M. Christopher Dean

How Neanderthal molar teeth grew

Growth and development are both fundamental components of demographic structure and life history strategy. Together with information about developmental timing they ultimately contribute to a better understanding of Neanderthal extinction. Primate molar tooth development tracks the pace of life history evolution most closely, and tooth histology reveals a record of birth as well as the timing of crown and root growth. High-resolution micro-computed tomography now allows us to image complex structures and uncover subtle differences in adult tooth morphology that are determined early in embryonic development. Here we show that the timing of molar crown and root completion in Neanderthals matches those known for modern humans but that a more complex enamel–dentine junction morphology and a late peak in root extension rate sets them apart. Previous predictions about Neanderthal growth, based only on anterior tooth surfaces, were necessarily speculative. These data are the first on internal molar microstructure; they firmly place key Neanderthal life history variables within those known for modern humans.

New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in early Homo

Since its discovery in 1972 (ref. 1), the cranium KNM-ER 1470 has been at the centre of the debate over the number of species of early Homo present in the early Pleistocene epoch of eastern Africa. KNM-ER 1470 stands out among other specimens attributed to early Homo because of its larger size, and its flat and subnasally orthognathic face with anteriorly placed maxillary zygomatic roots. This singular morphology and the incomplete preservation of the fossil have led to different views as to whether KNM-ER 1470 can be accommodated within a single species of early Homo that is highly variable because of sexual, geographical and temporal factors, or whether it provides evidence of species diversity marked by differences in cranial size and facial or masticatory adaptation. Here we report on three newly discovered fossils, aged between 1.78 and 1.95 million years (Myr) old, that clarify the anatomy and taxonomic status of KNM-ER 1470. KNM-ER 62000, a well-preserved face of a late juvenile hominin, closely resembles KNM-ER 1470 but is notably smaller. It preserves previously unknown morphology, including moderately sized, mesiodistally long postcanine teeth. The nearly complete mandible KNM-ER 60000 and mandibular fragment KNM-ER 62003 have a dental arcade that is short anteroposteriorly and flat across the front, with small incisors; these features are consistent with the arcade morphology of KNM-ER 1470 and KNM-ER 62000. The new fossils confirm the presence of two contemporary species of early Homo, in addition to Homo erectus, in the early Pleistocene of eastern Africa.

The developmental clock of dental enamel: a test for the periodicity of prism cross‐striations in modern humans and an evaluation of the most likely sources of error in histological studies of this kind

Dental tissues contain regular microscopic structures believed to result from periodic variations in the secretion of matrix by enamel‐ and dentine‐forming cells. Counts of these structures are an important tool for reconstructing the chronology of dental development in both modern and fossil hominids. Most studies rely on the periodicity of the regular cross‐banding that occurs along the long axis of enamel prisms. These prism cross‐striations are widely thought to reflect a circadian rhythm of enamel matrix secretion and are generally regarded as representing daily increments of tissue. Previously, some researchers have argued against the circadian periodicity of these structures and questioned their use in reconstructing dental development. Here we tested the periodicity of enamel cross‐striations – and the accuracy to which they can be used – in the developing permanent dentition of five children, excavated from a 19th century crypt in London, whose age‐at‐death was independently known. The interruption of crown formation by death was used to calibrate cross‐striation counts. All five individuals produced counts that were strongly consistent with those expected from the independently known ages, taking into account the position of the neonatal line and factors of preservation. These results confirm that cross‐striations do indeed reflect a circadian rhythm in enamel matrix secretion. They further validate their use in reconstructing dental development and in determining the age‐at‐death of the remains of children whose dentitions are still forming at the time of death. Significantly they identify the most likely source of error and the common difficulties encountered in histological studies of this kind.

