Publications by authors named "Timothy G Bromage"

64 Publications

Weaning, parturitions and illnesses are recorded in rhesus macaque (Macaca mulatta) dental cementum microstructure.

Am J Primatol 2021 Mar 1;83(3):e23235. Epub 2021 Feb 1.

Department of Molecular Pathobiology, New York University College of Dentistry, New York, New York, USA.

Many open questions in evolutionary studies relate to species' physiological adaptations, including the evolution of their life history and reproductive strategies. There are few empirical methods capable of detecting and timing physiologically impactful events such as weaning, parturition and illnesses from hard tissue remains of either extant or extinct species. Cementum is an incremental tissue with post eruption annual periodicity, which covers the tooth root and functions as a recording structure of an animal's physiology. Here we test the hypothesis that it is possible to detect and time physiologically impactful events through the analysis of dental cementum microstructure. Our sample comprises 41 permanent and deciduous teeth from male and female rhesus macaques (Macaca mulatta) with known medical, lifestyle and life history information. We develop a semi-automated method of cementum histological analysis for the purpose of event detection and timing, aimed at significantly reducing the amount of intra- and interobserver errors typically associated with histological analyses. The results of our work show that we were able to detect known events including weaning, parturition, illness and physical trauma with high accuracy (false negative rate = 3.2%; n = 1), and to time them within an average absolute difference of 0.43 years (R  = .98; p < .05). Nonetheless, we could not distinguish between the several types of stressful events underlying the changes in cementum microstructure. While this study is the first to identify a variety of life history events in macaque dental cementum, laying foundations for future work in conservation and evolutionary studies of both primates and toothed mammals at large, there are some limitations. Other types of analyses (possibly chemical ones) are necessary to tease apart the causes of the stressors.
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http://dx.doi.org/10.1002/ajp.23235DOI Listing
March 2021

MH-ICP-MS Analysis of the Freshwater and Saltwater Environmental Resources of Upolu Island, Samoa.

Molecules 2020 Oct 22;25(21). Epub 2020 Oct 22.

Department of Molecular Pathobiology, New York University College of Dentistry, 345 East 24th Street, New York, NY 10010, USA.

The elemental composition of freshwater and saltwater samples around the South Pacific island of Upolu, Samoa has been investigated together with other indicators of water quality. Up to 69 elements from Li (3) to U (92) are measured in each sample, analyzed by Mattauch-Herzog-inductively coupled plasma-mass spectrometry (MH-ICP-MS). One hundred and seventy-six samples were collected from surface freshwater sources (24 rivers, two volcanic lakes, one dam) and from seawater sources from the surface to 30 m depth (45 inner reef, reef, and outer reef locations) around Upolu Island, including river mouths and estuaries. Principal component and hierarchical clustering correlation analyses were performed on quantile normalized log transformed elemental composition data to identify groups of samples with similar characteristics and to improve the visualization of the full spectrum of elements. Human activities, such as the use of herbicides and pesticides, may relate to observed elevated concentrations of some elements contained in chemicals known to have deleterious obesogenic effects on humans that may also cause coral reef decline. Furthermore, the salinity of some saltwater samples tested were very high, possibly due to climate variability, which may additionally harm the health and biodiversity of coral reefs.
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http://dx.doi.org/10.3390/molecules25214871DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7659969PMC
October 2020

A comprehensive survey of Retzius periodicities in fossil hominins and great apes.

J Hum Evol 2020 12 15;149:102896. Epub 2020 Oct 15.

Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287, USA.

Recent studies have provided great insight into hominin life history evolution by utilizing incremental lines found in dental tissues to reconstruct and compare the growth records of extant and extinct humans versus other ape taxa. Among the hominins, studies that have examined Retzius periodicity (RP) variation have come to contradictory conclusions in some instances. To clarify RP variation among hominins and better place this variation in its broader evolutionary context, we conduct the most comprehensive analysis of published RP values for hominins and great apes to date. We gathered all available data from the literature on RP data from extant humans, great apes, and fossil hominins and assessed their variation using parametric and nonparametric analyses of variance. We also performed phylogenetic generalized least-squares regressions of RP data for these taxa as well as a larger set of hominoids for which RP data have been published against data for body mass, encephalization, and mean semicircular canal radius (a proxy for metabolic rate). Our results show that modern humans have a mean RP significantly differing from that of other hominins. Pongo also is significantly different from nearly all other taxa in all analyses. Our results also demonstrate that RP variation among hominins scales with respect to body mass, encephalization, and semicircular canal radius similarly to other hominids but that modern humans and Pongo stand out in this regard. Operating within the hypothesis that RP reflects autonomic biorhythms that regulate multiple life history variables, our results reinforce the idea that Homo sapiens has evolved a life history distinct from other hominins, even from other members of Homo, and suggest that many of these life history differences may be driven by hypothalamic output from the brain.
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http://dx.doi.org/10.1016/j.jhevol.2020.102896DOI Listing
December 2020

Enamel multidien biological timing and body size variability among individuals of Chinese Han and Tibetan origins.

Ann Hum Biol 2020 Jul 13:1-7. Epub 2020 Jul 13.

Department of Biomaterials, New York University College of Dentistry, New York, NY, USA.

Aims: To measure the number of days of enamel formation between periodic striae of Retzius growth lines, the Retzius periodicity (RP), and to compare this multi-day, or multidien rhythm, to body height and weight among people from Beijing, China and Lhasa, Tibet/China.

Subjects And Methods: Subjects requiring dental extractions from clinics in Beijing, China ( = 338) and Lhasa, Tibet/China ( = 227) provided a tooth and body size information. Multiple observers examined histological sections of the teeth and recorded RP. RP values were statistically compared to body height and weight.

Results: In Beijing and Lhasa samples, respectively, average height was 166.38 and 165.70 cm, average weight was 59.53 and 66.53 kg, and average RP was 7.47 and 7.69 d. Statistically significant differences were found between Beijing and Lhasa weight and RP means. Correlations for height and weight against RP were significant, but only comparatively strong for height.

