Phenotypic evolution of human craniofacial morphology after admixture: a geometric morphometrics approach

An evolutionary, diachronic approach to the phenotypic craniofacial pattern arisen in a human population after high levels of admixture and gene flow was achieved by means of geometric morphometrics. Admixture has long been studied after molecular data. Nevertheless, few efforts have been made to explain the morphological outcome in human craniofacial samples. The Spanish-Amerindian contact can be considered a good scenario for such an analysis. Here we present a comparative analysis of craniofacial shape changes observed between two putative ancestor groups, Spanish and precontact Aztecs, and two diachronic admixed groups, corresponding to early and late colonial periods from the Mexico's Central Valley. Quantitative shape comparisons of Amerindian, Spanish, and admixed groups were used to test the expectations of quantitative genetics for admixture events. In its simplest form, this prediction states that an admixed group will present phenotypic values falling between those of both parental groups. Results show that, in general terms, although the human skull is a complex, integrated structure, the craniofacial morphology observed fits the theoretical expectations of quantitative genetics. Thus, it is predictive of population structure and history. In fact, results obtained after the craniofacial analysis are in accordance with previous molecular and historical interpretations, providing evidence that admixture is a main microevolutionary agent influencing modern Mexican gene pool. However, expectations are not straightforward when moderate shape changes are considered. Deviations detected at localized structures, such as the upper and lower face, highlight the evolution of a craniofacial pattern exclusively inherent to the admixed groups, indicating that quantitative characters might respond to admixture in a complicated, nondirectional way.     

The Neanderthal taxonomic position: models of intra- and inter-specific craniofacial variation

The Neanderthal taxonomic position is a matter of wide disagreement among paleoanthropologists. Some workers consider this fossil human group to represent a different species, Homo neanderthalensis, while others see it as a subspecies of Homo sapiens. This study developed two models of morphological variation to be applied to a comparison between Neanderthals and modern humans: modern human populations provided a measure of intra-specific variation, while the species and subspecies of Pan provided measures of both intra- and inter-specific morphological differences. Although such an approach has been advocated strongly, it has not been systematically undertaken until recently. The techniques of geometric morphometrics were used to collect data in the form of three-dimensional coordinates of craniofacial landmarks. The data were processed using generalized procrustes analysis, and analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis and Mahalanobis D(2). The morphological distances between Neanderthals and modern humans, and between Neanderthals and Late Paleolithic/early anatomically modern specimens, are consistently greater than the distances among recent human populations, and greater than the distances between the two chimpanzee species. Furthermore, no strong morphological similarities were found between Neanderthals and Late Paleolithic Europeans. This study does not find evidence for Neanderthal contribution to the evolution of modern Europeans. Results are consistent with the recognition of Neanderthals as a distinct species.     

Quantitative analysis of Neanderthal temporal bone morphology using three-dimensional geometric morphometrics

The temporal bone is the location of several traits thought to differentiate Neanderthals from modern humans, including some proposed Neanderthal-derived traits. Most of these, however, are difficult to measure and are usually described qualitatively. This study applied the techniques of geometric morphometrics to the complex morphology of the temporal bone, in order to quantify the differences observed between Neanderthal and modern human anatomy. Two hundred and seventy modern human crania were measured, representing 9 populations of 30 individuals each, and spanning the extremes of the modern human geographical range. Twelve Neanderthal specimens, as well as Reilingen, Kabwe, Skhul 5, Qafzeh 9, and 4 Late Paleolithic European specimens, were included in the fossil sample. The data were collected in the form of three-dimensional (3-D) landmark coordinates, and specimen configurations were superimposed using generalized Procrustes analysis. The fitted coordinates were then analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis, and Mahalanobis D(2). The temporal bone landmark analysis was very successful in separating Neanderthals from modern humans. Neanderthals were separated from modern humans in both the principal components and canonical variates analyses. They were much further in Mahalanobis distances from all modern human populations than any two modern human groups were from each other. Most of the previously described temporal bone traits contributed to this separation.     

Testing hypotheses about tinkering in the fossil record: the case of the human skull

Efforts to test hypotheses about small-scale shifts in development (tinkering) that can only be observed in the fossil record pose many challenges. Here we use the origin of modern human craniofacial form to explore a series of analytical steps with which to propose and test evolutionary developmental hypotheses about the basic modules of evolutionary change. Using factor and geometric morphometric analyses of craniofacial variation in modern humans, fossil hominids, and chimpanzee crania, we identify several key shifts in integration (defined as patterns of covariation that result from interactions between components of a system) among units of the cranium that underlie the unique shape of the modern human cranium. The results indicate that facial retraction in modern humans is largely a product of three derived changes: a relatively longer anterior cranial base, a more flexed cranial base angle, and a relatively shorter upper face. By applying the Atchley-Hall model of morphogenesis, we show that these shifts are most likely the result of changes in epigenetic interactions between the cranial base and both the brain and the face. Changes in the size of the skeletal precursors to these regions may also have played some role. This kind of phenotype-to-genotype approach is a useful and important complement to more standard genotype-to-phenotype approaches, and may help to identify candidate genes involved in the origin of modern human craniofacial form.     

