Ontogenetic Sample Research Articles

A rare ‘flat-headed’ pachycephalosaur (Dinosauria: Pachycephalosauridae) from West Texas, USA, with morphometric and heterochronic considerations

A juvenile pachycephalosaur frontal from the upper Aguja Formation (Late Cretaceous: middle Campanian) of West Texas, USA is unusually thin dorsoventrally, even compared to ‘flat’ frontals of young individuals pertaining to other pachycephalosaur taxa. The specimen is most comparable morphologically and morphometrically to Stegoceras validum. However, it is much thinner than any ‘juvenile’ example of that species, and also differs in the elongate form and radial arrangement of the surficial tubercles, as well as occurrence of radial grooves along the lateral margins of the bone. Such differences are unlikely a reflection of intraspecific variation. Instead, the Aguja specimen likely represents a previously unknown juvenile semaphoront from the southern Western Interior, referred herein to Stegoceras sp. and likely extends the distribution of this widespread Campanian genus. A morphometric evaluation suggests that the holotype specimen of Texacephale langstoni, also from the Aguja Formation, is probably an adult semaphoront of Stegoceras. However, both specimens represent different ontogenetic stages with dissimilar morphologies and so their potential conspecifity remains equivocal. The new Aguja specimen described herein likely represents a ‘paedomorphic’ Campanian pachycephalosaur – one where the onset of doming is displaced until well into ontogeny – a heterochronic attribute Stegoceras sp. shares with S. validum and Pachycephalosaurus wyomingensis. Where an adequate ontogenetic sample is available for comparison, other pachycephalosaur taxa do not seem to exhibit a similar growth progression, and so this appears to be a significant taxonomic characteristic. That some pachycephalosaurs delayed doming of the skull roof during growth is enigmatic, but it may have been an expression of sexual dimorphism, an aid in species recognition, or a response to harsh environmental conditions.

How accurate are medical CT and micro-CT techniques compared to classical histology when addressing the growth of the internal rib parameters?

Rib internal anatomy and its cross-sectional morphology inform about important biomechanical or even evolutionary aspects. Classic histological studies require destructive techniques that are reprehensible depending on the case (e.g., fossils). In the last years, non-destructive CT-based methods are contributing to complementing previous knowledge without damaging the bone. Even though these methods have been proved to be useful to understand adult variation, we do not know whether these methods are useful to cover ontogenetic variation. This work compares classical histological methods with medical- and micro-CT to quantify the amount of mineral area at the rib midshaft (% Min. Ar.), a proxy for bone density. We compared cross-sections from an ontogenetic sample of 14 human first ribs ranging from perinates to adults using a) classical histology, b) HD (9-17 microns) and SD micro-CT (90 microns), and c) standard medical-CT (0.66 mm). We found that all the CT-based methods provide a larger % Min. Ar. compared to the histological techniques, but the HD micro-CT resolution is the only capable of producing results comparable to classical histology (p > 0.01), with the SD micro-CT and the medical-CT producing statistically larger results compared to classical histology (p < 0.01). In addition, it is important to state that the resolution of a standard medical-CT is not high enough to differentiate between mineral and non-mineral areas of the cross-sections for perinates and infants. These results could have important implications to avoid (when necessary) destructive techniques that are not appropriate in the case of highly valuable specimens such as fossils.

Neanderthal child's maxilla from Baume Moula-Guercy (Soyons, Ardèche, France).

