Space invaders: Reassessing the histology of hyperostosis frontalis interna.

Hyperostosis frontalis interna (HFI) is a human skeletal lesion characterized by nodules of hyperplastic bone and thickening of the frontal bone's inner surface. Despite its prevalence in the general population and its long history of observation-it is one of the most frequently observed pathologies in gross anatomy laboratories-HFI's etiology and pathogenesis remain poorly understood. This is largely due to the lack of a thorough survey of its histology across the various stages of its development. Our study has three major aims: (1) assess HFI histology from incipient to advanced lesions; (2) elucidate lamellar and trabecular structure in HFI; and (3) clarify impacts/roles of the dura mater in HFI. Sections of nondecalcified bone provide evidence for two different categories of lesions: (1) stratum lesions, characterized by lamellar-based overall thickening of the internal table, and (2) eruptive lesions, characterized by nodular formations of initially lamellar bone that appear to form the bulk of bone mass in advanced stages. Sections of nondecalcified bone also suggest that for both lesion types, HFI growths begin as deposits of lamellar bone, which are later remodeled into woven bone deposits; our data do not support the hypothesis that lesions begin as a "diploization" of cortical bone as suggested by prior studies. Trichrome-stained sections provide evidence that growing lesions erode through and engulf the dura mater, effectively destroying this tissue layer as they grow laterally and inwardly. Our results indicate possible avenues of research to better understand the root causes of this disorder.

Quantification of enamel decussation in gracile and robust capuchins (Cebus, Sapajus, Cebidae, Platyrrhini).

Multiple behavioral and biomechanical analyses have demonstrated that capuchin monkeys (Cebus and Sapajus) are specialized for breaking down hard-object foods as compared to other cebid monkeys. In addition to a complex suite of craniodental adaptations, it has specifically been demonstrated that capuchins possess highly complex dental enamel, with extensive Hunter-Schreger banding and other decussation, that likely serve as an adaptation to resist crack propagation during hard-object feeding. Furthermore, it has been demonstrated that robust capuchins (Sapajus spp., formerly Cebus apella) demonstrate further adaptation for hard-object feeding than other capuchins, routinely breaking down extremely mechanically challenging foods. However, there has been no comparison of dental enamel complexity in robust versus gracile capuchins, to assess whether the dental enamel in Sapajus follows this same pattern of further specialization. Therefore, this study compares dental enamel complexity in images of dental thin sections from a sample of robust versus gracile capuchins using image compression ratio (ICR) analysis. ICR is a variable that correlates with enamel complexity, such that higher ICR values are indicative of increased complexity in the form of enamel decussation. We found no significant difference between robust and gracile capuchins when assessing all teeth in our sample together, however, we did find that robust capuchins have significantly higher ICR values than gracile capuchins for canine teeth, specifically. Our results support prior studies suggesting that robust capuchins are specialized to generate increased masticatory loads with their anterior dentition, specifically, as compared to gracile species.

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

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 (N = 338) and Lhasa, Tibet/China (N = 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.

Comparative dental anatomy in newborn primates: Cusp mineralization.

Previous descriptive work on deciduous dentition of primates has focused disproportionately on great apes and humans. To address this bias in the literature, we studied 131 subadult nonhominoid specimens (including 110 newborns) describing deciduous tooth morphology and assessing maximum hydroxyapatite density (MHD). All specimens were CT scanned at 70 kVp and reconstructed at 20.5-39 µm voxels. Grayscale intensity from scans was converted to hydroxyapatite (HA) density (mg HA/cm3 ) using a linear conversion of grayscale values to calibration standards of known HA density (R2 = .99). Using Amira software, mineralized dental tissues were captured by segmenting the tooth cusps first and then capturing the remainder of the teeth at descending thresholds of gray levels. We assessed the relationship of MHD of selected teeth to cranial length using Pearson correlation coefficients. In monkeys, anterior teeth are more mineralized than postcanine teeth. In tarsiers and most lemurs and lorises, postcanine teeth are the most highly mineralized. This suggests that monkeys have a more prolonged process of dental mineralization that begins with incisors and canines, while mineralization of postcanine teeth is delayed. This may in part be a result of relatively late weaning in most anthropoid primates. Results also reveal that in lemurs and lorises, MHD of the mandibular first permanent molar (M1 ) negatively correlates with cranial length. In contrast, the MHD of M1 positively correlates with cranial length in monkeys. This supports the hypothesis that natural selection acts independently on dental growth as opposed to mineralization and indicates clear phylogenetic differences among primates.

Application of Image Compression Ratio Analysis as a Method for Quantifying Complexity of Dental Enamel Microstructure.

It is well recognized that enamel microanatomy in mammals reflects biomechanical demands placed upon teeth, as determined by mechanical properties of species' diets, use of teeth as weapons, and so forth. However, there are limited options for researchers wishing to perform large-scale comparisons of enamel microstructure with adaptive questions in mind. This is because to date there has been no efficient method for quantification and statistical analysis of enamel complexity. Our study proposes to apply a method previously developed for quantification of 3D tooth cusp morphology to the problem of quantifying microstructural enamel complexity. Here, we use image compression ratio (ICR) as a proxy variable for enamel complexity in 2D enamel photomicrographs taken using circularly polarized transmitted light microscopy. ICR describes the relationship between a digital image captured in an uncompressed file format and the identical image that has had its file size compressed using computer algorithms; more complex images receive less compression. In our analyses, ICR analysis is able to distinguish between images of teeth with simple, radial enamel and teeth with complex decussating enamel. Moreover, our results show a significant correlation between ICR and enamel complexity ranks assigned via visual assessment. Therefore, our results demonstrate that ICR analysis provides a viable methodology for efficient comparison of overall enamel complexity among dental samples. Anat Rec, 302:2279-2286, 2019. © 2019 American Association for Anatomy.

