Ontogenetic changes in cranial vault thickness in a modern sample of Homo sapiens.

OBJECTIVES: This work assesses cranial vault thickness (CVT) ontogenetic changes using a computed tomography database to register thickness across multiple regions. METHODS: Vault images of 143 individuals from 0 to 31 years old were analyzed by thickness semiautomatic measurements. For each individual, we obtained a thickness mean measure (TMM) and its coefficient of variation, a measure of endocranial volume (EV), the distribution of relative frequencies of thickness-relative frequency polygon, and a topographic mapping that shows the thickness arrangement through a chromatic scale. Ontogenetic changes of these variables were evaluated by different regression models (TMM vs. age, EV vs. age, TMM vs. EV) and visual comparisons between the age groups. RESULTS: TMM increased during ontogeny until the onset of adulthood without sex differences, but the most accelerated growth rates occur during the first 6 years of postnatal life. TMM variations were associated with EV only in infants and children, but not in later periods. The polygons showed a flattening during ontogeny, probably due to an increase in thickness variation within individuals. However, the adult pattern of thickness arrangement, with the lateral region thinner than the regions near sagittal plane, was detected from infancy. CONCLUSION: The pattern of thickness arrangement is established early in ontogeny but CVT increases and changes in distribution until adolescence. Several factors may influence CVT, such as the brain, muscles, vessels, and sutures.

Spatial patterns and evolutionary processes in southern South America: a study of dental morphometric variation.

The purpose of this article is to examine the patterns of evolutionary relationships between human populations from the later Late Holocene (1,500-100 years BP) of southern South America on the basis of dental morphometric data. We tested the hypotheses that the variation observed in this region would be explained by the existence of populations with different phylogenetic origin or differential action of gene flow and genetic drift. In this study, we analyzed permanent teeth from 17 samples of male and female adult individuals from throughout southern South America. We measured mesiodistal and buccolingual diameters at the base of the crown, along the cement-enamel junction. The results of multiple regression analysis and a mantel correlogram indicate the existence of spatial structure in dental shape variation, as the D(2) Mahalanobis distance between samples increases with increasing geographical distance between them. In addition, the correlation test results show a trend toward reduction of the internal variation of samples with increasing latitude. The detected pattern of dental variation agrees with the one expected as an outcome of founder serial effects related to an expansion of range during the initial occupation of southern South America.

Frontal sinus ontogeny and covariation with bone structures in a modern human population.

In humans, the frontal sinus (FS) is located in the medial part of the supraorbital region, sometimes expanded throughout the frontal squama. It exhibits high morphological variability, but its general form appears to be constrained by surrounding structures. The goal of this study is to analyze FS growth and test for covariation between FS volume and the glabellar region, upper nasal region, bone thickness and endocranial size in a human sample from Argentina. The sample comprises 149 reconstructions derived from computed tomography images of individuals aged 0-31 years. Volume of the FS and measurements of the surrounding structures were recorded. The FS growth trajectory was assessed by parametric and nonparametric methods, and covariation was determined using correlations and partial correlations. The FS volume could be measured at an age of about 6 years and older; adults had no aplasia but hyperplasia was found in some cases. Since the most conspicuous characteristic found was variation among individuals, the nonparametric smoothing spline produced very poor fitting. The modified logistic function was the only parametric method providing significant parameters. Sexes differed in the age at which FS growth began and ended, with FS developing earlier but at a slower rate in females than in males. The FS volume did not correlate with either upper nasal width or endocranial volume, but it correlated with bone thickness measurements (mainly from the glabellar region), even when age was held constant. Expansion of the FS at the frontal poles also correlated with frontal bone thickness. Despite the difficulty in modeling and predicting the trajectory and morphology of FS, our results suggest that it is affected by its surrounding bony environment.

Variation of functional cranial components in six Anthropoidea species.

Sixty male crania from three Platyrrhini and three Catarrhini genera were measured by means of the craniofunctional method. The aim was to analyze functional components of the skull and relate their function and the degree of encephalization to life history variables. We recognized two major and eight minor functional components. The objectives were to test (1) if within-taxa (Platyrrhini or Catarrhini) and/or between-taxa (Platyrrhini and Catarrhini) comparisons showed minor-component differentiation; and (2) if encephalization affects both primate groups differently. After standardization by size and scaling, 15 possible within-taxa and between-taxa comparisons were made. We found a strong phylogenetic signal, i.e., cranial differences were not randomly distributed, with the between-taxa variation being greater than within-taxa. Both hypotheses tested were accepted since: (1) There was no random variation between functional cranial components. They followed definite patterns for ancestral and derived traits. (2) Encephalization was present in all scaled comparisons, with Platyrrhini showing a higher degree of encephalization than Catarrhini. We conclude that major and minor craniofunctional components should be considered as correlated traits related to life history, because we found different patterns between platyrrhines and catarrhines, and within species of both taxa.

