The Middle Pleistocene human metatarsal from Sedia del Diavolo (Rome, Italy).

The peopling of Europe during the Middle Pleistocene is a debated topic among paleoanthropologists. Some authors suggest the coexistence of multiple human lineages in this period, while others propose a single evolving lineage from Homo heidelbergensis to Homo neanderthalensis. The recent reassessment of the stratigraphy at the Sedia del Diavolo (SdD) site (Latium, Italy), now dated to the beginning of marine isotope stage (MIS) 8, calls for a revision of the human fossils from the site. In this paper, we present the morphometric, biomechanical and palaeopathological study of the second right metatarsal SdD2, to both re-evaluate its taxonomical affinities and possibly determine the levels of physical activity experienced by the individual during lifetime. Results demonstrate the persistence of archaic features in SdD2 suggesting new insights into the technology and hunting strategies adopted by Homo between MIS 9 and MIS 8.

Mapping sexual dimorphism signal in the human cranium.

The study of sexual dimorphism in human crania has important applications in the fields of human evolution and human osteology. Current, the identification of sex from cranial morphology relies on manual visual inspection of identifiable anatomical features, which can lead to bias due to user's expertise. We developed a landmark-based approach to automatically map the sexual dimorphism signal on the human cranium. We used a sex-known sample of 228 individuals from different geographical locations to identify which cranial regions are most sexually dimorphic taking into account shape, form and size. Our results, which align with standard protocols, show that glabellar and supraciliary regions, the mastoid process and the nasal region are the most sexually dimorphic traits (with an accuracy of 73%). The accuracy increased to 77% if they were considered together. Surprisingly the occipital external protuberance resulted to be not sexually dimorphic but mainly related to variations in size. Our approach here applied could be expanded to map other variable signals on skeletal morphology.

Evaluation of age, sex, and ancestry-related variation in cortical bone and dentine volumes in modern humans, and a preliminary assessment of cortical bone-dentine covariation in later Homo.

Cortical bone and dentine share similarities in their embryological origin, development, and genetic background. Few analyses have combined the study of cortical bone and dentine to quantify their covariation relative to endogenous and exogenous factors. However, knowing how these tissues relate in individuals is of great importance to decipher the factors acting on their evolution, and ultimately to understand the mechanisms responsible for the different patterns of tissue proportions shown in hominins. The aims of this study are to examine age-, sex-, and ancestry-related variation in cortical bone and dentine volumes, and to preliminary assess the possible covariation between these tissues in modern humans and in five composite Neandertals. The modern analytical sample includes 12 immature individuals from France and 49 adults from France and South Africa. Three-dimensional tissue proportions were assessed from microtomographic records of radii and permanent maxillary canines. Results suggest ontogenic differences and a strong sexual dimorphism in cortical bone and dentine developments. The developmental pattern of dentine also seems to vary according to individual's ancestry. We measure a stronger covariation signal between cortical bone and dentine volumes than with any other dental tissue. A more complex covariation pattern is shown when splitting the modern sample by age, sex, and ancestry, as no signal is found in some subsamples while others show a covariation between cortical bone and either crown or radicular dentine. Finally, no difference in cortical bone volume is noticed between the modern young adults and the five young adult composite Neandertals from Marine Isotopic Stages (MIS) 5 and 3. Greater dentine Cortical bone and dentine (co)variation volumes are measured in the MIS 5 chimeric Neandertals whereas a strong interpopulation variation in dentine thickness is noticed in the MIS 3 chimeric Neandertals. Further research on the cortical bonedentine covariation will increase understanding of the impact of endogenous and exogenous factors on the development of the mineralized tissues.

Geometric morphometric analysis of Pleuronectiformes vertebrae: A new tool to identify archaeological fish remains?

Flatfish (Pleuronectiformes) vertebrae are difficult to identify to species due to the lack of diagnostic features. This has resulted in a lack of understanding of the species abundances across archaeological sites, hindering interpretations of historical fisheries in the North Sea area. We use a new approach, utilising a combined 2D landmark-based geometric morphometric analysis as an objective and non-destructive method for species identification of flatfish vertebrae from the North Sea area. Modern specimens were used as a reference to describe the morphological variation between taxa using principal component analysis (PCA) and to trial an automated classification using linear discriminant analysis. Although there is limited distinction between taxa using PCAs, the classification shows high accuracies, indicating that flatfish species identifications using geometric morphometrics are possible. Bone samples (n = 105) from two archaeological sites in the United Kingdom and France were analysed using this approach and their identifications were verified using collagen peptide mass fingerprinting. The success rate of species identification was usually less than 50%, indicating that this technique has limited applicability due to preservation/fragmentation of archaeological fish bone. Nonetheless, this could prove a valuable tool for modern and non-fragmented samples. Furthermore, the technique applied in this study can be easily adapted to work on other landmark datasets.

