechanics. A major consideration is the durability of the tooth under certain dietary conditions. Teeth with low cusps and thicker enamel are able to withstand heavy mastication of abrasive food bolus for a longer period. When comparisons are made between species of higher primates the variables of tooth size, cusp morphology, and enamel thickness appear to be related but until now no systematic analysis has been made to determine the functional relevance of several dental dimensions. This study provides data gained from comparisons of dentition of nine species of primates. Histological sections were made of the post canine teeth and 21 dimensions were compared. The relevant dimensions identified serve to withstand dental wear. The distribution of thicker enamel corresponded to the observed wear planes. Humans had thicker enamel than pongids while the macaque had the thinnest. These preliminary results tend to support theories which explain low, thick, enameled cusps in hominids.     

Hominid enamel thickness: I. The Krapina Neandertals

Dental x-rays were taken of isolated and in situ adult molar teeth of the Krapina Neandertal (n = 63) and of recent and contemporary molars (n = 423). The radiographs were digitized at high resolution (1,024 × 1,520 × 8 bits) with a 35 mm solid state scanner. Ratios of enamel cap area to the underlying dentinal-pulpal area were determined and comparisons were made between average ratios for the Neandertal and contemporary molars. Neandertal molars had significantly smaller ratios than did contemporary teeth (P < 0.05). It is suggested that the smaller ratios represent relatively thinner enamel for Neandertals and that the thin enamel may have been caused by a metabolic depression that resulted in reduced enamel quantity (hypoplasia). Alternately, the observed differences may be related to expanded pulps seen in various stages of taurodontism. © 1993 Wiley-Liss, Inc.     

Computed tomography and enamel thickness of maxillary molars of Plio-Pleistocene hominids from Sterkfontein, Swartkrans, and Kromdraai (South Africa): An exploratory study.

This paper is one in a series which explores the possibility of using the non-destructive CT technique to identify patterns in tooth enamel distribution and structure of hominid molars from Plio-Pleistocene sites in South Africa, notably Swartkrans, Sterkfontein, and Kromdraai. Whereas previous investigators have emphasised gross differences in absolute and relative or average enamel thickness between hominid taxa, the present study highlights differences in enamel thickness over functionally significant regions of the crown. Differences in the distribution of enamel in A. robustus, A. africanus, and Homo sp. are identified through the use of bivariate and multivariate analyses, and are interpreted in terms of dietary regimes.     

Some observations on enamel thickness and enamel prism packing in the miocene hominoid Otavipithecus namibiensis

Otavipithecus namibiensis is currently the sole representative of a Miocene hominoid radiation in subequatorial Africa. Several nondestructive techniques, such as computed tomography (CT) and confocal microscopy (CFM), can provide useful information about dental characteristics in this southern African Miocene hominoid. Our studies suggest that the molars of Otavipithecus are characterized by (1) thin enamel and (2) a predominance of pattern 1 enamel prism. Together, these findings provide little support for the recent suggestion of an Afropithecini clade consisting of Otavipithecus, Heliopithecus, and Afropithecus. Instead, they lend some (though not conclusive) support to the suggestion of an Otavipithecus/African ape clade distinct from Afropithecus. © 1995 Wiley-Liss, Inc.     

Basicranial anatomy of Plio-Pleistocene hominids from East and South Africa

The results of a metrical analysis of the basicranium of 19 Plio-Pleistocene fossil hominid crania are presented. The sample includes crania attributed to Australopithecus africanus, Australopithecus boisei, and robustus, and Homo erectus as well as crania whose attribution is still under discussion. These results confirm significant differences between the cranial base patterns of the "gracile" and "robust" australopithecines and the three crania attributed to Homo erectus have a pattern which resembles that of modern humans. None of the crania examined from East Africa sites have base patterns which resemble that of the "gracile" australopithecines. The crania KNM-ER 407 and 732 have patterns which are compatible with them being smaller-bodied females of Australopithecus boisei; KNM-ER 1470 and 1813 have base patterns which most closely resemble that of Homo erectus. The cranial base pattern of KNM-ER 1805 is compatible with its inclusion in either Australopithecus boisei or Homo. When account is taken of the immaturity of Taung, the evidence of its cranial base pattern suggests that if it had reached adulthood it would have resembled the "gracile" australopithecine crania from Sterkfontein and Makapansgat.     