Conclusions: Supporting the negative correlation presented in previous studies, RP is negatively associated with height and weight among a large intraspecific sample of people from Beijing and Lhasa. RP represents a metabolic-mediated multidien biological timing mechanism responsible for the rate of cell proliferation and maintenance of the body.
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http://dx.doi.org/10.1080/03014460.2020.1785010DOI Listing
July 2020

In vitro shear bond strength of 2 resin cements to zirconia and lithium disilicate: An in vitro study.

J Prosthet Dent 2020 Apr 27. Epub 2020 Apr 27.

Professor, Department of Biomaterials and Department of Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, NY.

Statement Of Problem: There is little evidence on how the multiple layers of zirconia (ZrO) or glazed material will affect the shear bond strength (SBS) of different resin cements.

Purpose: The purpose of this in vitro study was to compare the SBS of 2 resin cements with the different layers of a monolithic polychromatic ZrO ceramic, both glazed and nonglazed, and a lithium disilicate (LDS) ceramic.

Material And Methods: One hundred and sixty-eight composite resin cylinders and 48 monolithic polychromic ZrO plates were prepared. Twenty-four were milled and sintered, and 24 were milled and sintered and had a glaze cycle applied with no liquid glaze. These plates and 12 LDS plates were mounted in autopolymerized acrylic resin. Bonding surfaces were polished, airborne-particle abraded, and cleaned ultrasonically. The different layers (cubic, hybrid, and tetragonal) of the ZrO plates were identified and marked. The plates were assigned to 2 cement groups: a self-adhesive, autopolymerized resin cement, and a dual-polymerizing, adhesive resin cement (DPRC). Bonding surfaces were cleaned and treated according to the cement manufacturer's instructions. Three composite resin cylinders were luted to the ZrO plates at the appropriate layer, and 2 cylinders were luted to each LDS plate. The specimens were stored in a moist environment for 24 hours at 37 °C. The SBS test was performed with a universal testing machine. Visual inspections of the debonded surfaces were compared under magnification. The data were analyzed with a 2-way ANOVA and a subsequent Student t test (α=0.05).

Results: The 2-way ANOVA found no difference among luting agent and LDS and ZrO. The SBSs of the nonglazed tetragonal and cubic layer to the ZrO were higher than to the surface exposed to a glazing cycle (P=.001). The bonded surfaces were examined tactilely and under ×3.5 magnification, followed by light and scanning electron microscopy and recorded as either adhesive, cohesive, or mixed. Almost all failures in the glazed ZrO were mixed and cohesive. However, more adhesive failures were observed in the DPRC group of nonglazed ZrO.

Conclusions: No differences were found between the 2 luting agents for the LDS. For the ZrO cubic and tetragonal layers, the DPRC had higher bond strengths to the nonglazed surfaces.
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http://dx.doi.org/10.1016/j.prosdent.2020.02.020DOI Listing
April 2020

Parturitions, menopause and other physiological stressors are recorded in dental cementum microstructure.

Sci Rep 2020 03 25;10(1):5381. Epub 2020 Mar 25.

Department of Molecular Pathobiology, New York University College of Dentistry, New York, USA.

The life history pattern of recent humans is uniquely derived in many of its aspects including an extended post-reproductive lifespan combined with short interbirth intervals. A number of theories have been proposed to explain the evolution of this unusual pattern. However most have been difficult to test due to the fragmentary nature of the hominin fossil record and the lack of methods capable of inferring such later life history events. In search of a method we tested the hypothesis that the physiologically impactful events of parturition and menopause are recorded in dental cementum microstructure. We performed histomorphological analyses of 47 teeth from 15 individuals with known life history events and were able to detect reproductive events and menopause in all females. Furthermore, we found that other stressful events such as systemic illnesses and incarceration are also detectable. Finally, through the development of a novel analytical method we were able to time all such events with high accuracy (R-squared = 0.92).
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http://dx.doi.org/10.1038/s41598-020-62177-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7096390PMC
March 2020

Short and long period growth markers of enamel formation distinguish European Pleistocene hominins.

Sci Rep 2020 03 13;10(1):4665. Epub 2020 Mar 13.

Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca 3, 09002, Burgos, Spain.

Characterizing dental development in fossil hominins is important for distinguishing between them and for establishing where and when the slow overall growth and development of modern humans appeared. Dental development of australopiths and early Homo was faster than modern humans. The Atapuerca fossils (Spain) fill a barely known gap in human evolution, spanning ~1.2 to ~0.4 million years (Ma), during which H. sapiens and Neandertal dental growth characteristics may have developed. We report here perikymata counts, perikymata distributions and periodicities of all teeth belonging to the TE9 level of Sima del Elefante, level TD6.2 of Gran Dolina (H. antecessor) and Sima de los Huesos. We found some components of dental growth in the Atapuerca fossils resembled more recent H. sapiens. Mosaic evolution of perikymata counts and distribution generate three distinct clusters: H. antecessor, Sima de los Huesos and H. sapiens.
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http://dx.doi.org/10.1038/s41598-020-61659-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7069994PMC
March 2020

Faster growth corresponds with shallower linear hypoplastic defects in great ape canines.

J Hum Evol 2019 12 5;137:102691. Epub 2019 Nov 5.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, 800 22nd Street, NW, Suite 6000, WA, DC 20052, USA; Division of Mammals, National Museum of Natural History, Smithsonian Institution, 10th Street & Constitution Avenue, NW, WA, DC 20560, USA.