This article provides an ontogenetically-based comparative description of the Guercy 3 partial child's maxilla with Rdm2 -RM1 and unerupted RI2 -RP4 from Baume Moula-Guercy (MIS 5e) and examines its affinities to European and Middle Eastern Middle-to-Late Pleistocene (≈MIS 14-MIS 1) Homo. Description of the Guercy 3 maxilla and dentition (7.0 year ± 0.9 month) is based on observations of original fossils, casts, CT scans, literature descriptions, and virtual reconstructions. Our ontogenetic sample comprises a Preneanderthal-Neanderthal group and a Homo sapiens group. These groups are subdivided into (1) Preneanderthals (≈MIS 14-9), Early Neanderthals (MIS 7-5e), and Late Neanderthals (MIS 5d-3), and (2) Middle (MIS 5), Upper (MIS 3-2), and Late Upper Paleolithic (≈MIS 1), and recent H. sapiens. Standard techniques were employed for measurements and developmental age determinations.The Guercy 3 maxilla lacks changes found in Late Neanderthals, including the positioning of the root of the zygomatic process, infraorbital and nasal plates, premaxilla, buccal and labial alveolus, maxillary sinus, nasal cavity, and verticality of anterior tooth implantation. The morphology of the Guercy 3 maxilla more closely approximates that of Sima de los Huesos Preneanderthals, while the dentition more closely approximates the Early-Late Neanderthal condition. Maxillary remains of children and juveniles between MIS 14-MIS 5e are rare, and the available sample is fragmentary and distorted. Although fragmentary, the Guercy 3 maxilla is undistorted and provides new insights into the evolution of the midface in Neanderthals.

Icex: Advances in the automatic extraction and volume calculation of cranial cavities.

The use of non-destructive approaches for digital acquisition (e.g. computerised tomography-CT) allows detailed qualitative and quantitative study of internal structures of skeletal material. Here, we present a new R-based software tool, Icex, applicable to the study of the sizes and shapes of skeletal cavities and fossae in 3D digital images. Traditional methods of volume extraction involve the manual labelling (i.e. segmentation) of the areas of interest on each section of the image stack. This is time-consuming, error-prone and challenging to apply to complex cavities. Icex facilitates rapid quantification of such structures. We describe and detail its application to the isolation and calculation of volumes of various cranial cavities. The R tool is used here to automatically extract the orbital volumes, the paranasal sinuses, the nasal cavity and the upper oral volumes, based on the coordinates of 18 cranial anatomical points used to define their limits, from 3D cranial surface meshes obtained by segmenting CT scans. Icex includes an algorithm (Icv) for the calculation of volumes by defining a 3D convex hull of the extracted cavity. We demonstrate the use of Icex on an ontogenetic sample (0-19 years) of modern humans and on the fossil hominin crania Kabwe (Broken Hill) 1, Gibraltar (Forbes' Quarry) and Guattari 1. We also test the tool on three species of non-human primates. In the modern human subsample, Icex allowed us to perform a preliminary analysis on the absolute and relative expansion of cranial sinuses and pneumatisations during growth. The performance of Icex, applied to diverse crania, shows the potential for an extensive evaluation of the developmental and/or evolutionary significance of hollow cranial structures. Furthermore, being open source, Icex is a fully customisable tool, easily applicable to other taxa and skeletal regions.

Mugharet el'Aliya: Affinities of an enigmatic north African Aterian maxillary fragment

AbstractObjectivesThis study uses a virtual framework to examine the left maxillary fragment of the juvenile fossil from Mugharet el'Aliya, Morocco, found in association with an Aterian lithic industry. Previously, this fossil had been ascribed to modern humans or the Neanderthal lineage based on its “archaic”/“Neanderthal‐like” features and apparent large size. Here, we conducted a novel 3D shape comparative analysis of the maxillary fragment to clarify its taxonomic affinities with regard to its size and ontogeny.Materials and MethodsEighty Computed Tomography and surface scans representing ontogenetic samples of Homo sapiens and Homo neanderthalensis were used to capture species‐specific differences. The toolkit of geometric morphometrics in combination with surface registration and an elastic iterative closest point algorithm were used to create a dataset of meshes with an identical number of corresponding vertices for the maxillae. Multivariate statistics were applied to Procrustes superimposed coordinates derived from the vertices of this dataset.ResultsOur analysis showed affinities of the Mugharet el'Aliya individual with our H. sapiens sample, especially with a subadult individual from Qafzeh. No size‐independent affinities with Neanderthals of comparable dental age could be identified.DiscussionOur results add to the evidence connecting fossils from western Asia, especially Qafzeh and Skhul, and the North African Aterian. Furthermore, Mugharet el'Aliya adds to our knowledge of the ontogenetic development of adult morphology that is frequently used to characterize hominin groups, for example, Neanderthals and modern humans.

