Brief Communication: Elemental Models of Primate Nursing and Weaning Revisited.

Objectives: Intra-tooth patterns of trace elements barium (Ba) and strontium (Sr) have been used to infer human and nonhuman primate nursing histories, including australopithecine and Neanderthal juveniles. Here we contrast the two elemental models in first molars (M1s) of four wild baboons and explore the assumptions that underlie each. Materials and Methods: Laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS) was employed to create comprehensive calcium-normalized barium and strontium (Ba/Ca, Sr/Ca) maps of M1 enamel and dentine at 35 micron resolution. Results: Postnatal Ba/Ca values were typically high, peaking ~0.5 years of age and then decreasing throughout M1 crown formation; all four individuals showed minimal Ba/Ca values between ~1.2-1.8 years, consistent with field reports of the cessation of suckling. Enamel Sr/Ca did not support patterns of previous LA-ICP-MS spot sampling as the enamel rarely showed discrete Sr/Ca secretory zonation. Increases in Sr/Ca appeared in coronal dentine beginning ~0.3 years, with varied peak value ages (~0.7-2.7 years) and no evidence of a predicted postweaning decline. Discussion: Inferences of baboon weaning ages from initial Ba/Ca minima are more congruent with behavioral observations than Sr/Ca maxima; this is consistent with studies of captive macaques of known weaning ages. Elemental variation is more apparent in the coronal dentine than the enamel of these baboons, which may relate to its more rapid mineralization and protection from the oral environment. Inferences of nursing histories from enamel Sr/Ca patterns alone should be reconsidered, and elevated values of Ba/Ca and Sr/Ca in teeth formed after weaning require further study.

Fine-scaled climate variation in equatorial Africa revealed by modern and fossil primate teeth.

Variability in resource availability is hypothesized to be a significant driver of primate adaptation and evolution, but most paleoclimate proxies cannot recover environmental seasonality on the scale of an individual lifespan. Oxygen isotope compositions (δ18O values) sampled at high spatial resolution in the dentitions of modern African primates (n = 2,352 near weekly measurements from 26 teeth) track concurrent seasonal precipitation, regional climatic patterns, discrete meteorological events, and niche partitioning. We leverage these data to contextualize the first δ18O values of two 17 Ma Afropithecus turkanensis individuals from Kalodirr, Kenya, from which we infer variably bimodal wet seasons, supported by rainfall reconstructions in a global Earth system model. Afropithecus' δ18O fluctuations are intermediate in magnitude between those measured at high resolution in baboons (Papio spp.) living across a gradient of aridity and modern forest-dwelling chimpanzees (Pan troglodytes verus). This large-bodied Miocene ape consumed seasonally variable food and water sources enriched in 18O compared to contemporaneous terrestrial fauna (n = 66 fossil specimens). Reliance on fallback foods during documented dry seasons potentially contributed to novel dental features long considered adaptations to hard-object feeding. Developmentally informed microsampling recovers greater ecological complexity than conventional isotope sampling; the two Miocene apes (n = 248 near weekly measurements) evince as great a range of seasonal δ18O variation as more time-averaged bulk measurements from 101 eastern African Plio-Pleistocene hominins and 42 papionins spanning 4 million y. These results reveal unprecedented environmental histories in primate teeth and suggest a framework for evaluating climate change and primate paleoecology throughout the Cenozoic.

Dental microstructure records life history events: A histological study of mandrills (Mandrillus sphinx) from Gabon.

Accentuated lines in dental microstructure are hypothesized to correlate with potentially stressful life history events, but our understanding of when, how and why such accentuated lines form in relation to stressful events is limited. We examined accentuated line formation and life history events in the teeth of three naturally deceased mandrills (Mandrillus sphinx, Cercopithecidae), for whom we had detailed life history information. We determined the ages at formation of accentuated lines in histological tooth sections and used dates of birth and death to calibrate dental histology to calendar time and individual age. We found accentuated lines that matched their mother's resumption of sexual cycles in two individuals, and possibly in the third individual. The subjects also formed lines when their mothers were mate-guarded by males or wounded. Accentuated lines matched the birth of the next sibling in one of two cases. Both females formed accentuated lines when they experienced their own sexual swelling cycles, but lines did not match all sexual swelling cycles. Mate-guarding matched an accentuated line in one case, but not in another. Lines matched all three parturitions in the two females. Changes in alpha male and captures did not consistently coincide with accentuated line formation, but repeated captures were associated with lines. Using simulated data, we show that the observed number of matches between lines and events would be very unlikely under a null hypothesis of random line formation. Our results support the hypothesis that some life history events are physiologically stressful enough to cause accentuated line formation in teeth. They contribute to our understanding of how primate life histories are recorded during dental development and enhance our ability to use teeth to reconstruct life history in the absence of direct observation.