Deeper or more 'severe' linear enamel hypoplasia (LEH) defects are hypothesized to reflect more severe stress during development, but it is not yet clear how depth is influenced by intrinsic enamel growth patterns. Recent work documented inter- and intraspecific differences in LEH defect depth in extant great apes, with mountain gorillas having shallower defects than other taxa, and females having deeper defects than males. Here, we assess the correspondence of inter- and intraspecific defect depth and intrinsic aspects of enamel growth: enamel extension rates, outer enamel striae of Retzius angles, and linear enamel thickness. Thin sections of great ape canines (n = 40) from Gorilla beringei beringei, Gorilla gorilla gorilla, Pan troglodytes, and Pongo spp. were analyzed. Enamel extension rates were calculated within deciles of enamel-dentine junction length. Linear enamel thickness and the angle of intersection between striae of Retzius and the outer enamel surface were measured in the imbricational enamel. Mountain gorillas have faster enamel extension rates and shallower striae angles than the other taxa examined. Mountain gorillas have thinner imbricational enamel than western lowland gorillas and orangutans, but not chimpanzees. In the combined-taxon sample, females exhibit larger striae angles and thicker imbricational enamel than males. Enamel extension rates are highly negatively correlated with striae angles and LEH defect depth. Enamel growth variation corresponds with documented inter- and intraspecific differences in LEH defect depth in great ape canines. Mountain gorillas have shallower striae angles and faster extension rates than other taxa, which might explain their shallow LEH defect morphology and the underestimation of their LEH prevalence in previous studies. These results suggest that stressors of similar magnitude and timing might produce defects of different depths in one species or sex vs. another, which has implications for interpretations of stress histories in hominins with variable enamel growth patterns.
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http://dx.doi.org/10.1016/j.jhevol.2019.102691DOI Listing
December 2019

Parenchymal and stromal tissue regeneration of tooth organ by pivotal signals reinstated in decellularized matrix.

Nat Mater 2019 06 21;18(6):627-637. Epub 2019 May 21.

Columbia University, Center for Craniofacial Regeneration, New York, NY, USA.

Cells are transplanted to regenerate an organs' parenchyma, but how transplanted parenchymal cells induce stromal regeneration is elusive. Despite the common use of a decellularized matrix, little is known as to the pivotal signals that must be restored for tissue or organ regeneration. We report that Alx3, a developmentally important gene, orchestrated adult parenchymal and stromal regeneration by directly transactivating Wnt3a and vascular endothelial growth factor. In contrast to the modest parenchyma formed by native adult progenitors, Alx3-restored cells in decellularized scaffolds not only produced vascularized stroma that involved vascular endothelial growth factor signalling, but also parenchymal dentin via the Wnt/β-catenin pathway. In an orthotopic large-animal model following parenchyma and stroma ablation, Wnt3a-recruited endogenous cells regenerated neurovascular stroma and differentiated into parenchymal odontoblast-like cells that extended the processes into newly formed dentin with a structure-mechanical equivalency to native dentin. Thus, the Alx3-Wnt3a axis enables postnatal progenitors with a modest innate regenerative capacity to regenerate adult tissues. Depleted signals in the decellularized matrix may be reinstated by a developmentally pivotal gene or corresponding protein.
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http://dx.doi.org/10.1038/s41563-019-0368-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7362336PMC
June 2019

Differential regulation of Ca influx by ORAI channels mediates enamel mineralization.

Sci Signal 2019 04 23;12(578). Epub 2019 Apr 23.

Department of Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, NY 10010, USA.

Store-operated Ca entry (SOCE) channels are highly selective Ca channels activated by the endoplasmic reticulum (ER) sensors STIM1 and STIM2. Their direct interaction with the pore-forming plasma membrane ORAI proteins (ORAI1, ORAI2, and ORAI3) leads to sustained Ca fluxes that are critical for many cellular functions. Mutations in the human gene result in immunodeficiency, anhidrotic ectodermal dysplasia, and enamel defects. In our investigation of the role of ORAI proteins in enamel, we identified enamel defects in a patient with an null mutation. Targeted deletion of the gene in mice showed enamel defects and reduced SOCE in isolated enamel cells. However, mice showed normal enamel despite having increased SOCE in the enamel cells. Knockdown experiments in the enamel cell line LS8 suggested that ORAI2 and ORAI3 modulated ORAI1 function, with ORAI1 and ORAI2 being the main contributors to SOCE. ORAI1-deficient LS8 cells showed altered mitochondrial respiration with increased oxygen consumption rate and ATP, which was associated with altered redox status and enhanced ER Ca uptake, likely due to S-glutathionylation of SERCA pumps. Our findings demonstrate an important role of ORAI1 in Ca influx in enamel cells and establish a link between SOCE, mitochondrial function, and redox homeostasis.
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http://dx.doi.org/10.1126/scisignal.aav4663DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6818134PMC
April 2019

The evolutionary history of the human face.

Nat Ecol Evol 2019 05 15;3(5):726-736. Epub 2019 Apr 15.

Universidad Complutense de Madrid-Instituto Carlos III (UCMISCIII), Centro de Investigación de la Evolución y Comportamiento Humanos, Madrid, Spain.

The face is the most distinctive feature used to identify others. Modern humans have a short, retracted face beneath a large globular braincase that is distinctively different from that of our closest living relatives. The face is a skeletal complex formed by 14 individual bones that houses parts of the digestive, respiratory, visual and olfactory systems. A key to understanding the origin and evolution of the human face is analysis of the faces of extinct taxa in the hominin clade over the last 6 million years. Yet, as new fossils are recovered and the number of hominin species grows, the question of how and when the modern human face originated remains unclear. By examining key features of the facial skeleton, here we evaluate the evolutionary history of the modern human face in the context of its development, morphology and function, and suggest that its appearance is the result of a combination of biomechanical, physiological and social influences.
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http://dx.doi.org/10.1038/s41559-019-0865-7DOI Listing
May 2019

Assessment of the Silver Penetration and Distribution in Carious Lesions of Deciduous Teeth Treated with Silver Diamine Fluoride.

Caries Res 2019 26;53(4):431-440. Epub 2019 Feb 26.