East-West cranial differentiation in pre-Columbian human populations of South America.

South Amerindians are frequently thought of as a rather biologically homogeneous megapopulation. However, when native South Americans are assessed by information coming from DNA variability analysis, they resolve into two, major distinct entities of Eastern and Western zones. The purpose of this study is to investigate if the same dual pattern emerges from craniometric data. We approached this question by means of functional craniometric variables. We found strong evidence that Westerners and Easterners constitute two distinct and independent microevolutionary universes when cranial morphology is assessed. The existence of a third universe, Northwest, cannot be completely ruled out, but needs further investigation. We also discovered that Westerners and Easterners present similar degrees of internal variation, contrary to the findings of geneticists and molecular biologists. Palaeoamericans seem to be more similar to Easterners than to Westerners and North-Westerners. Our results suggest that this East-West cranial differentiation is more probably the result of differential rates of genetic drift and gene flow acting on each side of the Cordillera. However, different intensities of gene flow between Palaeoamericans and Amerindians in the highlands and in the lowlands cannot be completely dismissed as a possible explanation for the differentiation found.

Morphological Integration of the Orbital Region in a Human Ontogenetic Sample.

Most studies on craniofacial morphology have focused on adult individuals, but patterns of variation are the outcome of genetic and epigenetic variables that interact throughout ontogeny. Among cranial regions, the orbits exhibit morphological variation and occupy an intermediate position between neurocranial and facial structures. The main objective of this work was to analyze postnatal ontogenetic variation and covariation in the morphology of the orbital region in a cross-sectional series of humans from 0 to 31 years old. Landmarks and semilandmarks were digitized on the orbital rim, as well as in neighboring neural and facial structures. Data were analyzed using geometric morphometrics. Results indicated that orbital size increases during the first years of postnatal life, while the shape of the orbital aperture does not change significantly with age. In general, the pattern and magnitude of shape covariation do not vary markedly during postnatal life although some subtle shifts were documented. Additionally, the shape of the orbital aperture is more related to the anterior neurocranium than to zygomatic structures, even when the allometry is adjusted. Although we expected some influence from postnatal craniofacial growth and from some functional factors, such as mastication, on the development of the orbits, this assumption was not completely supported by our results. As a whole, our findings are in line with the prediction of an early influence of the eyes and extraocular tissues on orbital morphology, and could be interpreted in relation to processes promoting early neural development that coordinately affects orbital traits and the neurocranial skeleton.

Developmental covariation of human vault and base throughout postnatal ontogeny.

In the present study, we analyzed postnatal ontogenetic integration among morphological traits of the human neurocranium. Particularly, the covariation between the vault and the base during postnatal life was assessed. Since the association between these regions may depend on the generalized change produced by allometry, we tested its effect on their covariation. On a sample of adults and subadults ranging from 0 to 31 years, 3D coordinates of neurocranial landmarks and semilandmarks were digitized and geometric morphometric technics were applied. Main aspects of shape variation were examined using Principal Components analysis. Covariation between the vault and the base was examined by Partial Least Squares analysis. According to our results, the vault and the base covary strongly during postnatal ontogeny and their relation depends largely on allometry. Two size variables were studied: centroid size, which was obtained from the recorded morphometric points, and endocranial volume, taken as an estimation of brain size. Although growing brain was found to be a developmental process that contributes to covariation among neurocranial traits, there would be other factors that exert their influence during ontogeny. These results lead to reconsider cranial morphological evolution taking into account the developmental constraints given by ontogenetic patterns of integration and reinforcing the idea that in human evolution a suite of relevant characters may be fuelled by few developmental processes.

Ontogenetic patterns of morphological variation in the ectocranial human vault.

The skull is considered a modular structure in which different parts are influenced by different factors and, as a result, achieve adult shape at different ages. Previous studies have suggested that the basicranium presents a modular pattern that distinguishes sagittal and lateral parts, probably affected by the brain and masticatory structures, respectively. The vault of modern humans, in contrast, has been considered as a highly integrated system mainly influenced by brain growth. Here, we explored developmental shape variation in sagittal and lateral ectocranial vault in humans in order to assess if both regions are ontogenetically dissociated. We used a sample of 135 cranial computed tomography images from 0 to 31 ages. Landmarks and semilandmarks were collected on sagittal and lateral regions and geometric morphometric techniques were applied separately for each region. On the shape coordinates, we used Goodall's F-test in order to assess the age when the adult configuration is attained. Principal component analysis enabled us to evaluate shape variation during ontogeny. Results indicated that both sagittal and lateral structures attain adult shape at early adolescence. Both regions express coordinated shape modifications probably due to shared developmental factors. It is concluded that masticatory muscles may not exert a strong enough influence to produce independent variation in the lateral traits. Thus, it is likely that the brain integrates sagittal and lateral parts of the vault across human ontogeny.