Do femoral biomechanical properties follow locomotor changes in primates? An ontogenetic study of olive baboons (Papio anubis)

AbstractObjectivesThe locomotor repertoire of the olive baboon (Papio anubis) changes during ontogeny from a diversified pattern in infancy to a stereotyped pattern in adults. On the assumption that the femoral diaphysis adapts to variations in the loading regime, we aimed to evaluate the impact of locomotor changes on femoral biomechanical properties during the ontogeny of olive baboons.Materials and MethodsWe used the cross‐sectional geometry of 50 three‐dimensional‐reconstructed olive baboon femora of an ontogenetic sample including individuals from birth to 28 years of age and belonging to a single social group. Cross section parameters were extracted, and cortical thickness maps were produced from 20% to 80% of the femoral length.ResultsNewborns present a distribution of cortical thickness that is longitudinally symmetric and anteroposterior shaped cross sections at midshaft. From this condition, infants, juveniles and adults femoral diaphyses are all characterized by a proximal shift in cortical thickness and a mediolateralization of bending rigidity and strength at midshaft.DiscussionAs soon as locomotor autonomy is established and despite a combination of several significant locomotor modes, the biomechanical pattern remains stable during ontogeny. Our results do not reflect the changes in locomotor repertoires that occur during ontogeny of Papio anubis. We therefore advise caution when inferring complex locomotor behavior from femoral biomechanical properties.

Thoracopelvic Covariation Across Ontogeny in Humans

Clarifying human thoracopelvic covariation patterns can contribute to an understanding of body shape evolution. Previous research has shown that although adult human males and females share a common thoracopelvic covariation pattern, males tend to exhibit mediolaterally wide thoraces and narrow pelves, and females tend to exhibit mediolaterally narrow thoraces and wide pelves (2020 Am J Phys Anthropol 173(3) 514‐534). The current study tests for sex differences in thoracopelvic covariation across ontogeny.I analyzed decedent computed tomography data from the Center for Forensic Imaging at the University of New Mexico with a sample of 44 females and 48 males, aged 0‐21 years. I used SlicerMorph to collect three‐dimensional landmark coordinate data representing thoracic and pelvic shapes as well as R geomorph and Morpho for geometric morphometric analyses. After separate Generalized Procrustes Analyses on the pelvis and thorax, I analyzed thoracopelvic covariation with two‐block partial least squares analysis. To compare covariation magnitudes, I tested effect sizes of sex‐specific two‐block partial least squares. I assessed sex‐specific covariation patterns by projecting the male data into the female two‐block partial least squares analysis and then comparing the slopes of sex‐specific data via major axis regressions and the smatr R package.Results from the two‐block partial least squares analyses indicate significant covariation between the thorax and pelvis in females and males (p=0.001). The first latent variables explain 94.47% and 94.40% of the total covariation in the female and male samples, respectively. In both sexes, as the thorax becomes less pyramidal and more barrel‐shaped with development, the pelvis becomes more anteroposteriorly elongated. The sex‐specific two‐block partial least squares analyses do not exhibit significantly different magnitudes of thoracopelvic covariation. Slope comparison between sexes does not indicate significantly different patterns of thoracopelvic covariation.Previous research suggests that adult thoracopelvic covariation is driven by sex differences. The current study shows that subadult thoracopelvic covariation tracks with growth and development in both sexes, which is expected in the ontogenetic sample. Subadult females and males do not exhibit significantly different magnitudes nor patterns of thoracopelvic covariation. Processes such as sagittal balance of the upper body over the pelvis may influence thoracopelvic covariation.

Growth and development of trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata) reflects locomotor behavior, life history, and neuromuscular development.