Teeth reveal juvenile diet, health and neurotoxicant exposure retrospectively: What biological rhythms and chemical records tell us.

Integrated developmental and elemental information in teeth provide a unique framework for documenting breastfeeding histories, physiological disruptions, and neurotoxicant exposure in humans and our primate relatives, including ancient hominins. Here we detail our method for detecting the consumption of mothers' milk and exploring health history through the use of laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS) mapping of sectioned nonhuman primate teeth. Calcium-normalized barium and lead concentrations in tooth enamel and dentine may reflect milk and formula consumption with minimal modification during subsequent tooth mineralization, particularly in dentine. However, skeletal resorption during severe illness, and bioavailable metals in nonmilk foods, can complicate interpretations of nursing behavior. We show that explorations of the patterning of multiple elements may aid in the distinction of these important etiologies. Targeted studies of skeletal chemistry, gastrointestinal maturation, and the dietary bioavailability of metals are needed to optimize these unique records of human health and behavior.

First permanent molars with accentuated line patterns: Assessment of childhood health in an urban complex of the fifth millennium before the present.

OBJECTIVES: The objectives are 1) to calculate the position of highly accentuated lines in dental enamel of a group of individuals from Shahr-i-Sokhta, a thriving urban centre in Bronze Age South West Asia; 2) to identify peak frequencies of physiologically stressful periods during early childhood of these individuals; and 3) to relate these peak frequencies to developmental milestones at population level. DESIGN: We analysed highly accentuated lines in the enamel of nine (n = 9) permanent mandibular first molars of nine individuals from the 5th millennium before the present urban and long-distance-trading complex, Shahr-i Sokhta (Iran). Age at death ranged between 4.5 years and 18-20 years. Permanent mandibular first molar enamel begins to mineralise before birth, and is normally completed sometime between 2.1-3.3 years, giving us insight to early childhood physiological stress, the ages at which it occurs, and any peaks in the frequencies in highly accentuated line formation, through histological sections investigated using transmitted light microscopy. RESULTS: Highly accentuated line peak frequencies occur in the sample at c. four, nine, eleven, and twelve months. After 1 year of age, no more peaks occur. CONCLUSION: The peak frequencies coincide with the timing timing of the type of developmental milestones which may have exposed the individuals to an increased pathogen load, injury, or sub-optimal diet. We note similarity in peak timings in the few published, disparate populations, suggest a potential link with attainment of developmental milestones connected with morbidity, and propose reporting standardised statistics to enable exploration of differences between populations in terms of postnatal health-related stress.

Odontochronologies in male and female mandrills (Mandrillus sphinx) and the development of dental sexual dimorphism.

OBJECTIVES: We examine how dental sexual dimorphism develops in mandrills, an extremely sexually dimorphic primate. We aimed to (a) establish the chronology of dental development (odontochronology) in male and female mandrills, (b) understand interindividual and intersex variation in odontochronologies, and (c) determine how dental sexual dimorphism is achieved. MATERIALS AND METHODS: We prepared histological ground sections from the permanent teeth of four female and four male mandrills from the semi-free ranging colony at the Centre International de Recherches Médicales, Franceville, Gabon. We used the microscopic growth increments in the sections to create odontochronologies. We compared ages at crown initiation, crown formation times (CFT) and crown extension rates (CER) between individuals and sexes to assess interindividual and intersex variation. RESULTS: All mandrill teeth are sexually dimorphic in size. Dental sexual dimorphism in mandrills is achieved via sex differences in the duration of growth (bimaturism) and in growth rates. We also found interindividual and intersex variation in the ages at initiation and completion of crown formation. DISCUSSION: Our results show that the rate of ameloblast differentiation varies between individuals and that selection for both the age at tooth initiation and CER has occurred independently in males and females to ensure that the teeth develop at appropriate times relative to the growth of the sexually dimorphic jaws. They also show that canine dimorphism is achieved through differences in both CER and CFT, unlike extant great apes or Cantius. Given at least three mechanisms for achieving canine dimorphism, we need more information to trace the evolution of this trait in primates.

