Disparate and parallel craniofacial climatic adaptations in native populations of Asia, North America, and South America.

Understanding the impact that climate had in shaping cranial variation is critical for inferring the evolutionary mechanisms that played a role in human diversification. Here, we provide a comprehensive study aiming to analyze the association between climate and cranial variation of high latitude populations living in temperate to cold environments of Asia, North America, and South America. For this, we compiled a large morphometric dataset (N = 2633), which was combined with climatic and genomic data. We tested the influence of climate on the facial skeleton, nasal protrusion, and cranial vault and through multiple statistical tests at two geographical scales: intracontinental and intercontinental. We show that populations living in cold areas share a morphological pattern characterized by an increase in nasal height, facial and orbital heights and widths, a decrease in facial protrusion, and larger, longer, and lower cranial vaults. There are also distinctive features; populations from north Asia present the tallest noses, largest faces, and cranial vaults of the whole sample. Nasal breadth dimensions show small values in Asians, large values in South Americans, and non-significant changes in arctic North America. The morphological pattern in populations living at high latitude may be the result of parallel adaptation, as supported by physiological, morphometric, ecological, and genetic explanations, while the differences in magnitude and phenotypic expression could be due to the diverse population histories, severity of climate, and cultural strategies. Overall, our study shows that climate is a relevant factor shaping modern human morphology and it should be considered when studying modern human evolution and diversification.

Sexual dimorphism in human midfacial growth patterns from newborn to 5 years old based on computed tomography.

Recent studies have supported the presence and varying nature of craniofacial sexual dimorphism (SD) from the very first stages of ontogeny. But the exact patterns of between-sex differences during the first years of life remain obscure despite the importance of these data for craniofacial surgery treatment and forensic studies. Our study employs a large dataset of clinical computed tomography scans of individuals of East Slavonic descent from birth to 5 years of age (247 males and 184 females) to address the pattern of age-related between-sex differences in 22 linear measurements of the mid-face. At birth, SD of most dimensions is low, but it increases significantly during the first year of life. The level of SD of most variables fluctuates in both directions during the second year and peaks during the third and fourth years of life. During the sixth year, SD of about half of the variables markedly decreases. In adults, SD of all variables increases, but to a very different extent: from 2% to 13%. Most sexually dimorphic features of the facial skeleton begin to develop early in postnatal ontogeny and then may or may not become accentuated during puberty. Importantly, the patterns of age changes in the level of SD differ strongly between various dimensions, and so cannot be expressed by a single value for the whole face. Additionally, the level of SD for a particular variable is not ontogenetically stable during the first years of life.

New insights into the variability of upper airway morphology in modern humans.

The biological adaptation of the human lineage to its environment is a recurring question in paleoanthropology. Particularly, how eco-geographic factors (e.g., environmental temperature and humidity) have shaped upper airway morphology in hominins have been subject to continuing debate. Nasal shape is the result of many intertwined factors that include, but are not limited to, genetic drift, sexual selection, or adaptation to climate. A quantification of nasal airway (NA) morphological variation in modern human populations is crucial to better understand these multiple factors. In the present research, we study 195 in vivo CT scans of adult individuals collected in five different geographic areas (Chile, France, Cambodia, Russia, and South Africa). After segmentation of the nasal airway, we reconstruct 3D meshes that are analyzed with a landmark-free geometric morphometrics method based on surface deformation. Our results highlight subtle but statistically significant morphological differences between our five samples. The two morphologically closest groups are France and Russia, whose NAs are longer and narrower, with an important protrusion of the supero-anterior part. The Cambodian sample is the most morphologically distinct and clustered sample, with a mean NA that is wider and shorter. On the contrary, the Chilean sample form the most scattered cluster with the greatest intra-population variation. The South African sample is morphologically close to the Cambodian sample, but also partially overlaps the French and Russian variation. Interestingly, we record no correlation between NA volume and geographic groups, which raises the question of climate-related metabolic demands for oxygen consumption. The other factors of variation (sex and age) have no influence on the NA shape in our samples. However, NA volume varies significantly according both to sex and age: it is higher in males than in females and tends to increase with age. In contrast, we observe no effect of temperature or humidity on NA volume. Finally, we highlight the important influence of asymmetries related to nasal septum deviations in NA shape variation.

Nasal cavity and maxillary sinuses form variation among modern humans of Asian descent.

