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 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.

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.

Lack of support for the association between facial shape and aggression: a reappraisal based on a worldwide population genetics perspective.

Antisocial and criminal behaviors are multifactorial traits whose interpretation relies on multiple disciplines. Since these interpretations may have social, moral and legal implications, a constant review of the evidence is necessary before any scientific claim is considered as truth. A recent study proposed that men with wider faces relative to facial height (fWHR) are more likely to develop unethical behaviour mediated by a psychological sense of power. This research was based on reports suggesting that sexual dimorphism and selection would be responsible for a correlation between fWHR and aggression. Here we show that 4,960 individuals from 94 modern human populations belonging to a vast array of genetic and cultural contexts do not display significant amounts of fWHR sexual dimorphism. Further analyses using populations with associated ethnographical records as well as samples of male prisoners of the Mexico City Federal Penitentiary condemned by crimes of variable level of inter-personal aggression (homicide, robbery, and minor faults) did not show significant evidence, suggesting that populations/individuals with higher levels of bellicosity, aggressive behaviour, or power-mediated behaviour display greater fWHR. Finally, a regression analysis of fWHR on individual's fitness showed no significant correlation between this facial trait and reproductive success. Overall, our results suggest that facial attributes are poor predictors of aggressive behaviour, or at least, that sexual selection was weak enough to leave a signal on patterns of between- and within-sex and population facial variation.

Early Holocene human remains from the Argentinean Pampas: additional evidence for distinctive cranial morphology of early South Americans.

The cranial morphology of Early Holocene American human samples is characterized by a long and narrow cranial vault, whereas more recent samples exhibit a shorter and wider cranial vault. Two hypotheses have been proposed to account for the morphological differences between early and late-American samples: (a) the migratory hypothesis that suggests that the morphological variation between early and late American samples was the result of a variable number of migratory waves; and (b) the local diversification hypothesis, that is, the morphological differences between early and late American samples were mainly generated by local, random (genetic drift), and nonrandom factors (selection and phenotypic plasticity). We present the first craniometric study of three early skulls from the Argentinean Pampas, dated ∼8,000 cal. years BP (Arroyo Seco 2, Chocorí, and La Tigra), and one associated with mega-faunal remains (Fontezuelas skull). In addition, we studied several Late Holocene samples. We show that the skulls from the Argentinean Pampas are morphologically similar to other Early Holocene American skulls (i.e., Lagoa Santa from Brazil, Tequendama, Checua, and Aguazuque from Colombia, Lauricocha from Peru, and early Mexicans) that exhibit long and narrow cranial vaults. These samples differ from the Late Holocene American samples that exhibit a shorter and wider cranial vault. Our results underscore the important differences in cranial morphology between early and late-American samples. However, we emphasize the need for further studies to discuss alternative hypotheses regarding such differences.

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.

Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution.

Evolutionary novelties in the skeleton are usually expressed as changes in the timing of growth of features intrinsically integrated at different hierarchical levels of development. As a consequence, most of the shape-traits observed across species do vary quantitatively rather than qualitatively, in a multivariate space and in a modularized way. Because most phylogenetic analyses normally use discrete, hypothetically independent characters, previous attempts have disregarded the phylogenetic signals potentially enclosed in the shape of morphological structures. When analysing low taxonomic levels, where most variation is quantitative in nature, solving basic requirements like the choice of characters and the capacity of using continuous, integrated traits is of crucial importance in recovering wider phylogenetic information. This is particularly relevant when analysing extinct lineages, where available data are limited to fossilized structures. Here we show that when continuous, multivariant and modularized characters are treated as such, cladistic analysis successfully solves relationships among main Homo taxa. Our attempt is based on a combination of cladistics, evolutionary-development-derived selection of characters, and geometric morphometrics methods. In contrast with previous cladistic analyses of hominid phylogeny, our method accounts for the quantitative nature of the traits, and respects their morphological integration patterns. Because complex phenotypes are observable across different taxonomic groups and are potentially informative about phylogenetic relationships, future analyses should point strongly to the incorporation of these types of trait.

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.

Growth of functional cranial components in rats submitted to intergenerational undernutrition.

The aim of the present study was to discover how intergenerational undernutrition affects the growth of major and minor functional cranial components in two generations of rats. Control animals constituted the parental generation (P). The undernourished generations (F1 and F2) were fed 75% of the control diet. Animals were X-rayed every 10 days from 20 to 100 days of age. The length, width and height of the major (neurocranium and splanchnocranium) and minor (anterior-neural, middle-neural, posterior-neural, otic, respiratory, masticatory and alveolar) cranial components were measured on each radiograph. Volumetric indices were calculated to estimate size variations of these components. Data were processed using the Kruskal-Wallis and Kolmogorov-Smirnov tests for two samples. Impairment in splanchnocranial and neurocranial growth was found, the latter being more affected than the former in F1. Comparison between F2 and F1 animals showed cumulative effects of undernutrition in both major and minor components (anterior-neural, respiratory, masticatory and alveolar in males, and middle-neural and respiratory in females). Such differential effects on minor components may reflect a residual mechanical strain resulting from the linkage between components. This phenomenon was clearly observed in the neurocranium and could be understood as an adaptive response to the demands of the associated functional matrices.