Enamel hypoplasia in the Middle Pleistocene hominids from Atapuerca (Spain)

The prevalence and chronology of enamel hypoplasias were studied in a hominid dental sample from the Sima de los Huesos (SH) Middle Pleistocene site at the Sierra de Atapuerca (Burgos, northern Spain). A total of 89 permanent maxillary teeth, 143 permanent mandibular teeth, and one deciduous lower canine, belonging to a minimum of 29 individuals, were examined. Excluding the antimeres (16 maxillary and 37 mandibular cases) from the sample, the prevalence of hypoplasias in the permanent dentition is 12.8% (23/179), whereas the deciduous tooth also showed an enamel defect. No statistically significant differences were found between both arcades and between the anterior and postcanine teeth for the prevalence of hypoplasias. In both the maxilla and the mandible the highest frequency of enamel hypoplasias was recorded in the canines. Only one tooth (a permanent upper canine) showed two different enamel defects, and most of the hypoplasias were expressed as faint linear horizontal defects. Taking into account the limitations that the incompleteness of virtually all permanent dentitions imposes, we have estimated that the frequency by individual in the SH hominid sample was not greater than 40%. Most of the hypoplasias occurred between birth and 7 years (N = 18, X = 3.5, SD = 1.3). Both the prevalence and severity of the hypoplasias of the SH hominid sample are significantly less than those of a large Neandertal sample. Furthermore, prehistoric hunter-gatherers and historic agricultural and industrial populations exhibit a prevalence of hypoplasias generally higher than that of the SH hominids. Implications for the survival strategies and life quality of the SH hominids are also discussed. © 1995 Wiley-Liss, Inc.     

On thick and thin enamel in hominoids

Martin (1983, 1985) reviewed the significance of enamel thickness in hominoid evolution. He studied cut faces of hominoid teeth using the scanning electron microscope and related enamel prism packing patterns to both enamel formation rates and enamel thickness, although he did not present primary data on formation rates, which he summarised as being either “fast” or “slow.” Martin concluded that thick enamel formed at a fast rate represented the ancestral condition in the human and great ape clade. Thin enamel in African apes reflected a secondary reduction in secretion rates, with outer enamel being formed at a slow rate. The present study on ground sections of great ape and human teeth, using polarised light microscopy, was designed to measure the spacing between incremental growth lines in enamel, including striae of Retzius and prism cross striations, to determine rates of enamel formation in hominoids. Measurements on stria spacing showed that striae generally diverged as they passed outwards through enamel in all taxa. Cross-striation spacings also increased from inner to outer enamel. Secretion rates did not fall into two exclusive categories but varied, giving a spectrum of values generally increasing from within outwards at any one crown level and reducing in cervical enamel. There was no evidence for a reduction in enamel formation rates in outer enamel among African apes. These findings cast doubt on the proposition that the common ancestor of great apes and man had thick enamel formed at a fast rate. It is possible that thin enamel was the primitive condition, in which case thick enamel in humans and in Sivapithecus is derived, suggesting that thick enamel on low cusped teeth evolved on more than one occasion.     

Variation in hominoid molar enamel thickness

Enamel thickness has figured prominently in discussions of hominid origins for nearly a century, although little is known about its intra-taxon variation. It has been suggested that enamel thickness increases from first to third molars, perhaps due to varying functional demands or developmental constraints, but this has not been tested with appropriate statistical methods. We quantified enamel cap area (c), dentine area (b), and enamel-dentine junction length (e) in coronal planes of sections through the mesial and distal cusps in 57 permanent molars of Pan and 59 of Pongo, and calculated average (c/e) and relative enamel thickness (([c/e]/ radicalb) * 100). Posteriorly increasing or decreasing trends in each variable and average (AET) and relative enamel thickness (RET) were tested among molars in the same row. Differences between maxillary and mandibular analogues and between mesial and distal sections of the same tooth were also examined. In mesial sections of both genera, enamel cap area significantly increased posteriorly, except in Pan maxillary sections. In distal sections of maxillary teeth, trends of decreasing dentine area were significant in both taxa, possibly due to hypocone reduction. Significant increases in AET and RET posteriorly were found in all comparisons, except for AET in Pongo distal maxillary sections. Several significant differences were found between maxillary and mandibular analogues in both taxa. Relative to their mesial counterparts, distal sections showed increased enamel cap area and/or decreased dentine area, and thus increased AET and RET. This study indicates that when AET and RET are calculated from samples of mixed molars, variability is exaggerated due to the lumping of tooth types. To maximize taxonomic discrimination using enamel thickness, tooth type and section plane should be taken into account. Nonetheless, previous findings that African apes have relatively thinner enamel than Pongo is supported for certain molar positions.     