Different cranial ontogeny in Europeans and Southern Africans.

Modern human populations differ in developmental processes and in several phenotypic traits. However, the link between ontogenetic variation and human diversification has not been frequently addressed. Here, we analysed craniofacial ontogenies by means of geometric-morphometrics of Europeans and Southern Africans, according to dental and chronological ages. Results suggest that different adult cranial morphologies between Southern Africans and Europeans arise by a combination of processes that involve traits modified during the prenatal life and others that diverge during early postnatal ontogeny. Main craniofacial changes indicate that Europeans differ from Southern Africans by increasing facial developmental rates and extending the attainment of adult size and shape. Since other studies have suggested that native subsaharan populations attain adulthood earlier than Europeans, it is probable that facial ontogeny is linked with other developmental mechanisms that control the timing of maturation in other variables. Southern Africans appear as retaining young features in adulthood. Facial ontogeny in Europeans produces taller and narrower noses, which seems as an adaptation to colder environments. The lack of these morphological traits in Neanderthals, who lived in cold environments, seems a paradox, but it is probably the consequence of a warm-adapted faces together with precocious maturation. When modern Homo sapiens migrated into Asia and Europe, colder environments might establish pressures that constrained facial growth and development in order to depart from the warm-adapted morphology. Our results provide some answers about how cranial growth and development occur in two human populations and when developmental shifts take place providing a better adaptation to environmental constraints.

Measurement error of 3D cranial landmarks of an ontogenetic sample using Computed Tomography.

BACKGROUND/AIM: Computed Tomography (CT) is a powerful tool in craniofacial research that focuses on morphological variation. In this field, an ontogenetic approach has been taken to study the developmental sources of variation and to understand the basis of morphological evolution. This work aimed to determine measurement error (ME) in cranial CT in diverse developmental stages and to characterize how this error relates to different types of landmarks. MATERIAL AND METHODS: We used a sample of fifteen skulls ranging from 0 to 31 years. Two observers placed landmarks in each image three times. Measurement error was assessed before and after Generalized Procrustes Analysis. RESULTS: The results indicated that ME is larger in neurocranial structures, which are described mainly by type III landmarks and semilandmarks. In addition, adult and infant specimens showed the same level of ME. These results are specially relevant in the context of craniofacial growth research. CONCLUSION: CT images have become a frequent evidence to study cranial variation. Evaluation of ME gives insight into the potential source of error in interpreting results. Neural structures present higher ME which is mainly associated to landmark localization. However, this error is irrespective of age. If landmarks are correctly selected, they can be analyzed with the same level of reliability in adults and subadults.

Diversity among African pygmies.

Although dissimilarities in cranial and post-cranial morphology among African pygmies groups have been recognized, comparative studies on skull morphology usually pull all pygmies together assuming that morphological characters are similar among them and different with respect to other populations. The main aim of this study is to compare cranial morphology between African pygmies and non-pygmies populations from Equatorial Africa derived from both the Eastern and the Western regions in order to test if the greatest morphological difference is obtained in the comparison between pygmies and non-pygmies. Thirty three-dimensional (3D) landmarks registered with Microscribe in four cranial samples (Western and Eastern pygmies and non-pygmies) were obtained. Multivariate analysis (generalized Procrustes analysis, Mahalanobis distances, multivariate regression) and complementary dimensions of size were evaluated with ANOVA and post hoc LSD. Results suggest that important cranial shape differentiation does occur between pygmies and non-pygmies but also between Eastern and Western populations and that size changes and allometries do not affect similarly Eastern and Western pygmies. Therefore, our findings raise serious doubt about the fact to consider African pygmies as a homogenous group in studies on skull morphology. Differences in cranial morphology among pygmies would suggest differentiation after divergence. Although not directly related to skull differentiation, the diversity among pygmies would probably suggest that the process responsible for reduced stature occurred after the split of the ancestors of modern Eastern and Western pygmies.

East-West cranial differentiation in pre-Columbian populations from Central and North America.