Normal human craniofacial growth and development from 0 to 4 years.

Knowledge of human craniofacial growth (increase in size) and development (change in shape) is important in the clinical treatment of a range of conditions that affects it. This study uses an extensive collection of clinical CT scans to investigate craniofacial growth and development over the first 48 months of life, detail how the cranium changes in form (size and shape) in each sex and how these changes are associated with the growth and development of various soft tissues such as the brain, eyes and tongue and the expansion of the nasal cavity. This is achieved through multivariate analyses of cranial form based on 3D landmarks and semi-landmarks and by analyses of linear dimensions, and cranial volumes. The results highlight accelerations and decelerations in cranial form changes throughout early childhood. They show that from 0 to 12 months, the cranium undergoes greater changes in form than from 12 to 48 months. However, in terms of the development of overall cranial shape, there is no significant sexual dimorphism in the age range considered in this study. In consequence a single model of human craniofacial growth and development is presented for future studies to examine the physio-mechanical interactions of the craniofacial growth.

A Comparison of Semilandmarking Approaches in the Analysis of Size and Shape.

Often, few landmarks can be reliably identified in analyses of form variation and covariation. Thus, 'semilandmarking' algorithms have increasingly been applied to surfaces and curves. However, the locations of semilandmarks depend on the investigator's choice of algorithm and their density. In consequence, to the extent that different semilandmarking approaches and densities result in different locations of semilandmarks, they can be expected to yield different results concerning patterns of variation and co-variation. The extent of such differences due to methodology is, as yet, unclear and often ignored. In this study, the performance of three landmark-driven semilandmarking approaches is assessed, using two different surface mesh datasets (ape crania and human heads) with different degrees of variation and complexity, by comparing the results of morphometric analyses. These approaches produce different semilandmark locations, which, in turn, lead to differences in statistical results, although the non-rigid semilandmarking approaches are consistent. Morphometric analyses using semilandmarks must be interpreted with due caution, recognising that error is inevitable and that results are approximations. Further work is needed to investigate the effects of using different landmark and semilandmark templates and to understand the limitations and advantages of different semilandmarking approaches.

Virtual excavation and analysis of the early Neanderthal cranium from Altamura (Italy).

Complete Neanderthal skeletons are almost unique findings. A very well-preserved specimen of this kind was discovered in 1993 in the deepest recesses of a karstic system near the town of Altamura in Southern Italy. We present here a detailed description of the cranium, after we virtually extracted it from the surrounding stalagmites and stalactites. The morphology of the Altamura cranium fits within the Neanderthal variability, though it retains features occurring in more archaic European samples. Some of these features were never observed in Homo neanderthalensis, i.e. in fossil specimens dated between 300 and 40 ka. Considering the U-Th age we previously obtained (>130 ka), the morphology of Altamura suggests that the archaic traits it retains may have been originated by geographic isolation of the early Neanderthal populations from Southern Italy.

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

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

A Comparison of Semilandmarking Approaches in the Visualisation of Shape Differences.

In landmark-based analyses of size and shape variation and covariation among biological structures, regions lacking clearly identifiable homologous landmarks are commonly described by semilandmarks. Different algorithms may be used to apply semilandmarks, but little is known about the consequences of analytical results. Here, we assess how different approaches and semilandmarking densities affect the estimates and visualisations of mean and allometrically scaled surfaces. The performance of three landmark-driven semilandmarking approaches is assessed using two different surface mesh datasets with different degrees of variation and complexity: adult human head and ape cranial surfaces. Surfaces fitted to estimates of the mean and allometrically scaled landmark and semilandmark configurations arising from geometric morphometric analyses of these datasets are compared between semilandmarking approaches and different densities, as well as with those from warping to landmarks alone. We find that estimates of surface mesh shape (i.e., after re-semilandmarking and then re-warping) made with varying numbers of semilandmarks are generally consistent, while the warping of surfaces using landmarks alone yields surfaces that can be quite different to those based on semilandmarks, depending on landmark coverage and choice of template surface for warping. The extent to which these differences are important depends on the particular study context and aims.

Homo sapiens and Neanderthals share high cerebral cortex integration into adulthood.