Molar crown formation in the Late Miocene Asian hominoids, Sivapithecus parvada and Sivapithecus indicus

During the past decade, studies of enamel development have provided a broad temporal and geographic perspective on evolutionary developmental biology in Miocene hominoids. Here we report some of the first data for molar crown development in one hominoid genus, Sivapithecus. The data are compared to a range of extant and extinct hominoids. Crown formation times (CFTs), daily rates of enamel secretion (DSR), Retzius line number and periodicity, and relative enamel thickness (RET) were calculated in a mandibular first molar of Sivapithecus parvada and a maxillary first molar of Sivapithecus indicus from the Siwalik sequence of Pakistan. A CFT of 2.40 years for the protoconid of S. parvada and 2.25 years for the protocone of S. indicus lie within the range of first molar (M1) formation times for the majority of Miocene hominoids (1.96-2.40 years, excluding Proconsul heseloni), and are similar to an M(1) from Gorilla (2.31 years) and M(1)s from Pan (2.22-2.39 years). This is unlike the longer CFTs in modern humans, which appear to be linked with their extended growth period. In contrast to extant great apes and humans, daily rates of enamel secretion are rapid in the Sivapithecus M1s during the early stages of growth, which seems to be a common pattern for most Miocene apes. The rapid accumulation of cuspal enamel in the Sivapithecus molars produced thicker enamel than either Pan or Gorilla in a comparable period of time. Future studies on larger samples of living and fossil hominoids are needed to clarify trends in crown development, which may be better understood in the context of life history strategies coupled with good data on body mass and brain size.     

Variation in enamel development of South African fossil hominids

Dental tissues provide important insights into aspects of hominid palaeobiology that are otherwise difficult to obtain from studies of the bony skeleton. Tooth enamel is formed by ameloblasts, which demonstrate daily secretory rhythms developing tissue-specific structures known as cross striations, and longer period markings called striae of Retzius. These enamel features were studied in the molars of two well known South African hominid species, Australopithecus africanus and Paranthropus robustus. Using newly developed portable confocal microscopy, we have obtained cross striation periodicities (number of cross striations between adjacent striae) for the largest sample of hominid teeth reported to date. These data indicate a mean periodicity of seven days in these small-bodied hominids. Important differences were observed in the inferred mechanisms of enamel development between these taxa. Ameloblasts maintain high rates of differentiation throughout cervical enamel development in P. robustus but not in A. africanus. In our sample, there were fewer lateral striae of Retzius in P. robustus than in A. africanus. In a molar of P. robustus, lateral enamel formed in a much shorter time than cuspal enamel, and the opposite was observed in two molars of A. africanus. In spite of the greater occlusal area and enamel thickness of the molars of both fossil species compared with modern humans, the total crown formation time of these three fossil molars was shorter than the corresponding tooth type in modern humans. Our results provide support for previous conclusions that molar crown formation time was short in Plio-Pleistocene hominids, and strongly suggest the presence of different mechanisms of amelogenesis, and thus tooth development, in these taxa.     

Fore- and hindlimb proportions in Plio-Pleistocene hominids.

Associated fore- and hindlimb parts of five individuals are known from the hominid Plio-Pleistocene fossil collections in Africa. Four of these have been classified as Australopithecus and show definite evidence that in comparison with humans, forelimbs were relatively large and hindlimbs were relatively small. The fourth individual, placed in the genus Homo, has human proportions. These findings do not necessarily imply locomotor differences: the forelimbs may have been relatively long in Australopithecus simply because they were as yet not completely reduced from their generalized hominoid ancestral state.     

人类牙齿齿冠和齿根分离两种技术方法对牙釉质厚度测量的影响

在基于计算机断层扫描技术（CT）和虚拟图像处理技术的灵长类牙齿测量学研究中,经常需要分离三维虚拟模型的齿冠和齿根,再进行后续测量工作,如计算机辅助的生物力学分析、釉质厚度测量等。而分离齿冠和齿根这一步骤,目前有多种方法,如,1)根据齿颈线切分齿冠,或2)人工建立基底平面切分齿冠。为了评估这两种不同的处理方式对后续的牙齿测量学上的影响,本文使用三维方法测量了82例化石和现代人类下颌后部牙齿的釉质厚度,包括南方古猿、早期人属、尼安德特人和现代人。使用配对t检验对比发现,两种方法得到的釉质厚度数值上没有显著差别,但随后进行的种间比较发现,使用基底平面切分齿冠的方法比较费时,更依赖于测量者的人工操作,并且可能弱化了物种间前臼齿绝对釉质厚度的差异,造成系统误差。其原因是对于前臼齿和前部牙齿等齿颈线形状不规则的标本,基底平面难以建立或误差较大。在未来对釉质厚度的种间差异的研究中,特别对齿颈线形状不规则的标本（如人类前部牙齿及猩猩、黑猩猩的牙齿等）,本文推荐使用齿颈线分离齿冠和齿根,测量和计算齿颈线之上的釉质厚度。釉质厚度有一定的分类学、功能形态学和系统发育学意义。本文积累了一批可供未来对比研究的原始数据,并且发现尼安德特人前臼齿的相对釉质厚度显著小于现代人,这与前人利用臼齿、犬齿所做的对比研究结果相同,支持了尼安德特人拥有较薄的相对釉质厚度这一观点。     