Visualizing patterns of craniofacial shape variation in Homo sapiens

The geometric morphometric analysis of shape variation in complex biological structures such as the human skull poses a number of specific challenges: the registration of homologous morphologies, the treatment of bilateral symmetry, the graphical representation of form variability in three dimensions and the interpretation of the results in terms of differential growth processes. To visualize complex patterns of shape change, we propose an alternative to classical Cartesian deformation grids in the style of D'Arcy W. Thompson. Reference to the surface structures of the organism under investigation permits a comprehensive visual grasp of shape change and its tentative interpretation in terms of differential growth. The application of this method to the analysis of human craniofacial shape variation reveals distinct modes of growth and development of the neurocranial and viscerocranial regions of the skull. Our data further indicate that variations in the orientation of the viscerocranium relative to the neurocranium impinge on the shapes of the face and the cranial vault.     

Finite element scaling analysis of human craniofacial growth

The study of form change is central to traditional cephalometric research. Unfortunately, traditional cephalometric studies operate within systems of measurement that are based on registration and orientation. Measurements produced in registered systems are insufficient for the craniofacial biologist who is interested in locating morphological differences between forms. In this article we apply a registration-free method called finite element scaling analysis in a study of the form change occurring during growth of the normal human craniofacial complex. The method provides form change data that can be summarized at various morphological levels. Twenty normal male individuals are used to analyze the form change that occurs from age 4 to ages 5, 7, 8, 9, 10, 12, 13, and 15 years. The magnitude and direction of growth expressed as shape and size change specific to craniofacial landmarks are presented. Although exceptions occur, our analysis shows that localized size change is, on the average, greater than localized shape change. The relation between size and shape change during growth shows allometry (shape change increasing during growth along with size change) but at a lesser magnitude and slower rate. We conclude that although shape change occurs throughout ontogeny, the magnitude and rate of shape change in relation to size change diminishes as age increases. This analysis represents new insights into the understanding of human craniofacial growth at various levels of morphological integration.     

Advances in Geometric Morphometrics

Geometric morphometrics is the statistical analysis of form based on Cartesian landmark coordinates. After separating shape from overall size, position, and orientation of the landmark configurations, the resulting Procrustes shape coordinates can be used for statistical analysis. Kendall shape space, the mathematical space induced by the shape coordinates, is a metric space that can be approximated locally by a Euclidean tangent space. Thus, notions of distance (similarity) between shapes or of the length and direction of developmental and evolutionary trajectories can be meaningfully assessed in this space. Results of statistical techniques that preserve these convenient properties—such as principal component analysis, multivariate regression, or partial least squares analysis—can be visualized as actual shapes or shape deformations. The Procrustes distance between a shape and its relabeled reflection is a measure of bilateral asymmetry. Shape space can be extended to form space by augmenting the shape coordinates with the natural logarithm of Centroid Size, a measure of size in geometric morphometrics that is uncorrelated with shape for small isotropic landmark variation. The thin-plate spline interpolation function is the standard tool to compute deformation grids and 3D visualizations. It is also central to the estimation of missing landmarks and to the semilandmark algorithm, which permits to include outlines and surfaces in geometric morphometric analysis. The powerful visualization tools of geometric morphometrics and the typically large amount of shape variables give rise to a specific exploratory style of analysis, allowing the identification and quantification of previously unknown shape features.     

Regional shape change in adult facial bone curvature with age

Life expectancies have increased dramatically over the last 100 years, affording greater opportunities to study the impact of age on adult craniofacial morphology. This article employs a novel application of established geometric morphometric methods to examine shape differences in adult regional facial bone curvature with age. Three-dimensional semilandmarks representing the curvature of the orbits, zygomatic arches, nasal aperture, and maxillary alveolar process were collected from a cross-sectional cranial sample of mixed sex and ancestry (male and female; African- and European-American), partitioned into three age groups (young adult = 18-39; middle-aged = 40-59 years; and elderly = 60+ years). Each facial region's semilandmarks were aligned into a common coordinate system via generalized Procrustes superimposition. Regional variation in shape was then explored via a battery of multivariate statistical techniques. Age-related shape differences were detected in the orbits, zygomatic arches, and maxillary alveolar process. Interactions between age, sex, and ancestry were also identified. Vector plots revealed patterns of superoinferior compression, lateral expansion, and posterior recession depending on the population/subpopulation, location, and age groups examined. These findings indicate that adult craniofacial curvature shape is not static throughout human life. Instead, age-related spatial modifications occur in various regions of the craniofacial skeleton. Moreover, these regional alterations vary not only through time, but across human populations and the sexes.     