Enamel formation and growth in non-mammalian cynodonts.

The early evolution of mammals is associated with the linked evolutionary origin of diphyodont tooth replacement, rapid juvenile growth and determinate adult growth. However, specific relationships among these characters during non-mammalian cynodont evolution require further exploration. Here, polarized light microscopy revealed incremental lines, resembling daily laminations of extant mammals, in histological sections of enamel in eight non-mammalian cynodont species. In the more basal non-probainognathian group, enamel extends extremely rapidly from cusp to cervix. By contrast, the enamel of mammaliamorphs is gradually accreted, with slow rates of crown extension, more typical of the majority of non-hypsodont crown mammals. These results are consistent with the reduction in dental replacement rate across the non-mammalian cynodont lineage, with greater rates of crown extension required in most non-probainognathians, and slower crown extension rates permitted in mammaliamorphs, which have reduced patterns of dental replacement in comparison with many non-probainognathians. The evolution of mammal-like growth patterns, with faster juvenile growth and more abruptly terminating adult growth, is linked with this reduction in dental replacement rates and may provide an additional explanation for the observed pattern in enamel growth rates. It is possible that the reduction in enamel extension rates in mammaliamorphs reflects an underlying reduction in skeletal growth rates at the time of postcanine formation, due to a more abruptly terminating pattern of adult growth in these more mammal-like, crownward species.

Tracing fetal and childhood exposure to lead using isotope analysis of deciduous teeth.

We report progress in using the isotopic composition and concentration of Pb in the dentine and enamel of deciduous teeth to provide a high resolution time frame of exposure to Pb during fetal development and early childhood. Isotope measurements (total Pb and (208)Pb/(206)Pb, (207)Pb/(206)Pb ratios) were acquired by laser ablation inductively coupled mass spectrometry at contiguous 100 micron intervals across thin sections of the teeth; from the outer enamel surface to the pulp cavity. Teeth samples (n=10) were selected from two cohorts of children, aged 5-8 years, living in NE England. By integrating the isotope data with histological analysis of the teeth, using the daily incremental lines in dentine, we were able to assign true estimated ages to each ablation point (first 2-3 years for molars, first 1-2 years for incisors+pre-natal growth). Significant differences were observed in the isotope composition and concentration of Pb between children, reflecting differences in the timing and sources of exposure during early childhood. Those born in 2000, after the withdrawal of leaded petrol in 1999, have the lowest dentine Pb levels (<0.2µgPb/g) with (208)Pb/(206)Pb (mean ±2σ: 2.126-2.079) (208)Pb/(206)Pb (mean ±2σ: 0.879-0.856) ratios that correlate very closely with modern day Western European industrial aerosols (PM10, PM2.5) suggesting that diffuse airborne pollution was probably the primary source and exposure pathway. Legacy lead, if present, is insignificant. For those born in 1997, dentine lead levels are typically higher (>0.4µgPb/g) with (208)Pb/(206)Pb (mean ±2σ: 2.145-2.117) (208)Pb/(206)Pb (mean ±2σ: 0.898-0.882) ratios that can be modelled as a binary mix between industrial aerosols and leaded petrol emissions. Short duration, high intensity exposure events (1-2 months) were readily identified, together with evidence that dentine provides a good proxy for childhood changes in the isotope composition of blood Pb. Our pilot study confirms that laser ablation Pb isotope analysis of deciduous teeth, when carried out in conjunction with histological analysis, permits a reconstruction of the timing, duration and source of exposure to Pb during early childhood. With further development, this approach has the potential to study larger cohorts and appraise environments where the levels of exposure to Pb are much higher.

Lemur Biorhythms and Life History Evolution.