In a recent study we found that crania from South Amerindian populations on each side of the Andes differ significantly in terms of craniofacial shape. Western populations formed one morphological group, distributed continuously over 14,000km from the Fuegian archipelago (southern Chile) to the Zulia region (northwestern Venezuela). Easterners formed another group, distributed from the Atlantic Coast up to the eastern foothills of the Andes. This differentiation is further supported by several genetic studies, and indirectly by ecological and archaeological studies. Some authors suggest that this dual biological pattern is consistent with differential rates of gene flow and genetic drift operating on both sides of the Cordillera due to historical reasons. Here we show that such East-West patterning is also observable in North America. We suggest that the "ecological zones model" proposed by Dixon, explaining the spread of the early Americans along a Pacific dispersal corridor, combined with the evolution of different population dynamics in both regions, is the most parsimonious mechanism to explain the observed patterns of within- and between-group craniofacial variability.

Developmental connections between cranial components and the emergence of the first permanent molar in humans.

The age of emergence of the first molar (M1) is a developmental event correlated with many variables of primate life history, such as adult brain size. The evolution of human life history is characterized by the inclusion of childhood, which takes place between weaning and M1 emergence. Children still depend on adults for nutrition due to their small digestive system and their immature brains. By contrast, juveniles are not dependent because of M1 emergence, which enables shifting to adult type diet, and attainment of nearly adult brain size. In this study, developmental connections between M1 emergence and growth of cranial components were explored in two ways in order to understand the developmental basis of their evolutionary connections: (1) differences in growth trajectories of cranial components with respect to M1 emergence and (2) differences between individuals with and without fully emerged M1. Growth of anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory and alveolar cranial components was analysed in human skulls of individuals aged 0-20 years and in an adult reference skull. Volumetric indices were calculated to estimate size. Two subsamples were selected in order to focus on the transition between deciduous and permanent dentition: those with full deciduous dentition and before M1 reaches the occlusal plane; and those who present M1 in full emergence and no other cheek-tooth at the occlusal plane. The principal results were as follows. (1) Trajectories fitted using the whole sample are characterized by an inflection point that takes place before M1 emergence for neural components and around M1 emergence for facial components. (2) Associations between growth and age tend to be strong in those with full deciduous dentition, and weak in those who present M1 in full emergence. (3) Individuals who present M1 in full emergence are larger than those with full deciduous dentition. (4) Growth of components linked to the central nervous system is not linear until M1 emergence. Individuals who present M1 in full emergence are only larger than individuals with full deciduous dentition by 4-5% of adult size. (5) The alveolar component does not show increments between full deciduous dentition and M1 emergence. (6) When volumetric indices were standardized by age, the growth trajectories of individuals with full deciduous dentition and of those with M1 were not decoupled. In general terms, M1 emergence does not show a strong association with growth of the components that may explain differences in life histories. However, the main changes in neural and alveolar components occur in the first 3 years of life, which may be developmentally connected with M1 crown formation.

Allometries throughout the late prenatal and early postnatal human craniofacial ontogeny.

Craniofacial shape changes throughout the late prenatal and early postnatal ontogeny (32-47 weeks of gestational age) were explored. The purpose was to evaluate whether the skull follows an allometric growth pattern, as was observed in other ontogenetic periods, and to assess shape variation patterns for the cranial vault, cranial base, and face. Thirty three-dimensional landmarks were registered in 54 skulls. Wire-frames were built with landmarks to observe shape variation in the following cranial components: anteroneural, midneural, posteroneural, optic, respiratory, masticatory, and alveolar. The landmark configurations were subjected to generalized Procrustes analyses, and the shape coordinates obtained were subjected to Principal Components Analyses. Multivariate regression of the shape variables (the principal components) on the size vector (the centroid size) was performed to assess allometries. Transformation grids were constructed to identify how cranial components interact across ontogeny. Results indicated that highly significant shape changes depend on size changes. Important shape variation in the vault, small variation in the cranial base, and no variation in the face were observed. Brain growth is proposed to be the major influence on craniofacial shape change, which produces a relative elongation and compression of midneural and posteroneural components. The cranial base elongates by intrinsic factors and affects position of the face. Ontogenetically, the cranial base seems to be independent with respect to brain growth, in contrast to what has been suggested in comparisons at higher taxonomic levels.

Craniofacial morphology in the Argentine Center-West: consequences of the transition to food production.