Department of Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, New York, USA.

The aim of this study was to determine the effects of 38% silver diamine fluoride (SDF) on carious lesions of human deciduous teeth. Ten extracted deciduous incisors with caries were collected and treated with SDF. After the treatment, the teeth were sectioned through the center of the carious lesion. The extent of sliver precipitation was examined using quantitative backscattered electron scanning electron microscopy (qBSE-SEM), energy-dispersive X-ray spectroscopy (EDX), and micro-computed tomography (micro-CT). The qBSE-SEM images revealed that the silver particles could penetrate through the pellicle complex, along with the rod sheaths into the demineralized enamel rods and the dentinal tubules, and form silver-enriched barriers surrounding the carious lesions at depths up to 2,490.2 μm (mean 744.7 ± 448.7 μm) within the dentinal tubules of the carious lesions, but less likely in the sound enamel. The EDX spectrum analysis revealed that carbon, oxygen, phosphorus, chlorine, silver, and calcium were the main elements detected in the lesions treated with SDF. Additionally, sodium, magnesium, aluminum, silicon, zinc, sulfur, and fluorine were detected as the minor elements within the SDF precipitation "zone." The micro-CT analysis further showed that in the deep cavitated lesions, the silver precipitation could be observed in the pulp chamber. These findings provide new evidence defining the SDF mode of action for arresting caries and suggest that the application of a highly concentrated SDF solution on deciduous teeth should be used with caution for various carious lesions.
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http://dx.doi.org/10.1159/000496210DOI Listing
July 2020

Silver and fluoride content and short-term stability of 38% silver diamine fluoride.

J Am Dent Assoc 2019 02;150(2):140-146

Background: As silver diamine fluoride (SDF) gains popularity for caries arrest, the authors aimed to investigate the content of fluoride and silver in 38% SDF produced for the US market and its short-term stability.

Methods: Five samples of 38% SDF were evaluated when the bottle was first opened, and at 7 and 28 days. Fluoride concentrations were determined with a fluoride ion-selective electrode, and silver concentrations were determined with a simultaneous inductively coupled plasma mass spectrometer. pH was measured with a pH probe. Weight and volume of individual drops were measured.

Results: At day 0, 40% of individual measured values were above the expected fluoride concentration, and at day 28, 93% were above the expected fluoride concentration (P = .005). At day 0, 19% of individual measured values were below the lowest expected silver concentration, and at day 28, 93% were below (P < .001). Acidity (pH 10) was consistent over the 3 periods. Mean (standard deviation) weight of a drop was 40 (4.0) milligrams, and mean (standard deviation) volume was 32.55 (1.89) microliters, 30% more than the reported value of 25 μL.

Conclusion: Over 28 days, the product pH is stable, whereas the fluoride content tends to increase and the silver content tends to decrease. Drops were larger than expected when dispensed from the bottle.

Practical Implications: Drops are larger than expected, so each delivers higher than expected quantities of silver and fluoride. Clinicians should exercise caution when using this product on young children, replace the cap immediately, and use as soon as dispensed.
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http://dx.doi.org/10.1016/j.adaj.2018.10.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500427PMC
February 2019

Histology of dental long-period biorhythms in Canis familiaris.

J Anat 2018 11 11;233(5):618-624. Epub 2018 Sep 11.

Department of Biomaterials, New York University College of Dentistry, New York, NY, USA.

Our objective is to assess variation in Havers-Halberg oscillation (HHO) periodicities among domestic dogs (Canis familiaris). The HHO is hypothesized to be a hypothalamic-generated biorhythm coordinating multiple life history variables including body mass and lifespan. Dogs have a broad mass range spanning two orders of magnitude, but this variation has been shown to result from selection on very few genetic loci, and dogs have low variation in other life history traits. Therefore, we predict that HHO variation will not be correlated to body mass among domestic dogs, as it is in anthropoid primates. To test the prediction, we examined dog HHO periodicity via manifestations in tooth enamel and dentine, quantifying HHO rhythm histologically. HHO rhythm is reflected in teeth as the number of days between secretion of successive striae of Retzius (enamel) and Andresen lines (dentine), a value referred to as Retzius periodicity (RP). We counted ca. 24-h growth lines between successive Retzius and Andresen lines to determine RP in histological thin-sections from canine teeth of 19 dogs, representing different breeds and sizes. To test our hypothesis, we regressed RP periodicity against body mass data. Dogs have low RP variation for their body mass range, with a modal periodicity of 5 days and a range of 4-6 days. RP was not significantly correlated with body mass. We conclude that mass variation in dogs does not seem driven by HHO physiology, consistent with findings that IGF1 variants produce dog mass variation. However, low RP (and by extension HHO) variation is consistent with low variation in dog lifespan and gestation, suggesting that dog life history may still be governed by HHO mechanisms even if body mass does not reflect this.
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http://dx.doi.org/10.1111/joa.12876DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6183004PMC
November 2018

The biting performance of Homo sapiens and Homo heidelbergensis.

J Hum Evol 2018 05 15;118:56-71. Epub 2018 Mar 15.

Department of Archaeology, University of York, York, YO1 7EP, UK; Hull York Medical School (HYMS), University of York, Heslington, York, North Yorkshire YO10 5DD, UK.