Skeletal histology supports the hypothesis that primate life histories are regulated by a neuroendocrine rhythm, the Havers-Halberg Oscillation (HHO). Interestingly, subfossil lemurs are outliers in HHO scaling relationships that have been discovered for haplorhine primates and other mammals. We present new data to determine whether these species represent the general lemur or strepsirrhine condition and to inform models about neuroendocrine-mediated life history evolution. We gathered the largest sample to date of HHO data from histological sections of primate teeth (including the subfossil lemurs) to assess the relationship of these chronobiological measures with life history-related variables including body mass, brain size, age at first female reproduction, and activity level. For anthropoids, these variables show strong correlations with HHO conforming to predictions, though body mass and endocranial volume are strongly correlated with HHO periodicity in this group. However, lemurs (possibly excepting Daubentonia) do not follow this pattern and show markedly less variability in HHO periodicity and lower correlation coefficients and slopes. Moreover, body mass is uncorrelated, and brain size and activity levels are more strongly correlated with HHO periodicity in these animals. We argue that lemurs evolved this pattern due to selection for risk-averse life histories driven by the unpredictability of the environment in Madagascar. These results reinforce the idea that HHO influences life history evolution differently in response to specific ecological selection regimes.

Determinants of childhood lead exposure in the postleaded petrol era: The Tooth Fairy cohort from Newcastle upon Tyne.

Lead is an environmental contaminant causing irreversible health effects in children. We used dentine lead levels as a measure of early-life lead exposure and explored determinants of lead exposure in children living in Newcastle upon Tyne, a historically industrialised UK city, in a cohort born since legislation was introduced to remove lead from petrol, paint and water pipes. The "Tooth Fairy study" cohort comprised 69 children aged 5-8 years. We collected upper deciduous incisors from children and questionnaire data from their parents in 2005. We measured lead levels in pre- and postnatal enamel and dentine using laser ablation inductively coupled plasma mass spectrometry, and assessed associations between dentine lead levels and residential, dietary, lifestyle and socio-economic characteristics. Dentine lead levels were low (mean 0.26 µg/g, range 0.06-0.77); however, we observed considerable variability in dentine lead levels within and between children suggestive of differing exposure levels and/or exposure sources across this population. Variables earlier documented to be associated with childhood lead levels were not found to be significant determinants of dentine lead levels in this study. Exposure pathways should continue to be investigated to enable targeted interventions and prevention of lead-induced health impacts in vulnerable populations.

3D-Geomorphometrics tooth shape analysis in hypodontia.

Assessment of tooth morphology is an important part of the diagnosis and management of hypodontia patients. Several techniques have been used to analyze tooth form in hypodontia patients and these have shown smaller tooth dimensions and anomalous tooth shapes in patients with hypodontia when compared with controls. However, previous studies have mainly used 2D images and provided limited information. In the present study, 3D surface-imaging and statistical shape analysis were used to evaluate tooth form differences between hypodontia and control patients. Eighteen anatomical landmarks were recorded on the clinical crown of the lower left first permanent molar of 3D scanned study models of hypodontia and control subjects. The study sample group comprised of 120 hypodontia patients (40 mild, 40 moderate, and 40 severe hypodontia patients) and 40 age- and sex-matched controls. Procrustes coordinates were utilized to scale and superimpose the landmark coordinate data and then were subjected to principal component analysis (PCA). Subsequently, differences in shape as well as size were tested statistically using allometric analysis and MANOVA. Significant interaction was found between the two factor variables "group" and "sex" (p < 0.002). Overall expected accuracies were 66 and 56% for females and males, respectively, in the cross-validated discriminant-analysis using the first 20 PCs. Hypodontia groups showed significant shape differences compared with the control subjects (p < 0.0001). Significant differences in tooth crown shape were also found between sexes (p < 0.0001) within groups. Furthermore, the degree of variation in tooth form was proportional to the degree of the severity of the hypodontia. Thus, quantitative measurement of tooth shape in hypodontia patients may enhance the multidisciplinary management of those patients.

Reconstructing the life-time lead exposure in children using dentine in deciduous teeth.