A faithful record of stressful life events preserved in the dental developmental record of a juvenile gorilla

The pattern and rate of dental development are critical components of the life history of primates. Much recent research has focused on dental development in chimpanzees and other hominoids, but comparatively little is known about dental development in Gorilla. To date, dental chronologies for Gorilla are based on a sample of 1 and information about variations in the time and timing of crown initiation and completion is lacking. We provide data on dental development in 1 captive, juvenile, female, western lowland Gorilla gorilla gorilla of known age, sex, life events, and date of death (carefully documented as part of zoo records) that experienced various physical insults during her first year of life. The perfect natural experiment allowed us to test the association of the timing of accentuated stress lines in teeth with significant physiological and psychological events during ontogeny of this juvenile gorilla. We analyzed histological sections from 14 permanent teeth (maxillary and mandibular I1-M2) and assessed crown initiation (CI) and crown formation times (CFT) using short- and long-period incremental lines in both enamel and dentine; they are advanced for all teeth compared to previously published chronology. The data suggest a relatively accelerated pace of dental development in gorillas compared to chimpanzees and fit an emerging pattern of an accelerated life history schedule in gorillas. Data on the timing of major accentuated lines in the developing dentition are tightly associated with exact dates of surgical procedures and follow-up hospital visits as recorded on zoo medical records. Our data highlight the importance of captive individuals with well-documented medical records for studying life history.

Megadontia, striae periodicity and patterns of enamel secretion in Plio‐Pleistocene fossil hominins

Early hominins formed large and thick‐enamelled cheek‐teeth within relatively short growth periods as compared with modern humans. To understand better the developmental basis of this process, we measured daily enamel increments, or cross striations, in 17 molars of Plio‐Pleistocene hominins representing seven different species, including specimens attributed to early Homo. Our results show considerable variation across species, although all specimens conformed to the known pattern characterised by greater values in outer than inner enamel, and greater cuspal than cervical values. We then compared our results with the megadontia index, which represents tooth size in relation to body mass, for each species to assess the effect of daily growth rates on tooth size. Our results indicate that larger toothed (megadont) taxa display higher rates or faster forming enamel than smaller toothed hominins. By forming enamel quickly, large tooth crowns were able to develop within the constraints of shorter growth periods. Besides daily increments, many animals express long‐period markings (striae of Retzius) in their enamel. We report periodicity values (number of cross striations between adjacent striae) in 14 new specimens of Australopithecus afarensis, Paranthropus aethiopicus, Paranthropus boisei, Homo habilis, Homo rudolfensis and Homo erectus, and show that long‐period striae express a strong association with male and average male–female body mass. Our results for Plio‐Pleistocene hominins show that the biological rhythms that give rise to long‐period striae are encompassed within the range of variation known for modern humans, but show a lower mean and modal value of 7 days in australopithecines. In our sample of early Homo, mean and modal periodicity values were 8 days, and therefore similar to modern humans. These new data on daily rates of enamel formation and periodicity provide a better framework to interpret surface manifestations of internal growth markings on fossil hominin tooth crowns. Importantly, our data on early hominin cross striation variation may now contribute towards solving difficult taxonomic diagnoses where much may depend on fragmentary molar remains and enamel structure.

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.

A comparison of photographic, replication and direct clinical examination methods for detecting developmental defects of enamel

BackgroundDifferent methods have been used for detecting developmental defects of enamel (DDE). This study aimed to compare photographic and replication methods with the direct clinical examination method for detecting DDE in childrens permanent incisors.Methods110 8-10-year-old schoolchildren were randomly selected from an examined sample of 335 primary Shiraz school children. Modified DDE index was used in all three methods. Direct examinations were conducted by two calibrated examiners using flat oral mirrors and tongue blades. Photographs were taken using a digital SLR camera (Nikon D-80), macro lens, macro flashes, and matt flash filters. Impressions were taken using additional-curing silicon material and casts made in orthodontic stone. Impressions and models were both assessed using dental loupes (magnification=x3.5). Each photograph/impression/cast was assessed by two calibrated examiners. Reliability of methods was assessed using kappa agreement tests. Kappa agreement, McNemars and two-sample proportion tests were used to compare results obtained by the photographic and replication methods with those obtained by the direct examination method.ResultsOf the 110 invited children, 90 were photographed and 73 had impressions taken. The photographic method had higher reliability levels than the other two methods, and compared to the direct clinical examination detected significantly more subjects with DDE (P = 0.002), 3.1 times more DDE (P < 0.001) and 6.6 times more hypoplastic DDE (P < 0.001). The number of subjects with hypoplastic DDE detected by the replication method was not significantly higher than that detected by direct clinical examination (P = 0.166), but the replication detected 2.3 times more hypoplastic DDE lesions than the direct examination (P < 0.001).ConclusionThe photographic method was much more sensitive than direct clinical examination in detecting DDE and was the best of the three methods for epidemiological studies. The replication method provided less information about DDE compared to photography. Results of this study have implications for both epidemiological and detailed clinical studies on DDE.