Comparative study of normal, Crouzon, and Apert craniofacial morphology using finite element scaling analysis

Finite element scaling analysis is used to study differences in morphology between the craniofacial complex of normal individuals and those affected with the syndromes of Apert and Crouzon. Finite element scaling quantifies the differences in shape and size between forms without reference to any fixed, arbitrary registration point or orientation line and measures the amount of form change required to deform one object into another. Two-dimensional coordinates of landmarks digitized from annual sets of cephalometric radiographs were used in the analysis. A simple tabulation shows no difference in variances between the normal and pathological samples. A test of mean differences depicts the Apert and Crouzon morphologies as significantly different from normal. The Apert palate differs from normal in shape in the older age groups analyzed, and palatal size differences are most common at the posterior nasal spine. The Apert pituitary fossa and basi-occiput are significantly larger than normal. The Crouzon pituitary fossa is also larger than normal, but the difference is not always significant. The typical morphology of the Crouzon nose is due more to differences in shape than size. The Crouzon basi-occiput is significantly smaller than normal. An age association of the differences between the normal and pathological craniofacies was found in Apert syndrome but not in Crouzon syndrome. Apert syndrome is characterized by a more homogeneous pattern of craniofacial dysmorphology from 6 months to 18 years of age than Crouzon syndrome.     

Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex

The relationship between allometry and sexual dimorphism in the human craniofacial complex was analyzed using geometric morphometric methods. Thin-plate splines (TPS) analysis has been applied to investigate the lateral profile of complete adult skulls of known sex. Twenty-nine three-dimensional (3D) craniofacial and mandibular landmark coordinates were recorded from a sample of 52 adult females and 52 adult males of known age and sex. No difference in the influence of size on shape was detected between sexes. Both size and sex had significant influences on shape. As expected, the influence of centroid size on shape (allometry) revealed a shift in the proportions of the neurocranium and the viscerocranium, with a marked allometric variation of the lower face. Adjusted for centroid size, males presented a relatively larger size of the nasopharyngeal space than females. A mean-male TPS transformation revealed a larger piriform aperture, achieved by an increase of the angulation of the nasal bones and a downward rotation of the anterior nasal floor. Male pharynx expansion was also reflected by larger choanae and a more posteriorly inclined basilar part of the occipital clivus. Male muscle attachment sites appeared more pronounced. In contrast, the mean-female TPS transformation was characterized by a relatively small nasal aperture. The occipital clivus inclined anteriorly, and muscle insertion areas became smoothed. Besides these variations, both maxillary and mandibular alveolar regions became prognathic. The sex-specific TPS deformation patterns are hypothesized to be associated with sexual differences in body composition and energetic requirements.     

Technical note: Quantification of neurocranial shape variation using the shortest paths connecting pairs of anatomical landmarks

Three‐dimensional geometric morphometric techniques have been widely used in quantitative comparisons of craniofacial morphology in humans and nonhuman primates. However, few anatomical landmarks can actually be defined on the neurocranium. In this study, an alternative method is proposed for defining semi‐landmarks on neurocranial surfaces for use in detailed analysis of cranial shape. Specifically, midsagittal, nuchal, and temporal lines were approximated using Bezier curves and equally spaced points along each of the curves were defined as semi‐landmarks. The shortest paths connecting pairs of anatomical landmarks as well as semi‐landmarks were then calculated in order to represent the surface morphology between landmarks using equally spaced points along the paths. To evaluate the efficacy of this method, the previously outlined technique was used in morphological analysis of sexual dimorphism in modern Japanese crania. The study sample comprised 22 specimens that were used to generate 110 anatomical semi‐landmarks, which were used in geometric morphometric analysis. Although variations due to sexual dimorphism in human crania are very small, differences could be identified using the proposed landmark placement, which demonstrated the efficacy of the proposed method. Am J Phys Anthropol 151:658–666, 2013. © 2013 Wiley Periodicals, Inc.     