Modern humans have smaller faces relative to Middle and Late Pleistocene members of the genus Homo. While facial reduction and differences in shape have been shown to increase biting efficiency in Homo sapiens relative to these hominins, facial size reduction has also been said to decrease our ability to resist masticatory loads. This study compares crania of Homo heidelbergensis and H. sapiens with respect to mechanical advantages of masticatory muscles, force production efficiency, strains experienced by the cranium and modes of deformation during simulated biting. Analyses utilize X-ray computed tomography (CT) scan-based 3D models of a recent modern human and two H. heidelbergensis. While having muscles of similar cross-sectional area to H. heidelbergensis, our results confirm that the modern human masticatory system is more efficient at converting muscle forces into bite forces. Thus, it can produce higher bite forces than Broken Hill for equal muscle input forces. This difference is the result of alterations in relative in and out-lever arm lengths associated with well-known differences in midfacial prognathism. Apparently at odds with this increased efficiency is the finding that the modern human cranium deforms more, resulting in greater strain magnitudes than Broken Hill when biting at the equivalent tooth. Hence, the facial reduction that characterizes modern humans may not have evolved as a result of selection for force production efficiency. These findings provide further evidence for a degree of uncoupling between form and function in the masticatory system of modern humans. This may reflect the impact of food preparation technologies. These data also support previous suggestions that differences in bite force production efficiency can be considered a spandrel, primarily driven by the midfacial reduction in H. sapiens that occurred for other reasons. Midfacial reduction plausibly resulted in a number of other significant changes in morphology, such as the development of a chin, which has itself been the subject of debate as to whether or not it represents a mechanical adaptation or a spandrel.
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http://dx.doi.org/10.1016/j.jhevol.2018.02.010DOI Listing
May 2018

Influence of Polishing System on the Surface Roughness of Flowable and Regular-Viscosity Bulk Fill Composites.

Int J Periodontics Restorative Dent 2018 July/August;38(4):e79–e86. Epub 2018 Mar 7.

This study evaluated the influence of polishing protocols on the surface roughness of flowable and regular bulk fill composites. Five bulk fill composites were tested: SureFil SDR Flow (SDR), Tetric EvoFlow Bulk fill (TEF), Filtek Bulk Fill Flowable (FIF), Tetric EvoCeram Bulk Fill (TEC), and Filtek Bulk Fill Posterior (FIP). Two polishing protocols were tested: Sof-Lex and Astropol. Astropol created a smoother surface for FIP (P < .05); however, the polishing protocol did not influence surface roughness on TEC (P > .05). SDR, TEF, and FIF exhibited rougher surfaces when polished. Sof-Lex created rougher surfaces for bulk fill composites. It was concluded that surface roughness was related to material composition rather than the polishing system.
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http://dx.doi.org/10.11607/prd.3033DOI Listing
December 2018

The effects of estrogen deficiency on cortical bone microporosity and mineralization.

Bone 2018 05 31;110:1-10. Epub 2018 Jan 31.

Department of Biomedical Engineering, The City College of New York, New York, NY 10031, United States. Electronic address:

Recent studies have demonstrated matrix-mineral alterations in bone tissue surrounding osteocytes in estrogen-deficient animals. While cortical bone porosity has been shown to be a contributor to the mechanical properties of bone tissue, little analysis has been done to investigate the effects of estrogen deficiency on bone's microporosities, including the vascular and osteocyte lacunar porosities. In this study we examined alterations in cortical bone microporosity, mineralization, and cancellous bone architecture due to estrogen deficiency in the ovariectomized rat model of postmenopausal osteoporosis. Twenty-week-old female Sprague-Dawley rats were subjected to either ovariectomy or sham surgery. Six weeks post-surgery tibiae were analyzed using high-resolution micro-CT, backscattered electron imaging, nanoindentation, and dynamic histomorphometry. Estrogen deficiency caused an increase in cortical bone vascular porosity, with enlarged vascular pores and little change in tissue mineral density in the proximal tibial metaphysis. Measurements of cancellous architecture corresponded to previous studies reporting a decrease in bone volume fraction, an increase in trabecular separation, and a decrease in trabecular number in the proximal tibia due to estrogen deficiency. Nanoindentation results showed no differences in matrix stiffness in osteocyte-rich areas of the proximal tibia of estrogen-deficient rats, and bone labeling and backscattered electron imaging showed no significant changes in mineralization around the vascular pores. The findings demonstrate local surface alterations of vascular pores due to estrogen deficiency. An increase in cortical vascular porosity may diminish bone strength as well as alter bone mechanotransduction via interstitial fluid flow, both of which could contribute to bone fragility during postmenopausal osteoporosis.
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http://dx.doi.org/10.1016/j.bone.2018.01.019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377161PMC
May 2018

Store-operated Ca entry controls ameloblast cell function and enamel development.

JCI Insight 2017 03 23;2(6):e91166. Epub 2017 Mar 23.

Department of Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, New York, USA.

Loss-of-function mutations in stromal interaction molecule 1 (STIM1) impair the activation of Ca release-activated Ca (CRAC) channels and store-operated Ca entry (SOCE), resulting in a disease syndrome called CRAC channelopathy that is characterized by severe dental enamel defects. The cause of these enamel defects has remained unclear given a lack of animal models. We generated mice to delete STIM1 and its homolog STIM2 in enamel cells. These mice showed impaired SOCE in enamel cells. Enamel in mice was hypomineralized with decreased Ca content, mechanically weak, and thinner. The morphology of SOCE-deficient ameloblasts was altered, showing loss of the typical ruffled border, resulting in mislocalized mitochondria. Global gene expression analysis of SOCE-deficient ameloblasts revealed strong dysregulation of several pathways. ER stress genes associated with the unfolded protein response were increased in -deficient cells, whereas the expression of components of the glutathione system were decreased. Consistent with increased oxidative stress, we found increased ROS production, decreased mitochondrial function, and abnormal mitochondrial morphology in ameloblasts of mice. Collectively, these data show that loss of SOCE in enamel cells has substantial detrimental effects on gene expression, cell function, and the mineralization of dental enamel.
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http://dx.doi.org/10.1172/jci.insight.91166DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5358480PMC
March 2017

A radiographic study of permanent molar development in wild Virunga mountain gorillas of known chronological age from Rwanda.

Am J Phys Anthropol 2017 05 2;163(1):129-147. Epub 2017 Mar 2.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC, 20052.

Objectives: While dental development is important to life history investigations, data from wild known-aged great apes are scarce. We report on the first radiographic examination of dental development in wild Virunga mountain gorillas, using known-age skeletal samples recovered in Rwanda.