Bone structure dynamically adapts to its mechanical environment throughout ontogeny by altering the structure of trabecular bone, the three‐dimensional mesh‐like structure found underneath joint surfaces. Trabecular structure, then, can provide a record of variation in loading directions and magnitude; and in ontogenetic samples, it can potentially be used to track developmental shifts in limb posture. We aim to broaden the analysis of trabecular bone ontogeny by incorporating interactions between ontogenetic variation in locomotor repertoire, neuromuscular maturation, and life history. We examine the associations between these variables and age‐related variation in trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata). We used high‐resolution micro‐computed tomography scanning to image the calcaneus in a cross‐sectional sample of 34 juvenile M. fuscata aged between 0 and 7 years old at the Primate Research Institute, Japan. We calculated whole bone averages of standard trabecular properties and generated whole‐bone morphometric maps of bone volume fraction and Young’s modulus. Trabecular structure becomes increasingly heterogeneous in older individuals. Bone volume fraction (BV/total volume [TV]) decreases during the first month of life and increases afterward, coinciding with the onset of independent locomotion in M. fuscata. At birth, primary Young’s modulus is oriented orthogonal to the ossification center, but after locomotor onset bone structure becomes stiffest in the direction of joint surfaces and muscle attachments. Age‐related variation in bone volume fraction is best predicted by an interaction between the estimated percentage of adult brain size, body mass, and locomotor onset. To explain our findings, we propose a model where interactions between age‐related increases in body weight and maturation of the neuromuscular system alter the loading environment of the calcaneus, to which the internal trabecular structure dynamically adapts. This model cannot be directly tested based on our cross‐sectional data. However, confirmation of the model by longitudinal experiments and in multiple species would show that trabecular structure can be used both to infer behavior from fossil morphology and serve as a valuable proxy for neuromuscular maturation and life history events like locomotor onset and the achievement of an adult‐like gait. This approach could significantly expand our knowledge of the biology and behavior of fossil species.

Development of bipedal walking in olive baboons, Papio anubis: A kinematic analysis.

Although extant nonhuman primates are not habitual bipeds, they are able to walk bipedally from an early age. In humans, children improve their walking skills through developmental processes and learning experience. In nonhuman primates, infants do not routinely experience bipedalism and their musculoskeletal system gradually specializes for other locomotor modes. The aim of this study is to explore the development of occasional bipedal walking in olive baboon and to test whether the postural adjustments change with age. We collected kinematics and spatiotemporal parameters of bipedal gait in an ontogenetic sample of 24 baboons. Data were collected at the primatology station of the CNRS (France) and a total of 47 bipedal strides were extracted for the present analysis. Adults and adolescents walk bipedally in the same way, and the average kinematic pattern is similar across the age-classes. Infants walk bipedally with longer duty factor, they present larger movement amplitude of the thigh and the amplitude of the knee joint decreases with speed. In contrast, older baboons increase the amplitude of the knee and ankle joints with speed. In a non-adapted biped, the postural adjustments of bipedal walking vary with age. In infant baboons, the balance requirements are likely to be higher and these are solved by adopting a "blocking strategy". In older baboons, the postural adjustments are focused on the lower limb and the movements increase with speed. These results may echo, in some respects, the developmental sequence of the intersegmental coordination described in the ontogeny of human locomotion.

Quantifying maxillary development in chimpanzees and humans: An analysis of prognathism and orthognathism at the morphological and microscopic scales

Facial orientation (projection and degree of prognathism) and form in hominins is highly variable, likely related to evolutionary modifications of the microscopic process of bone modeling (the simultaneous cellular activities of bone formation and resorption) during ontogeny. However, in anteriorly projected faces such as those of early hominins, little is known about the link between bone modeling and facial developmental patterns. Similarly, these aspects have been infrequently investigated in extant great apes. In this study, quantitative methods were applied to a cross-sectional ontogenetic sample of 33 chimpanzees (Pan troglodytes verus) and 59 modern humans (Homo sapiens) to compare the development of maxillary prognathism to orthognathism at both microscopic and macroscopic (or morphological) scales using surface histology and geometric morphometric techniques. Chimpanzees express on average lower amounts of bone resorption than humans on the maxillary periosteum throughout ontogeny; however, the premaxilla is consistently resorbed from early stages on. The presence of bone resorption in the chimpanzee premaxilla, such as that seen in some early hominins, suggests a more ape-like pattern of maxillary bone modeling in these specimens. However, this shows that similarities in bone modeling patterns can lead to variations in shape, suggesting that other aspects of facial growth (such as modifications of rates and timings of development, as well as sutural growth) also played a crucial role in facial evolution.