Bioanthropological analysis of human occipital condyles using geometric morphometric method

Sex differences are present in all parts of the body, including the skeletal system. Several methods are used to analyze the sex differences of skeleton, while more recently, a new method called geometric morphometry has been used. The aim of this study was to examine the sexual dimorphism of occipital condyles on human skulls originating from the population of Bosnia and Herzegovina using the geometric morphometric method.Material and methodsThe study was conducted on 214 human skulls of known gender from Bosnian population. For analysis of sexual dimorphism of occipital condyles, we used geometric morphometry, where all the skulls were scanned to obtain three-dimensional skull models. On the obtained models, we marked anthropometric points on occipital condyles in a Landmark Editor program from which we exported data in the form NTSYS file and analyzed it in MorphoJ program.ResultsFirst principal component PC1 describes 26.917% of total variability, the second principal component PC2 describes 20.992% of total variability, while the first eight principal components together describe 100% of total variability. The greatest variability between the male skulls and female skulls was present in the anterior-posterior diameter (length of occipital condyles). Discriminant functional analysis of the shape and size of the occipital condyles was possible with 69.50% accuracy for male skulls and with 60.27% accuracy for female skulls. The size of the occipital condyles showed a statistically significant effect on sexual determination. Discriminant functional analysis of the shape of the occipital condyles without affecting size enabled the determination of gender with with 65.96% accuracy for male skulls and with 63.01% accuracy for female skulls.ConclusionAnalysis of sexual dimorphism of occipital condyles using geometric morphometry showed statistically significant differences in the shape and size of occipital condyles between the sexes. The accuracy of sex determination based on occipital condyles was higher for male gender.     

Ossification and midline shape changes of the human fetal cranial base

An appreciation of ontogenetic changes to the cranial base is important for understanding the evolution of modern human skull form. Using geometric morphometric techniques, this study explores midline shape variations of the basicranium and midface during human prenatal ontogeny. In particular, the analysis sets out to explore shape variations associated with endochondral ossification and to reassess shape variations previously observed on the basis of angular measures.Fifty-four formalin-preserved human fetuses were imaged using high-resolution MRI. Coordinates for 10 landmarks defining the midline basicranium and midface were acquired and areas of ossification in the midline basioccipital, basisphenoid, and presphenoid cartilages were measured as percentages of overall cranial base area. The results show shape variations with increasing fetal size that are consistent with cranial base retroflexion, anterior facial projection and dorsal facial rotation. These growth variations are centered on the midsphenoid area and are associated with disproportionate variations of sphenoid height and length. Small but significant correlations were observed between ossification of the presphenoid cartilage and components of shape that described, among other variations, sphenoid shortening. While ossification cannot be directly linked with the shape variations observed, it seems likely that bone formation plays a role in modulating the influence of other factors on the fetal cranial base.     

Cranial growth in the squirrel monkey (Saimiri sciureus): a quantitative analysis using three dimensional coordinate data.

Improvements in data gathering technology have made it possible to quickly and accurately digitize large numbers of objects. The three dimensional coordinates of 44 homologous landmarks were obtained from a sample of 104 squirrel monkey (Saimiri sciureus) crania. After sorting by sex, the crania were assigned to one of four dental age groups. Two quantitative methods, Euclidean distance matrix analysis (EDMA) and finite element scaling analysis (FESA), were used to study craniofacial form change during growth within each sex. Form differences between the sexes at each developmental age were also examined. Both sexes show a small amount of cranial growth overall; however, there are areas of substantial local growth. These areas include the anterior neurocranium and basicranium, the basioccipital, and the anterior palate. Sexual dimorphism in the craniofacial complex is minimal. The most dimorphic regions are the orbitonasal portion of the lower face, the cranial base, and the palate.     

Assessing cranial plasticity in humans: The impact of artificial deformation on masticatory and basicranial structures

Artificial cranial deformations (ACD) are a widespread cultural practice found in numerous historical and prehistoric contexts. Their study can yield valuable insight into craniofacial growth, specifically into the interactions between neurocranial and basicranial modules. This study seeks to reinvestigate the presumed effect of ACD on basicranial and masticatory elements by applying a 3D geometric morphometric approach to CT scans. A total of 51 French and Bolivian skulls, representing anteroposterior and circumferential deformations and including undeformed individuals, were scanned, and 3D landmarks were submitted to between-group principal components analysis and two-block partial least-squares analysis. Our results illustrate changes in basicranial shape and in cranial base angles induced by ACD, as well as in masticatory geometry, namely in the relative position of the mandibular fossae. Furthermore, our findings highlight differential effects of the various deformation types, which suggest that patterns of covariation between modified vaults and their associated basicrania are more complex than previously assumed, thereby stressing the degree of plasticity in human craniofacial growth.     