OBJECTIVES: This study explores variation, covariation, and ecogeographic pattern of the nasal cavity, maxillary sinuses, and external midfacial skeleton across 15 populations of east Asian origin inhabiting the Far East, Siberia, Alaska and Greenland. MATERIALS AND METHODS: We have collected linear measurements of the internal nasal cavity, maxillary sinus and external midfacial skeleton as well as volumes and surface areas of three-dimensional models of the cavity. A set of seven climatic variables, mtDNA and Y-chromosome genetic matrices and a matrix of geographic distances were also utilized. RESULTS: A strong association between form of the nasal cavity and climate was found, whereby all north Asian groups display increased volumes, areas and lengths of the cavity, and surface area to volume ratios (SA/V). Most of Siberian groups exhibit not only large and long, but also wide and tall nasal cavity. The Eskimo-Aleutian speaking groups possess cavities that are vertically short and narrow but of a high SA/V ratio. The sinuses exhibit an exceptionally high level of within- and between-group variation which supports the views on the sinus as an architectural byproduct. Both volume and area of the nasal cavity can be reliably estimated based on a set of simple and repeatable linear measurements. DISCUSSION: While the nasal cavity and maxillary sinus are both larger in a larger facial skeleton, there is a strong inverse relationship between them at a given facial size. Our results do not support the notion that the shape of the internal nasal cavity is more strongly associated with climate compared to the external midfacial morphology.

Midfacial growth patterns in males from newborn to 5 years old based on computed tomography.

OBJECTIVES: Growth patterns of the human facial skeleton have been of great interest and importance for biological anthropologists, forensic scientists, craniofacial surgeons, and orthopedists. Nevertheless, growth trends of the facial skeleton in infancy and early childhood are still poorly known and clinical CT data have been insufficiently used for studying craniofacial ontogeny. The purpose of this study was to provide a comprehensive quantitative description of human midfacial ontogeny in infancy and early childhood, and to contribute to debates regarding the role of modularity vs. integration in shaping the human face. METHODS: Our dataset includes 146 high resolution clinical CT datasets of males from the 2nd to 6th years of life and 101 dataset of infants (males) in the 1st year of life. Forty landmarks were collected from each 3D reconstructed skull, then 25 linear measurements describing the morphological features of the facial skeleton were calculated. The integration/modularity issue was addressed via comparison of intragroup correlation matrices at different ages. RESULTS: Growth trends for all the measurements are presented in charts and tables of statistical parameters that can be used as normative data. The midfacial variables display a great diversity of growth patterns. The correlation structure of the measurements is different at different ages. CONCLUSIONS: Variables commonly assigned to the same unit of the facial skeleton can exhibit rather different growth trends, but some measurements display seemingly coordinated patterns of growth change. The level of interindividual variation of most measurements is stable after the second half of the first year of life.

The association between mid-facial morphology and climate in northeast Europe differs from that in north Asia: Implications for understanding the morphology of Late Pleistocene Homo sapiens.

The climate of northeastern Europe is likely to resemble in many ways Late Pleistocene periglacial conditions in Europe, but there have been relatively few studies exploring the association between climate and morphology in the mid-face of modern northeastern European populations. To fill this gap, we sampled 540 male skulls from 22 European and Near Eastern groups, including 314 skulls from 11 populations from northeastern Europe, to test for possible climate-morphology association at the continental scale. Our results found a moderate and highly significant association (R = 0.48, p = 0.0013, Mantel test) between sets of 23 mid-facial measurements and eight climatic variables. A partial least squares analysis revealed this association to be mostly driven by differences between groups from northeastern Europe and populations from the Mediterranean and the Caucasus. Matrices of between-group genetic distances based on Y-chromosome and mtDNA markers, as well as cranial non-metric and geographic distance matrices, were used to control for the possible influence of shared population history. Irrespective of which measure of neutral between-population distances is taken into account, the association between cranial variables and climate remains significant. The pattern of association between climate and morphology of the mid-face in western Eurasia was then compared to that in east and north Asia. Although differences between the two were found, there were also similarities that support existing functional interpretations of morphology for the bony parts of the upper airways. Last, in a preliminary analysis using a reduced set of measurements, mid-facial morphology of several Upper Paleolithic European Homo sapiens specimens was found to be more similar to groups from northern and northeastern Europe than to southern European populations. Thus, the population of northeastern Europe rather than east and north Asian groups should be used as a model when studying climate-mediated mid-facial morphology of Upper Paleolithic European H. sapiens.

Testing the association between human mid-facial morphology and climate using autosomal, mitochondrial, Y chromosomal polymorphisms and cranial non-metrics.