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.

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.

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.

Cranial growth in normal and low-protein-fed Saimiri. An environmental heterochrony.

Protein malnutrition has a significant and measurable effect on the rate and timing of growth. Heterochrony is generally viewed as the study of evolutionary changes in the relative rates and timing of growth and development. Although changes in growth commonly result from experimental manipulations of diet, nobody has previously attempted to explain such changes from a heterochronic perspective. We use a heterochronic perspective to compare a group of squirrel monkeys fed a low-protein diet to individuals on a high-protein diet, but, in contrast to previous works, we focus particularly on the effects of environmental and not genetic factors. In the present study, Gould's (1977) and Godfrey and Sutherland's (1996) methodologies for studying heterochrony, as well as geometric morphometrics, are used to compare two groups of Saimiri sciureus boliviensis. Two groups of Saimiri were constructed on the basis of the protein content in their diets: a high-protein group (HP) (N=12) and a low-protein group (LP) (N=12). All individuals are males born in captivity. Two major functional components of the skull, the neurocranium and the face, were analysed. Four minor components were studied in each major component. Comparison of craniofacial ontogeny patterns based on major and minor components suggests that changes in the skull of LP animals can be explained by heterochrony. The skull of LP animals exhibits isomorphism produced by proportioned dwarfism. Our results suggest that heterochrony can be environmentally, rather than exclusively genetically, induced. The study of genetic assimilation (Waddington, 1953, 1956; see Scharloo, 1991; Hallgrimsson et al., 2002) has demonstrated that environmentally induced phenotypes often have a genetic basis, and thus parallel changes can be easily induced genetically. It is possible that proportioned dwarfism is far more common than currently appreciated.

Functional-cranial approach to the influence of economic strategy on skull morphology.

Environmental factors are assumed to play an important role in the shaping of craniofacial morphology. Here we propose a statistical approach which can be of utility in estimating the magnitude and localization of a particular nongenetic factor upon the specific functional components of the skull. Our analysis is a combination of previous attempts of apportionment of variance and the application of craniofunctional theory. The effect of subsistence strategy on craniofacial functional components was studied on 18 populations of hunter-gatherers and farmers from South America. Results demonstrate that the environmental factors studied likely influenced the masticatory component's size and shape. Even when this effect is not large enough to clearly differentiate among subsistence strategies (since whole craniofacial variation among populations remains greater), the method used here provides interesting clues to localize plastic or adaptive responses to external stimuli.

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.

Sexual dimorphism and postnatal growth of intrauterine growth retarded rats.

The intrauterine growth retardation (IUGR) is a complex phenomenon since it causes variability in postnatal growth responses. The aim of the present study was to analyze the effects of lactational rehabilitation on body and cranial growth and sexual dimorphism in IUGR rats. IUGR model was carried out by means of uterine vessels bending in pregnant rats at the first day of pregnancy. Control and sham-operated animals were also included. During suckling, IUGR and sham-operated pups were cross-fostered to a control dam. The animals were x-rayed every four days, from birth to weaning. Body weight and length, and neural and facial variables were measured. The reduced placental blood flow delayed growth in pups. Facial growth was more impaired than the neural one. An incomplete catch up growth was found, since males reached sham values only in neurocranial height and females--except facial length and width--were similar to sham. Because of sex differences in growth recovery, normal sexual dimorphism in body and craniofacial pattern was not expressed in the IUGR group. This study suggests that reduced uteroplacental blood supply in the rat interferes with the full expression of normal dimorphism based on gender and confirms the impact of IUGR on postnatal growth.

Craniometric evidence for Palaeoamerican survival in Baja California.

A current issue on the settlement of the Americas refers to the lack of morphological affinities between early Holocene human remains (Palaeoamericans) and modern Amerindian groups, as well as the degree of contribution of the former to the gene pool of the latter. A different origin for Palaeoamericans and Amerindians is invoked to explain such a phenomenon. Under this hypothesis, the origin of Palaeoamericans must be traced back to a common ancestor for Palaeoamericans and Australians, which departed from somewhere in southern Asia and arrived in the Australian continent and the Americas around 40,000 and 12,000 years before present, respectively. Most modern Amerindians are believed to be part of a second, morphologically differentiated migration. Here we present evidence of a modern Amerindian group from the Baja California Peninsula in Mexico, showing clearer affinities with Palaeoamerican remains than with modern Amerindians. Climatic changes during the Middle Holocene probably generated the conditions for isolation from the continent, restricting the gene flow of the original group with northern populations, which resulted in the temporal continuity of the Palaeoamerican morphological pattern to the present.