Data are presented to demonstrate that the circumpulpal dentine of deciduous teeth can be used to reconstruct a detailed record of childhood exposure to lead. By combining high spatial resolution laser ablation ICP-MS with dental histology, information was acquired on the concentration of lead in dentine from in utero to several years after birth, using a true time template of dentine growth. Time corrected lead analyses for pairs of deciduous molars confirmed that between-tooth variation for the same child was negligible and that meaningful exposure histories can be obtained from a single, multi-point ablation transect on longitudinal sections of individual teeth. For a laser beam of 100 µm diameter, the lead signal for each ablation point represented a time span of 42 days. Simultaneous analyses for Sr, Zn and Mg suggest that the incorporation of Pb into dentine (carbonated apatite) is most likely controlled by nanocrystal growth mechanisms. The study also highlights the importance of discriminating between primary and secondary dentine and the dangers of translating lead analyses into blood lead estimates without determining the age or duration of dentine sampled. Further work is in progress to validate deciduous teeth as blood lead biomarkers.

The relationship of accentuated lines in enamel to weaning stress in juvenile baboons (Papio hamadryas anubis).

Weaning conflict may represent an evolutionary conflict of interest between parent and offspring, an honest signal of need on the part of a weanling, or both. Accentuated lines visible in histological sections of teeth are indicators of stress during enamel formation and have been hypothesised to form in baboon teeth during weaning. We analysed growth increments in 5 tooth sections from 2 Ugandan baboons (Papio hamadryas anubis), using polarised light microscopy, to determine when stresses occurred during the weaning process. Dietary transitions were reconstructed using normalised strontium intensities (Sr/Ca) in enamel. Accentuated lines were cross-matched between teeth from the same animal and plotted by month. The highest frequency of stress was experienced at around 6 months in 1 baboon, coinciding with an inferred reduction in suckling frequency, and at 11 months in another, coinciding with the inferred cessation of suckling. Because accentuated lines appear to indicate weaning stress at dietary transitions, weaning conflict may represent an honest signal of need on the part of the weanling.

Phylogeny, life history and the timing of molar crown formation in two archaic ungulates, Meniscotherium and Phenacodus (Mammalia, 'Condylarthra').

The condylarths, or archaic ungulates, are a paraphyletic mammalian group including a number of fossil taxa whose relationships are unresolved. Included are two genera from the Paleocene and Eocene of North America, Meniscotherium and Phenacodus. Some workers place both genera in the family Phenacodontidae, while others exclude the highly dentally derived Meniscotherium. In this study, we use growth increments in histological thin sections to examine the timing of crown formation in five molars of Meniscotherium and one each of Phenacodusintermedius and Phenacodus trilobatus. We also use perikymata counts on an additional six molars of Meniscotherium. Although estimated body mass and molar dimensions in Meniscotherium are smaller than in either species of Phenacodus, molar formation times are longer, ranging from 0.71 to 1.44 years. Both Phenacodus molars take less than a year to form. Crown extension rates, the rate at which the crown grows in height, are as low as 3-15 microm per day in Meniscotherium, but range from 13 to 54 microm per day in Phenacodus. Although striae periodicities and daily enamel secretion rate are similar in both genera, the differences in the crown extension rate and overall timing of crown formation suggest differences in life histories and raise questions about the phylogenetic relationship of the two genera.

Lamellar bone is an incremental tissue reconciling enamel rhythms, body size, and organismal life history.

Mammalian enamel formation is periodic, including fluctuations attributable to the daily biological clock as well as longer-period oscillations that enigmatically correlate with body mass. Because the scaling of bone mass to body mass is an axiom of vertebrate hard tissue biology, we consider that long-period enamel formation rhythms may reflect corresponding and heretofore unrecognized rhythms in bone growth. The principal aim of this study is to seek a rhythm in bone growth demonstrably related to enamel oscillatory development. Our analytical approach is based in morphology, using a variety of hard tissue microscopy techniques. We first ascertain the relationship among long-period enamel rhythms, the striae of Retzius, and body mass using a large sample of mammalian taxa. In addition, we test whether osteocyte lacuna density (a surrogate for rates of cell proliferation) in bone is correlated with mammalian body mass. Finally, using fluorescently labeled developing bone tissues, we investigate whether the bone lamella, a fundamental microanatomical unit of bone, relates to rhythmic enamel growth increments. Our results confirm a positive correlation between long-period enamel rhythms and body mass and a negative correlation between osteocyte density and body mass. We also confirm that lamellar bone is an incremental tissue, one lamella formed in the species-specific time dependency of striae of Retzius formation. We conclude by contextualizing our morphological research with a current understanding of autonomic regulatory control of the skeleton and body mass, suggesting a central contribution to the coordination of organismal life history and body mass.