Long bone histomorphogenesis of the naked mole-rat: Histodiversity and intraspecific variation.

Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole-rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists. Here, we examined a large ontogenetic sample (n=76) of subordinate individuals to assess the pattern of bone growth and bone microstructure of fore- and hindlimb bones by using histomorphological techniques. Over 290 undecalcified thin cross-sections from the midshaft of the humerus, ulna, femur, and tibia from pups, juveniles and adults were analyzed with polarized light microscopy. Similar to other fossorial mammals, NMRs exhibited a systematic cortical thickening of their long bones, which clearly indicates a conserved functional adaptation to withstand the mechanical strains imposed during digging, regardless of their chisel-tooth predominance. We describe a high histodiversity of bone matrices and the formation of secondary osteons in NMRs. The bones of pups are extremely thin-walled and grow by periosteal bone formation coupled with considerable expansion of the medullary cavity, a process probably tightly regulated and adapted to optimize the amount of minerals destined for skeletal development, to thus allow the female breeder to produce a higher number of pups, as well as several litters. Subsequent cortical thickening in juveniles involves high amounts of endosteal bone apposition, which contrasts with the bone modeling of other mammals where a periosteal predominance exists. Adults have bone matrices predominantly consisting of parallel-fibered bone and lamellar bone, which indicate intermediate to slow rates of osteogenesis, as well as the development of poorly vascularized lamellar-zonal tissues separated by lines of arrested growth (LAGs) and annuli. These features reflect the low metabolism, low body temperature and slow growth rates reported for this species, as well as indicate a cyclical pattern of osteogenesis. The presence of LAGs in captive individuals was striking and indicates that postnatal osteogenesis and its consequent cortical stratification most likely represents a plesiomorphic thermometabolic strategy among endotherms which has been suggested to be regulated by endogenous rhythms. However, the generalized presence of LAGs in this and other subterranean taxa in the wild, as well as recent investigations on variability of environmental conditions in burrow systems, supports the hypothesis that underground environments experience seasonal fluctuations that may influence the postnatal osteogenesis of animals by limiting the extension of burrow systems during the unfavorable dry seasons and therefore the finding of food resources. Additionally, the intraspecific variation found in the formation of bone tissue matrices and vascularization suggested a high degree of developmental plasticity in NMRs, which may help explaining the polymorphism reported for this species. The results obtained here represent a valuable contribution to understanding the relationship of several aspects involved in the morphogenesis of the skeletal system of a mammal with extraordinary adaptations.

Intraspecific variability in human maxillary bone modeling patterns during ontogeny.

This study compares the ontogenetic bone modeling patterns of the maxilla to the related morphological changes in three human populations to better understand how morphological variability within a species is established during ontogeny at both micro- and macroscopic levels. The maxillary bones of an ontogenetic sample of 145 subadult and adult individuals from Greenland (Inuit), Western Europe (France, Germany, and Portugal), and South Africa (Khoekhoe and San) were analyzed. Bone formation and resorption were quantified using histological methods to visualize the bone modeling patterns. In parallel, semilandmark geometric morphometric techniques were used on 3D models of the same individuals to capture the morphological changes. Multivariate statistics were applied and shape differences between age groups were visualized through heat maps. The three populations show differences in the degree of shape change acquired during ontogeny, leading to divergences in the developmental trajectories. Only subtle population differences in the bone modeling patterns were found, which were maintained throughout ontogeny. Bone resorption in adults mirrors the pattern found in subadults, but is expressed at lower intensities. Our data demonstrate that maxillary morphological differences observed in three geographically distinct human populations are also reflected at the microscopic scale. However, we suggest that these differences are mostly driven by changes in rates and timings of the cellular activities, as only slight discrepancies in the location of bone resorption could be observed. The shared general bone modeling pattern is likely characteristic of all Homo sapiens, and can be observed throughout ontogeny.