Materials And Methods: In 43 individuals (0.0-14.94 years), we collected radiographs of mandibular molars, and where possible, cone beam CT scans. Molar crown and root calcification status was assessed using two established staging systems, and age prediction equations generated using polynomial regression. Results were compared to available data from known-age captive and wild chimpanzees.

Results: Mountain gorillas generally fell within reported captive chimpanzee distributions or exceeded them, exhibiting older ages at equivalent radiographic stages of development. Differences reflect delayed initiation and/or an extended duration of second molar crown development, and extended first and second molar root development, in mountain gorillas compared to captive chimpanzees. However, differences in the duration of molar root development were less evident compared to wild chimpanzees.

Discussion: Despite sample limitations, our findings extend the known range of variation in radiographic estimates of molar formation timing in great apes, and provide a new age prediction technique based on wild specimens. However, mountain gorillas do not appear accelerated in radiographic assessment of molar formation compared to chimpanzees, as they are for other life history traits. Future studies should aim to resolve the influence of species differences, wild versus captive environments, and/or sampling phenomena on patterns observed here, and more generally, how they relate to variation in tooth size, eruption timing, and developmental life history.
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http://dx.doi.org/10.1002/ajpa.23192DOI Listing
May 2017

Collagen Fiber Orientation in Primate Long Bones.

Anat Rec (Hoboken) 2017 Jul 31;300(7):1189-1207. Epub 2017 Mar 31.

Thomas Hill Emeritus Professor, Department of Orthodontics, Case Western Reserve University, Cleveland, Ohio.

Studies of variation in orientation of collagen fibers within bone have lead to the proposition that these are preferentially aligned to accommodate different kinds of load, with tension best resisted by fibers aligned longitudinally relative to the load, and compression best resisted by transversely aligned fibers. However, previous studies have often neglected to consider the effect of developmental processes, including constraints on collagen fiber orientation (CFO), particularly in primary bone. Here we use circularly polarized light microscopy to examine patterns of CFO in cross-sections from the midshaft femur, humerus, tibia, radius, and ulna in a range of living primate taxa with varied body sizes, phylogenetic relationships and positional behaviors. We find that a preponderance of longitudinally oriented collagen is characteristic of both periosteal primary and intracortically remodeled bone. Where variation does occur among groups, it is not simply understood via interpretations of mechanical loads, although prioritized adaptations to tension and/or shear are considered. While there is some suggestion that CFO may correlate with body size, this relationship is neither consistent nor easily explicable through consideration of size-related changes in mechanical adaptation. The results of our study indicate that there is no clear relationship between CFO and phylogenetic status. One of the principle factors accounting for the range of variation that does exist is primary tissue type, where slower depositing bone is more likely to comprise a larger proportion of oblique to transverse collagen fibers. Anat Rec, 300:1189-1207, 2017. © 2017 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/ar.23571DOI Listing
July 2017

Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue.

J Bone Miner Res 2017 04 12;32(4):688-697. Epub 2016 Dec 12.

Department of Biomedical Engineering, City College of New York, New York, NY, USA.

Osteocytes can remove and remodel small amounts of their surrounding bone matrix through osteocytic osteolysis, which results in increased volume occupied by lacunar and canalicular space (LCS). It is well established that cortical bone stiffness and strength are strongly and inversely correlated with vascular porosity, but whether changes in LCS volume caused by osteocytic osteolysis are large enough to affect bone mechanical properties is not known. In the current studies we tested the hypotheses that (1) lactation and postlactation recovery in mice alter the elastic modulus of bone tissue, and (2) such local changes in mechanical properties are related predominantly to alterations in lacunar and canalicular volume rather than bone matrix composition. Mechanical testing was performed using microindentation to measure modulus in regions containing solely osteocytes and no vascular porosity. Lactation caused a significant (∼13%) reduction in bone tissue-level elastic modulus (p < 0.001). After 1 week postweaning (recovery), bone modulus levels returned to control levels and did not change further after 4 weeks of recovery. LCS porosity tracked inversely with changes in cortical bone modulus. Lacunar and canalicular void space increased 7% and 15% with lactation, respectively (p < 0.05), then returned to control levels at 1 week after weaning. Neither bone mineralization (assessed by high-resolution backscattered scanning electron microscopy) nor mineral/matrix ratio or crystallinity (assessed by Raman microspectroscopy) changed with lactation. Thus, changes in bone mechanical properties induced by lactation and recovery appear to depend predominantly on changes in osteocyte LCS dimensions. Moreover, this study demonstrates that tissue-level cortical bone mechanical properties are rapidly and reversibly modulated by osteocytes in response to physiological challenge. These data point to a hitherto unappreciated role for osteocytes in modulating and maintaining local bone mechanical properties. © 2016 American Society for Bone and Mineral Research.
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http://dx.doi.org/10.1002/jbmr.3044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5395324PMC
April 2017

Line of Sight in Hominoids.

J Clin Pediatr Dent 2016;40(3):251-8

Objectives: It remains unclear how the realignments of the face and basicranium that characterize humans were acquired, both phylogenetically and ontogenetically. The developmentally constrained nature of the skull has been previously demonstrated in other primates using Donald H. Enlow's mammalian craniofacial architectural relationships. Here, we compare crania of our closest relatives to gain greater understanding of how and why the relationship of the face and cranial base is developmentally constrained in order to inform instances of abnormal growth and clinical intervention.

Study Design: A method for evaluating these fundamental architectural relationships using 3D landmark data was developed, thereby taking overall size and the geometric relationships among points into account. A sample of cone-beam computed tomography scans derived from humans and extant apes were analyzed (n=10 and n=6, respectively), as well as fossil hominid crania (n=7). Landmarks for 23 craniofacial architectural points were identified and recorded.