Tracking dietary transitions in weanling baboons (Papio hamadryas anubis) using strontium/calcium ratios in enamel.

Strontium and calcium are incorporated into developing teeth in a manner that reflects changing physiological concentrations in the body. A new model predicts changes in strontium/calcium (Sr/Ca) ratios in response to dietary transitions experienced at birth and during the weaning period. Microsampling of longitudinal thin sections of tooth enamel using laser ablation inductively coupled plasma mass spectrometry provides a basis for the systematic evaluation of variation in Sr/Ca ratios within the tooth crown. Incremental growth markers in enamel are used to determine the age of onset of enamel mineralization at each sampling point. Thin sections of 5 teeth from 2 wild-caught baboons (Papio hamadryas anubis) were systematically analysed using this technique. Intra- and intertooth analyses of Sr/Ca ratios reveal a pattern of dietary development during the period of enamel formation that is consistent with observational data on the timing of weaning behaviour in anubis baboons.

Life history theory and dental development in four species of catarrhine primates.

Dental development was reconstructed in several individuals representing four species of catarrhine primates--Symphalangus syndactylus, Hylobates lar, Semnopithecus entellus priam, and Papio hamadryas--using the techniques of dental histology. Bar charts assumed to represent species-typical dental development were constructed from these data and estimated ages at first and third molar emergence were plotted on them along with ages at weaning, menarche, and first reproduction from the literature. The estimated age at first molar emergence appears to occur at weaning in the siamang, lar gibbon, and langur, and just after weaning in the baboon. Age at menarche and first reproduction occur earlier relative to dental development in both cercopithecoids than in the hylobatids, suggesting that early reproduction may be a derived trait in cercopithecoids. The results are examined in the context of life history theory.

Effect of diet on dental development in four species of catarrhine primates.

In this study, dental development is described in two pairs of closely related catarrhine primate species that differ in their degree of folivory: 1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental development to determine how dental development is accelerated in the more folivorous species of each pair. Although anterior tooth formation appears to be unrelated to diet, both S. syndactylus and S. entellus initiate the slowest-forming molar earlier than the related less-folivorous species, which supports the hypothesis that dental acceleration is related to food processing. S. syndactylus initiates M2 crown formation at an earlier age than H. lar, and S. entellus initiates and completes M3 at an earlier age than P. h. hamadryas. Similar stages of M3 eruption occur earlier in the more folivorous species; however, the sex of the individual may also play a role in creating such differences. Although the age at M3 emergence is close to that reported for the end of body mass growth in lar gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence may not be coupled to body mass growth in siamangs.

Out of the mouths of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia.

The techniques of dental histology provide a method for reconstructing much of the life history of an individual, as accentuated increments visible in polarized light microscopy record incidents of physiological stress during the formation of dental tissues. Combined with counts of the normal periodic growth increments, they provide a means of reconstructing the chronology of dental development, age at death, and the ages at which stress occurs. In this study, we determine age at death and reconstruct the chronology of dental development in two male anubis baboons from Uganda and two female baboons from the Awash National Park hybrid zone. For the female baboons, we used the dates of death and rainfall records for the region to determine date of birth, ages at periods of physiological stress, dates at which these stresses occurred, and rainfall amounts for those months. Ages determined histologically for each specimen are comparable to ages estimated from dental emergence schedules and dental scores for wild baboons. Crown formation times are longer than those reported in radiographic studies of captive yellow baboons. Age at initiation of crown formation is similar to that reported for radiographic studies, but ages at completion of crown formation are consistently later. The pattern of stresses is similar in the two female baboons, suggesting that individual life history intersects with local ecology to produce a pattern of accentuated increments occurring during the weaning process and at the onset of menarche, as well as during the first postweaning dry and rainy periods.