Revised estimates of Taung’s brain size growth

Cranial capacity, a proxy for the volume of the brain and associated cranial contents, is an important yardstick used to compare early hominin species because increasing brain size is a key characteristic of our lineage. In 1925, Raymond Dart claimed that a natural endocast found at the Buxton Limeworks near Taung, South Africa (which he named Australopithecus africanus), showed signs of neural reorganisation, but its juvenile status complicated comparison to other hominoid species. In an attempt to put its brain size and reorganisation into a comparative context, subsequent researchers have tried to estimate Taung’s adult cranial capacity by comparison to coarse-grained hominoid growth data. In this study, we simulated brain growth in A. africanus using asymptotic growth models in known-age mountain gorillas, chimpanzees and modern humans, and show that, at just under 4 years old, Taung’s brain had already finished or nearly finished growing according to hominoid developmental schedules. Percentage-growth remaining estimates are lower here than in previous studies using cross-sectional ontogenetic samples of unknown chronological age. Our new adult estimates (between 404 cm3 and 430 cm3 overall and 405–406 cm3 for chimpanzee models) are smaller than previous estimates with a ‘starting’ cranial capacity of 404 cm3, supporting the hypothesis that Taung’s adult brain size would have fallen toward the lower end of the A. africanus range of variation and strengthening the case that Taung was female.&#x0D; Significance:&#x0D; &#x0D; This is one of several recent studies to show that brain growth is completed in African apes and humans earlier than previously appreciated.&#x0D; New adult cranial capacity estimates for Taung are lower than previous estimates, supporting the hypothesis that Taung was female.&#x0D; Cessation of brain growth in hominoids at earlier ages than previously reported suggests that adult cranial capacities for hominin juvenile specimens have been overestimated.&#x0D; &#x0D; Open data set:&#x0D; http://dx.doi.org/10.17632/wyfvwd4s22

Modeling the effect of brain growth on cranial bones using finite-element analysis and geometric morphometrics.

Brain expansion during ontogeny has been identified as a key factor for explaining the growth pattern of neurocranial bones. However, the dynamics of this relation are only partially understood and a detailed characterization of integrated morphological changes of the brain and the neurocranium along ontogeny is still lacking. The aim of this study was to model the effect of brain growth on cranial bones by means of finite-element analysis (FEA) and geometric morphometric techniques. First, we described the postnatal changes in brain size and shape by digitizing coordinates of 3D semilandmarks on cranial endocasts, as a proxy of brain, segmented from CT-scans of an ontogenetic sample. Then, two scenarios of brain growth were simulated: one in which brain volume increases with the same magnitude in all directions, and other that includes the information on the relative expansion of brain regions obtained from morphometric analysis. Results indicate that in the first model, in which a uniform pressure is applied, the largest displacements were localized in the sutures, especially in the anterior and posterior fontanels, as well as the metopic suture. When information of brain relative growth was introduced into the model, displacements were also concentrated in the lambda region although the values along both sides of the neurocranium (parietal and temporal bones) were larger than under the first scenario. In sum, we propose a realistic approach to the use of FEA based on morphometric data that offered different results to more simplified models.

The chondrocranial key: Development of the sphenoid bone in primates

It has been hypothesized that the human sphenoid bone is uniquely truncated, which in turn contributes to a reduction of forward midfacial growth. If so, the perinatal fusion of the intrasphenoidal synchondrosis (ISS) in humans may contribute to midfacial reduction. However, there is a lack of detailed knowledge on sphenoid development of non‐human primates. In this study, orientation and direction of growth of basicranial interface with the midface of late prenatal and early postnatal sphenoid development was examined in ontogenetic samples of primates including three species of monkeys (n = 25) and four species of lemurs and bushbabies (strepsirrhines; n= 28). Micro‐computed tomographic (CT) and histological methods were used to track cross‐sectional age changes in the sphenoid bone. In monkeys (Saguinus spp.), histological findings indicated the number of proliferating chondrocytes is reduced across age leading to a reduction in absolute anteroposterior length of the proliferating zone. Preliminary data from micro‐CT reconstructions suggest that absolute length of the ISS decreases more rapidly in monkeys than in strepsirrhines. Measurements of presphenoid (PS) and basisphenoid (BS) length indicate that in strepsirrhines, these bones grow similarly to one another as cranial length increases. In contrast, in monkeys, the PS increases at a faster pace (i.e. higher linear regression line slopes) than the BS. However, unlike humans, the monkeys studied have prolonged postnatal patency of the ISS. Thus, the reduced midfacial projection in humans and these monkeys cannot be explained by the timing of ISS fusion alone. Dichotomous growth patterns of the cranial base and midface among primates suggest different patterns of regional integration of the cranium. In particular, our results suggest that in monkeys, integration of the midface is stronger with the anterior compared to the posterior portion of the sphenoid bone. In strepsirrhines by comparison, growth of the midface progressively deviates from that of the sphenoid bone over time.Support or Funding InformationNSF; grant numbers BCS‐1830894, BCS‐1830919, BCS‐0959438