Results And Conclusions: Principal components analyses reveal that despite the similarities in craniofacial architecture between humans, extant apes and fossil hominids, appreciable trends in variation between the extant species suggest that the repositioning of the foramen magnum was only one of a constellation of traits that realigned the basicranium and face during the transition to bipedalism.
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http://dx.doi.org/10.17796/1053-4628-40.3.251DOI Listing
January 2017

Primary bone microanatomy records developmental aspects of life history in catarrhine primates.

J Hum Evol 2016 Mar 10;92:60-79. Epub 2016 Mar 10.

Department of Biomaterials and Biomimetics, New York University College of Dentistry, 345 East 24th Street, New York, NY 10010, USA. Electronic address:

A central challenge in human origins research is to understand how evolution has shaped modern human life history. As fossilized remains of our ancestors provide the only direct evidence for life history evolution, efforts to reconstruct life history in paleontological contexts have focused on hard tissues, particularly on dental development. However, among investigators of other vertebrate groups, there is a long tradition of examining primary bone microstructure to decipher growth rates and maturational timing, based on an empirical relationship between the microanatomy of primary bone and the rate at which it is deposited. We examined ontogenetic variation in primary bone microstructure at the midshaft femur of Chlorocebus aethiops, Hylobates lar, and Pan troglodytes to test whether tissue type proportions vary in accordance with predictions based on body mass growth patterns described previously. In all taxa, younger age classes were characterized by significantly higher percent areas of fibro-lamellar and/or parallel-fibered tissues, while older age classes showed significantly higher proportions of lamellar bone. In prior experimental studies, fibro-lamellar and parallel-fibered tissue types have been associated with faster depositional rates than lamellar bone. Principal components analysis revealed differences among taxa in the timing of this transition, and in the particular tissue types observed among individuals of similar dental emergence status. Among M1 and M2 age classes, higher proportions of parallel-fibered and fibro-lamellar tissues were observed in those taxa characterized by reportedly faster body mass growth rates. Further, persistence of fibro-lamellar tissue throughout DECID, M1 and M2 age classes in chimpanzees contrasts with the pattern reported previously for modern humans. Despite the necessary limitations of our cross-sectional study design and the secondary remodeling of bone in primates, large areas of primary bone remain intact and represent a valuable and independent source of information about the evolution of growth and development in the fossil record.
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http://dx.doi.org/10.1016/j.jhevol.2015.12.004DOI Listing
March 2016

Age-related changes in molar topography and shearing crest length in a wild population of mountain Gorillas from Volcanoes National Park, Rwanda.

Am J Phys Anthropol 2016 May 8;160(1):3-15. Epub 2016 Feb 8.

Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, AZ.

Objectives: Great ape teeth must remain functional over long lifespans. The molars of the most folivorous apes, the mountain gorillas, must maintain shearing function for 40+ years while the animals consume large quantities of mechanically challenging foods. While other folivorous primates experience dental senescence, which compromises their occlusal surfaces and affects their reproductive success as they age, it is unknown whether dental senescence also occurs in mountain gorillas. In this article, we quantified and evaluated how mountain gorilla molars change throughout their long lifespans.

Materials And Methods: We collected high-resolution replicas of M(1)s (n = 15), M(2)s (n = 13), and M(3)s (n = 11) from a cross-sectional sample of wild mountain gorilla skeletons from the Virunga Volcanoes, ranging in age from 4 to 43 years. We employed dental topographic analyses to track how aspects of occlusal slope, angularity, relief index, and orientation patch count rotated change with age. In addition, we measured the relative length of shearing crests in two- and three-dimensions.

Results: Occlusal topography was found to decrease, while 2D relative shearing crest length increased, and 3D relative crest lengths were maintained with age.

Discussion: Our findings indicate that shearing function is maintained throughout the long lifetimes of mountain gorillas. Unlike the dental senescence experienced by other folivorous primates, mountain gorillas do not appear to possess senesced molars despite their long lifetimes, mechanically challenging diets, and decreases in occlusal topography with age.
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http://dx.doi.org/10.1002/ajpa.22943DOI Listing
May 2016

Persistent C3 vegetation accompanied Plio-Pleistocene hominin evolution in the Malawi Rift (Chiwondo Beds, Malawi).

J Hum Evol 2016 Jan 1;90:163-75. Epub 2015 Dec 1.

Senckenberg Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325 Frankfurt, Germany; Institute of Geosciences, Goethe University Frankfurt, Altenhöferallee 1, 60438 Frankfurt, Germany.

The development of East African savannas is crucial for the origin and evolution of early hominins. These ecosystems, however, vary widely in their fraction of woody cover and today range from closed woodland to open grassland savanna. Here, we present the first Plio-Pleistocene long-term carbon isotope (δ(13)C) record from pedogenic carbonate and Suidae teeth in the southern East African Rift (EAR). These δ(13)C data from the Chiwondo and Chitimwe Beds (Karonga Basin, Northern Malawi) represent a southern hemisphere record in the EAR, a key region for reconstructing vegetation patterns in today's Zambezian Savanna, and permit correlation with data on the evolution and migration of early hominins in today's Somali-Masai Endemic Zone. The sediments along the northwestern shore of Lake Malawi contain fossils attributed to Homo rudolfensis and Paranthropus boisei. The associated hominin localities (Uraha, Malema) are situated between the well-known hominin bearing sites of the Somali-Masai Endemic Zone in the Eastern Rift and the Highveld Grassland in southern Africa, and fill an important geographical gap for hominin research. Persistent δ(13)C values around -9‰ from pedogenic carbonate and suid enamel covering the last ∼4.3 Ma indicate a C3-dominated closed environment with regional patches of C4-grasslands in the Karonga Basin. The overall fraction of woody cover of 60-70% reflects significantly higher canopy density in the Malawi Rift than the Eastern Rift through time. The discrepancy between the two savanna types originated in the Late Pliocene, when the Somali-Masai ecosystem started to show increasing evidence for open, C4-dominated landscapes. Based on the Malawi δ(13)C data, the evolution of savanna ecosystems in Eastern Africa followed different patterns along the north-south extent of the EAR. The appearance of C4-grasses is considered a driver of evolutionary faunal shifts, but despite the difference of ecosystem evolution in the north, similar hominins and suids occurred in both landscapes, pointing to distinct habitat flexibility and also nutritional versatility.
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http://dx.doi.org/10.1016/j.jhevol.2015.10.014DOI Listing
January 2016

The Swine Plasma Metabolome Chronicles "Many Days" Biological Timing and Functions Linked to Growth.