The Argentine Center-West was the southernmost portion of the Andes where domestication of plants and animals evolved. Populations located in the southern portion of this area displayed a hunter-gatherer subsistence economy up to historical times, and coexisted with farmers located to the north. Archaeological and biological evidence suggests that the transition to food production was associated with the consumption of a softer diet and a more sedentary way of life. This study tests the hypothesis that diet-related factors influenced morphological differentiation, by comparing functional cranial components of farmers and hunter-gatherers. Three-dimensional changes on eight minor functional components (anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory, and alveolar) were measured on skulls derived from both subareas. Volumetric and morphometric indices were calculated to estimate the absolute and relative size of components, respectively. Results of a paired t-test indicated that farmers have a smaller craniofacial size than hunter-gatherers. The components that varied the most were masticatory and posteroneural, showing smaller absolute and relative sizes in farmers. Discriminant analyses indicated that lengths and widths were the most affected dimensions of these and other components. The pattern of differentiation, which involves specific components, enabled us to exclude differential gene flow and stochastic mechanisms as the main causes. Instead, results support the hypothesis that diet-related factors associated with both subsistence economies influenced craniofacial morphology. A proportion of the observed variation associated with size differences can be explained by two systemic factors: the lesser quality of nutrition due to a low protein content in the diet, and a decrease of growth hormone circulation induced by a lower mobility due to sedentism. However, differentiation is better explained by a localized factor: the reduction in the masticatory and posteroneural components in farmers resulted from a decrease of masticatory stresses and workload on the head and neck, linked to the consumption of a softer diet.

A cross-sectional study of human craniofacial growth.

It is generally accepted that different cranial regions do not follow the same growth pattern. In this study, size changes of the functional cranial components (FCCs) in 228 human skulls of age at death between 0 and 20 years were evaluated. The skull is considered as divided into anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory and alveolar FCCs. Age-related changes of FCCs were assessed by fitting curves with the smoothing spline method, and quantifying the proportional increments at different stages. All FCCs show a high growth rate in the first 3-5 years of life. Two groups of growth trajectories can be distinguished. The anteroneural, midneural, posteroneural and optic FCCs are more advanced at all stages; they show a high growth rate before 3-5-years-old and a low rate later. This difference is less pronounced in the group comprising the respiratory, masticatory and otic FCCs. The alveolar FCC shows an independent pattern. The similarities among FCCs of the two groups are best explained by their common embryological origin. In contrast, the participation in a common function cannot be associated with the co-ordinated variation, given that the masticatory and alveolar FCCs show independent trajectories.

South Amerindian craniofacial morphology: diversity and implications for Amerindian evolution.

The most compelling models concerning the peopling of the Americas consider that modern Amerindians share a common biological pattern, showing affinities with populations of the Asian Northeast. The aim of the present study was to assess the degree of variation of craniofacial morphology of South American Amerindians in a worldwide context. Forty-three linear variables were analyzed on crania derived from American, Asian, Australo-Melanesian, European, South-Saharan African, and Polynesian regions. South America was represented by seven Amerindian samples. In order to understand morphologic diversity among Amerindians of South America, variation was estimated using regions and local populations as units of analysis. Variances and F(ST) values were calculated for each unit, respectively. Both analyses indicated that morphologic variation in Southern Amerindians is extremely high: an F(ST) of 0.01531 was obtained for Southern Amerindians, and values from 0.0371-0.1205 for other world regions. Some aspects linked to the time and mode of the peopling of the Americas and various microevolutionary processes undergone by Amerindians are discussed. Some of the alternatives proposed to explain this high variation include: a greater antiquity of the peopling than what is mostly accepted, a peopling by several highly differentiated waves, an important effect of genetic drift, and gene flow with Paleoamericans. A combination of some of these alternatives explains at least some of the variation.

The Neolithic transition in Europe and North Africa. The functional craneology contribution.

The origin and mode of the process that led to food production in Europe and North Africa is a matter intensively discussed. It is not clear in the transition to the Neolithic in these regions if it results by a migration of peoples from the Near East, by changes in the behaviour of local populations, or by an interaction of both processes. Morphological changes in Europe and North Africa, from the Upper Palaeolithic to modern periods were assessed. A method based on the Functional Matrix Hypothesis was carried out, which implies that the bone shape is modified by the related soft tissues. Absolute and relative size and shape changes were estimated on two major--neural and facial--and eight minor--anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory and alveolar--functional cranial components (FCC). ANOVA and Canonical Correlation analyses indicate that neither a temporal trend nor a pattern characteristic of each region is evidenced. But a shift is observed between the Upper Palaeolithic groups and the later samples. Size is greater in the Upper Palaeolithics. Shape is modified because Upper Palaeolithics have greater midneural and masticatory FCCs, and smaller optic FCC. The greater masticatory volume is associated to wider faces in hunter-gatherers. Our study cannot enable to conclude if the morphological shift is caused by a replacement or by a change in the local populations, however, the morphological changes can be attributed to the reduced mobility and the masticatory stress since the Neolithic period.