The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus

Many studies pertaining to the masticatory apparatus have focused on the mandibular adductors (the temporalis, masseter, and medial pterygoid) ‐ the muscles that work cooperatively to produce bite force. Specifically, the architectural properties of these muscles have been correlated with diet. For instance, felids that eat relatively large prey have relatively longer fascicles to allow for the necessary gape. Primate diet also correlates with muscle architecture and, in some instances (e.g., tree gouging in Callithrix), the mode of foraging. However, there is little known about the ontogenetic development of these muscles. To characterize age‐related changes, we used an intraspecific sample of 28 specimens from a captive colony, spanning the entire lifespan of the small Malagasy primate, Microcebus murinus.We dissected each of the jaw adductors and obtained their masses as well as linear morphometrics. We then chemically dissected them using 35% nitric acid for 15–30 hours until their constituent fascicles could be separated. Then the reaction was neutralized in 50% glycerol and fascicles were photographed and measured using ImageJ (NIH) and all logged variables were statistically analyzed in JMP (SAS).A quadratic curvilinear model is significant when muscle mass is regressed against age with p‐values &lt;0.01 for each adductor. The trends demonstrate that the muscle mass of the adductors peak during early to mid‐adulthood with a point of inflection occurring at late adulthood to early senescence. When physiological cross‐sectional area (PCSA) is scaled against age, a quadratic model represents the data significantly better for the masseter and medial pterygoid with p‐values &lt;0.01. However, a linear model is more appropriate when characterizing changes in the PCSA of temporalis as the quadratic model was found to be insignificant. The general trend for changes in PCSA for masseter and medial pterygoid are consistent with the patterns observed in muscle mass, but temporalis PCSA does not appear to atrophy significantly with age. When fiber length is scaled against age for each mandibular adductor, the curvilinear relationship was observed to be a good fit with p‐values &lt;0.05. However, for the temporalis and medial pterygoid this trend appears to be driven by the inclusion of a low outlier. When this specimen is excluded, the trend line is horizontal suggesting that, once fiber length reaches maximum length early in life, it remains relatively constant. The trend for medial pterygoid also suggests that fiber length peaks early in life; however, it also indicates a point of inflection occurring in early adulthood.From these results, representing the most complete ontogenetic sample of primate masticatory muscle architecture, we have successfully characterized myological changes across the lifespan of M. murinus. Our findings suggest that the changes in PCSA are driven mostly by changes in muscle mass including growth through early adulthood and slight but clear reduction into senescence, while masticatory fascicle lengths remain surprisingly constant throughout life.Support or Funding InformationThis project was supported by the NSF (IOS‐15‐57125 and BCS‐14‐40599).This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Ontogenia de las órbitas en Pan troglodytes: implicancias estructurales, funcionales y evolutivas

Las órbitas de los primates Haplorrhini son particulares dentro de los mamíferos por estar completamente separadas de la fenestra temporal y rodeadas por hueso, ser convergentes, estar frontalizadas y proveer la base para el desarrollo de un notorio torus supraorbitario. Estas características han sido descriptas, algunas como adaptaciones al hábito de vida y otras como resultado de reacomodaciones estructurales de las matrices funcionales del cráneo. El objetivo de este trabajo es analizar los cambios morfológicos de las órbitas en una muestra ontogenética transversal de Pan troglodytes y su asociación con estructuras adyacentes a fin de discutir implicancias estructurales y funcionales. Se utilizaron 52 imágenes de tomografías computadas de cráneos de Pan troglodytes desde 8 meses de vida postnatal hasta adultos. Se registraron landmarks y se tomaron medidas volumétricas y lineales que permitieron extraer variables angulares y proporciones. Se realizó ANOVA, regresiones lineales y parciales y Análisis de Componentes Principales. Los resultados indican que los rasgos de valor adaptativo (funcionales) de la órbita de Pan troglodytes se establecen tempranamente en la ontogenia y no varían durante el período postnatal, mientras que su relación con estructuras adyacentes muestra importantes cambios.