OBJECTIVES: To figure out which and how many systems of genetic markers should be used to control for the effects of shared population history in studies examining the association between morphology and climate and to test cranial non-metric traits as an additional source of neutral distances for such studies. MATERIALS AND METHODS: We employed three systems of genetic markers (mtDNA, Y-chromosome and autosomal SNPs) and cranial non-metrics to control for potential impact of population history on apparent associations between climatic variables and mid-facial morphology found in a set of seven North Asian and one East Asian populations. RESULTS: A significant association between morphology and climate remained, independent of which of the four neutral distance matrices were used as a control. Matrices of neutral distances based on different systems of genetic markers show just one case of significant correlation among each other namely between the mtDNA and autosomal SNPs matrices. The correlation between the autosomal SNP and cranial non-metrics matrices is also fairly high but does not reach significance. DISCUSSION: A combination of several sources of genetic information could provide a more robust control for the effect of shared population history compared to just one type of markers since each of them has its own sources of bias and each provides a slightly different view of genetic relationships among the populations. Use of cranial non-metrics in researches examining the association between morphology and climate appears promising as they produce results that are generally consistent with those obtained using genetic markers.

Extreme climate, rather than population history, explains mid-facial morphology of Northern Asians.

Previous studies have examined mid-facial cold adaptation among either widely dispersed and genetically very diverse groups of humans isolated for tens of thousands of years, or among very closely related groups spread over climatically different regions. Here we present a study of one East Asian and seven North Asian populations in which we examine the evidence for convergent adaptations of the mid-face to a very cold climate. Our findings indicate that mid-facial morphology is strongly associated with climatic variables that contrast the temperate climate of East Asians and the very cold and dry climate of North Asians. This is also the case when either maxillary or nasal cavity measurements are considered alone. The association remains significant when mtDNA distances among populations are taken into account. The morphological contrasts between populations are consistent with physiological predictions and prior studies of mid-facial cold adaptation in more temperate regions, but among North Asians there appear to be some previously undescribed morphological features that might be considered as adaptive to extreme cold. To investigate this further, analyses of the seven North Asian populations alone suggest that mid-facial morphology remains strongly associated with climate, particularly winter precipitation, contrasting coastal Arctic and continental climates. However, the residual covariation among North Asian mid-facial morphology and climate when genetic distances are considered, is not significant. These findings point to modern adaptations to extreme climate that might be relevant to our understanding of the mid-facial morphology of fossil hominins that lived during glaciations.

Beyond skeletal studies: A computational analysis of nasal airway function in climate adaptation.

OBJECTIVES: Ecogeographic variation in human nasal anatomy has historically been analyzed on skeletal morphology and interpreted in the context of climatic adaptations to respiratory air-conditioning. Only a few studies have analyzed nasal soft tissue morphology, actively involved in air-conditioning physiology. MATERIALS AND METHODS: We used in vivo computer tomographic scans of (N = 146) adult individuals from Cambodia, Chile, Russia, and Spain. We conducted (N = 438) airflow simulations during inspiration using computational fluid dynamics to analyze the air-conditioning capacities of the nasal soft tissue in the inflow, functional, and outflow tract, under three different environmental conditions: cold-dry; hot-dry; and hot-humid. We performed statistical comparisons between populations and sexes. RESULTS: Subjects from hot-humid regions showed significantly lower air-conditioning capacities than subjects from colder regions in all the three conditions, specifically within the isthmus region in the inflow tract, and the anterior part of the internal functional tract. Posterior to the functional tract, no differences were detected. No differences between sexes were found in any of the tracts and under any of the conditions. DISCUSSION: Our statistical analyses support models of climatic adaptations of anterior nasal soft tissue morphology that fit with, and complement, previous research on dry skulls. However, our results challenge a morpho-functional model that attributes air-conditioning capacities exclusively to the functional tract located within the nasal cavity. Instead, our findings support studies that have suggested that both, the external nose and the intra-facial soft tissue airways contribute to efficiently warming and humidifying air during inspiration. This supports functional interpretations in modern midfacial variation and evolution.

The role of the nasal region in craniofacial growth: An investigation using path analysis.

This study focuses on the role of the nasal region and its interactions with adjacent facial elements during early ontogeny. A series of linear measurements, areas and volumes were extracted from a collection of 227 medical CT-scans of children from 0 to 6 years of age. These measurements describe aspects of the form of the orbit, maxilla, peri-alveolar (subnasal) region, nasal area, eye, oral region, masseter, and temporal muscles. Hypothesized interactions were then examined using path analysis. Two paths were designed: the first to investigate potential interactions in, and relative contributions of the nasal derivatives and adjacent regions to overall facial growth and development; the second path sees the addition of facial soft tissue measurements and aims to assess their effects on skeletal components, and on overall facial growth and development. The results of the first path indicate a large contribution of the nasal and subnasal regions to facial development. This indicates that the nasal septum and the developing dentition provide an important but variable contribution to facial ontogeny during early years. This result is confirmed in the second path, where the soft tissue elements were added to the diagram. Results of the second path indicate that the soft tissues contribute only locally to the development of some skeletal elements of the face. This indicates that the contribution of skeletal components has a more direct effect on facial height than soft tissue matrices, however there are complex interactions between soft tissues and skeletal elements throughout ontogeny.