Enamel and dentine development and the life history profile of Victoriapithecus macinnesi from Maboko Island, Kenya

Two permanent lower second molar teeth (KNM-MB 19841 and KNM-MB 27844) attributed to Victoriapithecus macinnesi were prepared for histological analysis. A further five male and three female canine teeth were replicated with a silicone impression material and perikymata counts subsequently made on epoxy casts over the whole crown surface. Daily enamel cross striations averaged 6 microm apart in both cuspal and lateral enamel of the molars and the total crown formation times were approximately 1.24 years in the molars and, using the same periodicity determined from the molars, 1.84 and 1.36 years respectively in the male and female canines. Rates of dentine formation matched those known for extant macaques and were used to calculate root extension rates, which averaged 11.5 microm per day over the whole 8 mm root length of KNM-MB 19841. The period between M2 initiation and gingival emergence was estimated to be approximately 1.95 years in Victoriapithecus which is greater than estimates for Cebus albifrons and Chlorocebus aethiops, (which are similar in body mass to Victoriapithecus), but less than estimates made here for several macaque species. A speculative picture of dental development in Victoriapithecus emerges that is slower than that known for modern vervet monkeys and may have been more similar to that in some smaller modern macaque species.

Permanent tooth mineralization in bonobos (Pan paniscus) and chimpanzees (P. troglodytes).

The timing of tooth mineralization in bonobos (Pan paniscus) is virtually uncharacterized. Analysis of these developmental features in bonobos and the possible differences with its sister species, the chimpanzee (P. troglodytes), is important to properly quantify the normal ranges of dental growth variation in closely related primate species. Understanding this variation among bonobo, chimpanzee and modern human dental development is necessary to better contextualize the life histories of extinct hominins. This study tests whether bonobos and chimpanzees are distinguished from each other by covariance among the relative timing and sequences of tooth crown initiation, mineralization, root extension, and completion. Using multivariate statistical analyses, we compared the relative timing of permanent tooth crypt formation, crown mineralization, and root extension between 34 P. paniscus and 80 P. troglodytes mandibles radiographed in lateral and occlusal views. Covariance among our 12 assigned dental scores failed to statistically distinguish between bonobos and chimpanzees. Rather than clustering by species, individuals clustered by age group (infant, younger or older juvenile, and adult). Dental scores covaried similarly between the incisors, as well as between both premolars. Conversely, covariance among dental scores distinguished the canine and each of the three molars not only from each other, but also from the rest of the anterior teeth. Our study showed no significant differences in the relative timing of permanent tooth crown and root formation between bonobos and chimpanzees.

Structural organization and tooth development in a Homo aff. erectus juvenile mandible from the Early Pleistocene site of Garba IV at Melka Kunture, Ethiopian highlands

OBJECTIVES The immature partial mandible GAR IVE from the c. 1.7 Ma old Garba IV site at Melka Kunture (Upper Awash Basin, Ethiopia), the earliest human representative from a mountain-like environment, represents one of the oldest early Homo specimens bearing a mixed dentition. Following its first description (Condemi, ), we extended the analytical and comparative record of this specimen by providing unreported details about its inner morphology, tooth maturational pattern and age at death, crown size, and tooth tissue proportions. MATERIALS AND METHODS The new body of quantitative structural information and virtual imaging derives from a medical CT record performed in 2013. RESULTS Compared to the extant human condition and to some fossil representatives of comparable individual age, the GAR IVE mandible reveals absolutely and relatively thick cortical bone. Crown size of the permanent lateral incisor and the canine fit the estimates of H. erectus s.l., while the dm2 and the M1 more closely approach those of H. habilis-rudolfensis. Molar crown pulp volumes are lower than reported in other fossil specimens and in extant humans. The mineralization sequence of the permanent tooth elements is represented four times in our reference sample of extant immature individuals (N = 795). CONCLUSIONS The tooth developmental pattern displayed by the immature individual from Garba IV falls within the range of variation of extant human populations and is also comparable with that of other very young early fossil hominins. Taken together, the evidence presented here for mandibular morphology and dental development suggest GAR IVE is a robust 2.5- to 3.5-year old early Homo specimen.