Phylogenetic and environmental effects on limb bone structure in gorillas.

The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas. A total of 281 wild-collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas (G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross-sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development. Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals. Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.

Ontogeny of hallucal metatarsal rigidity and shape in the rhesus monkey (Macaca mulatta) and chimpanzee (Pan troglodytes).

Life history variables including the timing of locomotor independence, along with changes in preferred locomotor behaviors and substrate use during development, influence how primates use their feet throughout ontogeny. Changes in foot function during development, in particular the nature of how the hallux is used in grasping, can lead to different structural changes in foot bones. To test this hypothesis, metatarsal midshaft rigidity [estimated from the polar second moment of area (J) scaled to bone length] and cross-sectional shape (calculated from the ratio of maximum and minimum second moments of area, Imax /Imin ) were examined in a cross-sectional ontogenetic sample of rhesus macaques (Macaca mulatta; n = 73) and common chimpanzees (Pan troglodytes; n = 79). Results show the hallucal metatarsal (Mt1) is relatively more rigid (with higher scaled J-values) in younger chimpanzees and macaques, with significant decreases in relative rigidity in both taxa until the age of achieving locomotor independence. Within each age group, Mt1 rigidity is always significantly higher in chimpanzees than macaques. When compared with the lateral metatarsals (Mt2-5), the Mt1 is relatively more rigid in both taxa and across all ages; however, this difference is significantly greater in chimpanzees. Length and J scale with negative allometry in all metatarsals and in both species (except the Mt2 of chimpanzees, which scales with positive allometry). Only in macaques does Mt1 midshaft shape significantly change across ontogeny, with older individuals having more elliptical cross-sections. Different patterns of development in metatarsal diaphyseal rigidity and shape likely reflect the different ways in which the foot, and in particular the hallux, functions across ontogeny in apes and monkeys.

Shape analysis of spatial relationships between orbito-ocular and endocranial structures in modern humans and fossil hominids.

The orbits and eyes of modern humans are situated directly below the frontal lobes and anterior to the temporal lobes. Contiguity between these orbital and cerebral elements could generate spatial constraints, and potentially lead to deformation of the eye and reduced visual acuity during development. In this shape analysis we evaluate whether and to what extent covariation exists between ocular morphology and the size and spatial position of the frontal and temporal areas in adult modern humans. Magnetic resonance imaging (MRI) was used to investigate patterns of variation among the brain and eyes, while computed tomography (CT) was used to compare cranial morphology in this anatomical region among modern humans, extinct hominids and chimpanzees. Seventeen landmarks and semi-landmarks that capture the outline of the eye, frontal lobe, anterior fossa/orbital roof and the position of the temporal tips were sampled using lateral scout views in two dimensions, after projection of the average grayscale values of each hemisphere, with midsagittal and parasagittal elements overlapped onto the same plane. MRI results demonstrated that eye position in adult humans varies most with regard to its horizontal distance from the temporal lobes and, secondly, in its vertical distance from the frontal lobes. Size was mainly found to covary with the distance between the eye and temporal lobes. Proximity to these cerebral lobes may generate spatial constraints, as some ocular deformation was observed. Considering the CT analysis, modern humans vary most with regard to the orientation of the orbits, while interspecific variation is mainly associated with separation between the orbits and endocranial elements. These findings suggest that size and position of the frontal and temporal lobes can affect eye and orbit morphology, though potential effects on eye shape require further study. In particular, possible effects of these spatial and allometric relationships on the eye and vision should be examined using ontogenetic samples, vision parameters such as refractive error in diopters, and three-dimensional approaches that include measures of extraocular soft tissues within the orbit.