Three-dimensional primate molar enamel thickness

Molar enamel thickness has played an important role in the taxonomic, phylogenetic, and dietary assessments of fossil primate teeth for nearly 90 years. Despite the frequency with which enamel thickness is discussed in paleoanthropological discourse, methods used to attain information about enamel thickness are destructive and record information from only a single plane of section. Such semidestructive planar methods limit sample sizes and ignore dimensional data that may be culled from the entire length of a tooth. In light of recently developed techniques to investigate enamel thickness in 3D and the frequent use of enamel thickness in dietary and phylogenetic interpretations of living and fossil primates, the study presented here aims to produce and make available to other researchers a database of 3D enamel thickness measurements of primate molars (n=182 molars). The 3D enamel thickness measurements reported here generally agree with 2D studies. Hominoids show a broad range of relative enamel thicknesses, and cercopithecoids have relatively thicker enamel than ceboids, which in turn have relatively thicker enamel than strepsirrhine primates, on average. Past studies performed using 2D sections appear to have accurately diagnosed the 3D relative enamel thickness condition in great apes and humans: Gorilla has the relatively thinnest enamel, Pan has relatively thinner enamel than Pongo, and Homo has the relatively thickest enamel. Although the data set presented here has some taxonomic gaps, it may serve as a useful reference for researchers investigating enamel thickness in fossil taxa and studies of primate gnathic biology.     

Allometric patterns of cranial bone thickness in fossil hominids

The interspecific allometry of five measures of total cranial bone thickness is examined in 10 extant catarrhine genera and two fossil hominid samples representing A. africanus and Asian H. erectus. Analysis of the modern sample shows that most interspecific variation in vault thickness can be accounted for by variation in body size. Correlation values are moderate to high (r = 0.75–0.98), and all variables exhibit positive allometry. The bone thickness:body mass relationship of modern humans broadly conforms with that of other primates. However, in the distribution of relative thickness throughout the skull, H. sapiens is distinguished by relative thickening of the parietal and extreme relative thinning of the temporal squama. The bone thickness:body mass relationship in the two early hominid species is examined using published mean body weight estimates generated from post-cranial predictor variables. A. africanus exhibits great similarity to modern humans in its relation to the catarrhine regression data and in the distribution of relative thickness throughout the skull. H. erectus also shows a modern human-like pattern in the distribution of its relative thickness; however, its bone thickness:body mass relationship is dissimilar to that displayed by all other taxa, including the other hominid species. On the basis of these results, it is suggested that the published body weight estimate assigned to H. erectus greatly underestimates actual mean body size for Asian members of this species. © 1996 Wiley-Liss, Inc.     

Dental indicators of growth disturbance in a series of ancient Lower Nubian populations: Changes over time

Previous studies of accentuated striae of Retzius in tooth enamel suggest that early childhood growth disturbance tends to be severe in state-level agricultural societies. The present study investigates the diachronic stability of levels of growth disturbance with a series of Lower Nubian agricultural states broadly similar in terms of mode of subsistence and way of life. The sample consists of 114 first permanent molars from the Meroitic (100 B.C. to 300 A.D.) and X-Group (300 to 600 A.D.) cultures. These teeth were sectioned according to standard histological technique. Data on the frequency and severity of accentuated striae of Retzius were then used to derive estimates of the magnitude of individual growth disturbance. Populations were compared by means of a two-way ANOVA, with growth disturbance as the dependent variable, and age and population as the independent variables. The results show that those dying in childhood experienced significantly higher levels of early childhood growth disturbance than did those surviving to adulthood. The results also show a decline in growth disturbance levels over time. Both X-Group children and X-Group adults experience significantly less early childhood growth disturbance than their Meroitic counterparts. These results suggest an improvement in child health status from Meroitic to X-Group times. Tentative explanatory hypotheses imply an increase in village autonomy, an increase in helminthic disease related to a change in irrigation technology, or direct and indirect effects of consumption of naturally-occurring tetracyclines. These hypotheses are not mutually exclusive, and further research is needed before any of them can be tested.