Histology of dental long-period biorhythms in Canis familiaris.

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.

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.

Primate enamel evinces long period biological timing and regulation of life history.

The factor(s) regulating the combination of traits that define the overall life history matrix of mammalian species, comprising attributes such as brain and body weight, age at sexual maturity, lifespan and others, remains a complete mystery. The principal objectives of the present research are (1) to provide evidence for a key variable effecting life history integration and (2) to provide a model for how one would go about investigating the metabolic mechanisms responsible for this rhythm. We suggest here that a biological rhythm with a period greater than the circadian rhythm is responsible for observed variation in primate life history. Evidence for this rhythm derives from studies of tooth enamel formation. Enamel contains an enigmatic periodicity in its microstructure called the striae of Retzius, which develops at species specific intervals in units of whole days. We refer to this enamel rhythm as the repeat interval (RI). For primates, we identify statistically significant relationships between RI and all common life history traits. Importantly, RI also correlates with basal and specific metabolic rates. With the exception of estrous cyclicity, all relationships share a dependence upon body mass. This dependence on body mass informs us that some aspect of metabolism is responsible for periodic energy allocations at RI timescales, regulating cell proliferation rates and growth, thus controlling the pace, patterning, and co-variation of life history traits. Estrous cyclicity relates to the long period rhythm in a body mass-independent manner. The mass-dependency and -independency of life history relationships with RI periodicity align with hypothalamic-mediated neurosecretory anterior and posterior pituitary outputs. We term this period the Havers-Halberg Oscillation (HHO), in reference to Clopton Havers, a 17th Century hard tissue anatomist, and Franz Halberg, a long-time explorer of long-period rhythms. We propose a mathematical model that may help elucidate the underlying physiological mechanism responsible for the HHO.

Life-history correlates of enamel microstructure in cebidae (Platyrrhini, Primates).

Previous studies have examined tooth eruption as it relates intrinsically to body mass, brain mass, and other life history variables, and extrinsically to ecological factors (e.g., age at foraging independence, environmental risk aversion, and maternal investment). Different models have been explored wherein each of these variables impacts ontogeny. However, anthropoid and strepsirhine primates exhibit interesting differences in the relationships of these ecological and life history variables with tooth eruption. Moreover, interactions between ecological variables and dental tissue growth have only been explored in the lemurs. This study examines dental microstructure of the New World monkey family, Cebidae, to provide further insight into forces influencing the evolution of primate dental ontogeny. The Cebidae were chosen because they are a diverse group which is distinct in ecology and phylogeny from the better known catarrhines of the Old World. Using phylogenetic generalized least squares analyses (PGLS), we test whether brain mass, body mass, or the three above-mentioned ecological variables have stronger correlations with enamel growth. Results show that ecological factors have stronger relationships with cebid dental growth rates than brain or body mass. Foraging independence has the most impact on overall enamel growth as it has the strongest correlation with enamel extension rates. However, another estimate of enamel growth, rate of secretion, has the highest correlation with maternal investment. Our results suggest that an overarching ecological model encompassing the three current ecological hypotheses is needed to further understand the evolution of dental ontogeny within primates.

The functional morphology of the anterior masticatory apparatus in tree-gouging marmosets (Cebidae, Primates).

Although all genera of Callitrichinae feed on tree exudates, marmosets (Callithrix and Cebuella) use specialized anterior teeth to gouge holes in trees and actively stimulate exudate flow. Behavioral studies demonstrate that marmosets use large jaw gapes but do not appear to generate large bite forces (relative to maximal ability) during gouging. Nonetheless, the anterior teeth of marmosets likely experience different loads during gouging compared to nongouging platyrrhines. We use histological data from sectioned teeth, µCTs of jaws and teeth, and in vitro tests of symphyseal strength to compare the anterior masticatory apparatus in Callithrix to nongouging tamarins (Saguinus) and other cebids. We test the hypotheses that (1) marmoset anterior teeth are adapted to accommodate relatively high stresses linked to dissipating gouging forces and (2) the mandibular symphysis does not provide increased load resistance ability compared with closely related nongouging platyrrhines. Differences in decussation between Callithrix and Saguinus are greatest in the anterior teeth, suggesting an increased load resistance ability specifically in incisor and canine enamel of Callithrix. Callithrix lower incisor crowns are labiolingually thicker suggesting increased bending resistance in this plane and improved wedging ability compared with Saguinus. Anterior tooth roots are larger relative to symphyseal bone volume in Callithrix. Anterior tooth root surface areas also are larger in marmosets for their symphyseal volume, but it remains unclear whether this relative increase is an adaptation for dissipating dental stresses versus a growth-related byproduct of relatively elongated incisors. Finally, simulated jaw loading suggests a reduced ability to withstand external forces in the Callithrix symphysis. The contrast between increased load resistance ability in the anterior dentition versus relatively reduced symphyseal strength (1) suggests a complex loading environment during gouging, (2) highlights the possibility of distinct loading patterns in the anterior teeth versus the symphysis, and (3) points to a potential mosaic pattern of dentofacial adaptations to tree gouging.