PLoS One 2016 6;11(1):e0145919. Epub 2016 Jan 6.

Department of Palaeoanthropology, Senckenberg Research Institute, Frankfurt am Main, Germany.

The paradigm of chronobiology is based almost wholly upon the daily biological clock, or circadian rhythm, which has been the focus of intense molecular, cellular, pharmacological, and behavioral, research. However, the circadian rhythm does not explain biological timings related to fundamental aspects of life history such as rates of tissue/organ/body size development and control of the timing of life stages such as gestation length, age at maturity, and lifespan. This suggests that another biological timing mechanism is at work. Here we focus on a "many days" (multidien) chronobiological period first observed as enigmatic recurring growth lines in developing mammalian tooth enamel that is strongly associate with all adult tissue, organ, and body masses as well as life history attributes such as gestation length, age at maturity, weaning, and lifespan, particularly among the well studied primates. Yet, knowledge of the biological factors regulating the patterning of mammalian life, such as the development of body size and life history structure, does not exist. To identify underlying molecular mechanisms we performed metabolome and genome analyses from blood plasma in domestic pigs. We show that blood plasma metabolites and small non-coding RNA (sncRNA) drawn from 33 domestic pigs over a two-week period strongly oscillate on a 5-day multidien rhythm, as does the pig enamel rhythm. Metabolomics and genomics pathway analyses actually reveal two 5-day rhythms, one related to growth in which biological functions include cell proliferation, apoptosis, and transcription regulation/protein synthesis, and another 5-day rhythm related to degradative pathways that follows three days later. Our results provide experimental confirmation of a 5-day multidien rhythm in the domestic pig linking the periodic growth of enamel with oscillations of the metabolome and genome. This association reveals a new class of chronobiological rhythm and a snapshot of the biological bases that regulate mammalian growth, body size, and life history.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0145919PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4703299PMC
July 2016

Donald H. Enlow: The Integrative Single Double Life of a Hard Tissue Naturalist.

Int J Orthod Milwaukee 2015 ;26(3):13-5

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March 2016

Ontogeny of the maxilla in Neanderthals and their ancestors.

Nat Commun 2015 Dec 7;6:8996. Epub 2015 Dec 7.

Institut Català de Paleoecologia Humana i Evolució Social, Tarragona, Spain.

Neanderthals had large and projecting (prognathic) faces similar to those of their putative ancestors from Sima de los Huesos (SH) and different from the retracted modern human face. When such differences arose during development and the morphogenetic modifications involved are unknown. We show that maxillary growth remodelling (bone formation and resorption) of the Devil's Tower (Gibraltar 2) and La Quina 18 Neanderthals and four SH hominins, all sub-adults, show extensive bone deposition, whereas in modern humans extensive osteoclastic bone resorption is found in the same regions. This morphogenetic difference is evident by ∼5 years of age. Modern human faces are distinct from those of the Neanderthal and SH fossils in part because their postnatal growth processes differ markedly. The growth remodelling identified in these fossil hominins is shared with Australopithecus and early Homo but not with modern humans suggesting that the modern human face is developmentally derived.
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http://dx.doi.org/10.1038/ncomms9996DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4686851PMC
December 2015

Tooth wear and feeding ecology in mountain gorillas from Volcanoes National Park, Rwanda.

Am J Phys Anthropol 2016 Mar 24;159(3):457-65. Epub 2015 Nov 24.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, DC.

Objectives: Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and individual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda.

Material And Methods: We calculated the percent of dentine exposure (PDE) for all permanent molars (M1-M3) of known-age mountain gorillas (N = 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International's Karisoke Research Center.

Results: PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of primate taxa from forest and savanna habitats.

Discussion: Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothesis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear variation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear.
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http://dx.doi.org/10.1002/ajpa.22897DOI Listing
March 2016

Distinct growth of the nasomaxillary complex in Au. sediba.

Sci Rep 2015 Oct 15;5:15175. Epub 2015 Oct 15.

Evolutionary Studies Institute, University of the Witwatersrand, Private Bag 3,Wits 2050, South Africa.

Studies of facial ontogeny in immature hominins have contributed significantly to understanding the evolution of human growth and development. The recently discovered hominin species Autralopithecus sediba is represented by a well-preserved and nearly complete facial skeleton of a juvenile (MH1) which shows a derived facial anatomy. We examined MH1 using high radiation synchrotron to interpret features of the oronasal complex pertinent to facial growth. We also analyzed bone surface microanatomy to identify and map fields of bone deposition and bone resorption, which affect the development of the facial skeleton. The oronasal anatomy (premaxilla-palate-vomer architecture) is similar to other Australopithecus species. However surface growth remodeling of the midface (nasomaxillary complex) differs markedly from Australopithecus, Paranthropus, early Homo and from KNM-WT 15000 (H. erectus/ergaster) showing a distinct distribution of vertically disposed alternating depository and resorptive fields in relation to anterior dental roots and the subnasal region. The ontogeny of the MH1 midface superficially resembles some H. sapiens in the distribution of remodeling fields. The facial growth of MH1 appears unique among early hominins representing an evolutionary modification in facial ontogeny at 1.9 my, or to changes in masticatory system loading associated with diet.
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http://dx.doi.org/10.1038/srep15175DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4606807PMC
October 2015