Shell geometric morphometrics in Biomphalaria glabrata (Mollusca: Planorbidae) uninfected and infected with Schistosoma mansoni

Freshwater planorbid mollusks belonging to the genus Biomphalaria act as intermediate hosts for Schistosoma mansoni,the etiological agent of human intestinal schistosomiasis,in the Neotropical Region.Identification ofBiomphalaria spp.are carried out based on morphological characters,and the Schistosoma infection are determined by the presence of cercariae (verified through microscope preparation and mounting).Recently,the geometric morphometrics has proven to be a useful tool for determining shape differences in disease vectors arthropods.Due to this,we used geometric morphometrics to determine Biomphalaria glabrata shell differences (shape and size)between uninfected and infected specimens.We digitalized 12 anatomical points over the shell left side (from umbilicus to the last whorl) by combining type Ⅰ and Ⅱ landmarks and sliding semilandmarks;the coordinates were aligned by generalized Procrustes analysis.Principal component analyses were implemented for examining main variation axes,and discriminant analysis for testing group membership significance.We found significant separation between infected and uninfected shell conformation.All specimens were 100％correctly classified.The main differences occur in the peristome.The Kruskal-Wallis test finds significant differences in shell isometric size among infected and uninfected specimens.These findings correspond to other studies of traditional morphometrics,that infected snails showed the reduction in shell size in contrast to those uninfected specimens.     

Allometric and Group Differences in the Xenarthran Femur

The aim of this study is to analyze shape variation in the xenarthran femur to gain insights into their behavior and locomotion. Specimens of both Cingulata (armadillos and glyptodonts) and Pilosa (anteaters and sloths) were studied and within each group body mass varies by several orders of magnitude. The main focus of the analysis was allometric variation in femoral shape in the three groups studied, armadillos, glyptodonts, and pilosans. Three dimensional coordinates were recorded for 40 homologous landmarks on each of 51 xenarthran femurs. The data were analyzed by geometric morphometric methods, and form space analysis was used to identify the allometric variation in each of the three groups. Across all groups, larger specimens tended to have larger articular surfaces, more robust femora generally, and the shape of the femoral condyles was more suited to extended postures. In addition, in larger specimens the medial condyle was much larger than the lateral condyle and the third trochanter was located more distally. The larger armadillo femora had a greater trochanter located considerably proximal to the femoral head and this is thought to improve femoral extension, but in glyptodonts and pilosans the larger specimens had a greater trochanter that was far lateral to the femoral head and this is interpreted as enhancing femoral rotation.     

Comparison of cranial ontogenetic trajectories among great apes and humans

Molecular data suggest that humans are more closely related to chimpanzees than either is to the gorillas, yet one finds the closest similarity in craniofacial morphology to be among the great apes to the exclusion of humans. To clarify how and when these differences arise in ontogeny, we studied ontogenetic trajectories for Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. A total of 96 traditional three-dimensional landmarks and semilandmarks on the face and cranial base were collected on 268 adult and sub-adult crania for a geometric morphometric analysis. The ontogenetic trajectories are compared by various techniques, including a new method, relative warps in size-shape space. We find that adult Homo sapiens specimens are clearly separated from the great apes in shape space and size-shape space. Around birth, Homo sapiens infants are already markedly different from the great apes, which overlap at this age but diverge among themselves postnatally. The results suggest that the small genetic differences between Homo and Pan affect early human ontogeny to induce the distinct adult human craniofacial morphology. Pure heterochrony does not sufficiently explain the human craniofacial morphology nor the differences among the African apes.     

Comparison of craniofacial features of major human groups

Distance analysis and factor analysis, based on Q-mode correlation coefficients, were applied to 23 craniofacial measurements in 1,802 recent and prehistoric crania from major geographical areas of the Old World. The major findings are as follows: 1) Australians show closer similarities to African populations than to Melanesians. 2) Recent Europeans align with East Asians, and early West Asians resemble Africans. 3) The Asian population complex with regional difference between northern and southern members is manifest. 4) Clinal variations of craniofacial features can be detected in the Afro-European region on the one hand, and Australasian and East Asian region on the other hand. 5) The craniofacial variations of major geographical groups are not necessarily consistent with their geographical distribution pattern. This may be a sign that the evolutionary divergence in craniofacial shape among recent populations of different geographical areas is of a highly limited degree. Taking all of these into account, a single origin for anatomically modern humans is the most parsimonious interpretation of the craniofacial variations presented in this study. © 1996 Wiley-Liss, Inc.