There is controversy around the mechanisms that guided the change in brain shape during the evolution of modern humans. It has long been held that different cortical areas evolved independently from each other to develop their unique functional specializations. However, some recent studies suggest that high integration between different cortical areas could facilitate the emergence of equally extreme, highly specialized brain functions. Here, we analyse the evolution of brain shape in primates using three-dimensional geometric morphometrics of endocasts. We aim to determine, firstly, whether modern humans present unique developmental patterns of covariation between brain cortical areas; and secondly, whether hominins experienced unusually high rates of evolution in brain covariation as compared to other primates. On the basis of analyses including modern humans and other extant great apes at different developmental stages, we first demonstrate that, unlike our closest living relatives, Homo sapiens retain high levels of covariation between cortical areas into adulthood. Among the other great apes, high levels of covariation are only found in immature individuals. Secondly, at the macro-evolutionary level, our analysis of 400 endocasts, representing 148 extant primate species and 6 fossil hominins, shows that strong covariation between different areas of the brain in H. sapiens and Homo neanderthalensis evolved under distinctly higher evolutionary rates than in any other primate, suggesting that natural selection favoured a greatly integrated brain in both species. These results hold when extinct species are excluded and allometric effects are accounted for. Our findings demonstrate that high covariation in the brain may have played a critical role in the evolution of unique cognitive capacities and complex behaviours in both modern humans and Neanderthals.

Multi-proxy analysis suggests Late Pleistocene affinities of human skeletal remains attributed to Balzi Rossi.

In two publications from 1967 and 1971, M. Masali described human skeletal remains presumed to have been found in the Balzi Rossi caves (Ventimiglia, Italy), based on a signed note dated to 1908. Since then, the remains - dubbed "Conio's Finds" and preserved at the University of Torino - had not been further studied. We performed a multidisciplinary investigation aimed at clarifying the geographical and chronological attribution of these specimens. Collagen extraction for AMS dating was unsuccessful, but we obtained two direct dates on the best- preserved crania via 231Pa/235U direct gamma-ray spectrometry (10,500±2,000 years BP and 12,500±2,500 years BP). We analyzed the metrics and morphology of the crania and femora by comparing them with samples belonging to the Upper Paleolithic, Mesolithic, and Neolithic periods, and evidenced that the "Conio's Finds" are morphologically more compatible with a Late Pleistocene rather than Holocene attribution. We analyzed the literature regarding the history of excavations at Balzi Rossi, and we propose that - if any credence should be given to the note accompanying the material - the remains may have been found in front of Grotta dei Fanciulli or Grotta del Caviglione, in the redeposited soil dug up during the installation of lime kilns carried out between the late 18th and the early 19th centuries. These hypotheses may be tested in the future by comparing the speleothem deposited on one of the crania and the remaining deposit at the site.

Bone density and genomic analysis unfold cold adaptation mechanisms of ancient inhabitants of Tierra del Fuego.

The Fuegians, ancient inhabitants of Tierra del Fuego, are an exemplary case of a cold-adapted population, since they were capable of living in extreme climatic conditions without any adequate clothing. However, the mechanisms of their extraordinary resistance to cold remain enigmatic. Brown adipose tissue (BAT) plays a crucial role in this kind of adaptation, besides having a protective role on the detrimental effect of low temperatures on bone structure. Skeletal remains of 12 adult Fuegians, collected in the second half of XIX century, were analyzed for bone mineral density and structure. We show that, despite the unfavorable climate, bone mineral density of Fuegians was close to that seen in modern humans living in temperate zones. Furthermore, we report significant differences between Fuegians and other cold-adapted populations in the frequency of the Homeobox protein Hox-C4 (HOXC4) rs190771160 variant, a gene involved in BAT differentiation, whose identified variant is predicted to upregulate HOXC4 expression. Greater BAT accumulation might therefore explain the Fuegians extreme cold-resistance and the protection against major cold-related damage. These results increase our understanding of how ecological challenges have been important drivers of human-environment interactions during Humankind history.

Digital restoration of the Wilson-Leonard 2 Paleoindian skull (~10,000 BP) from central Texas with comparison to other early American and modern crania.

OBJECTIVES: Craniofacial morphology (CFM) is often used to address questions about the biological affinities of the earliest Americans, or Paleoindians, but resolution is complicated in part by a lack of well-preserved crania. The Wilson-Leonard 2 (WL-2) Paleoindian skull from Texas has never been fully analyzed because it is crushed and cannot be physically reconstructed. This study employs a digital restoration for comprehensive assessment and analysis of WL-2. MATERIALS AND METHODS: High-resolution CT data and geometric morphometrics are used to restore the WL-2 skull and analyze its morphology using 65 craniometric measurements acquired on the restoration. These data allow for a full morphological description and multivariate (Mahalanobis Distance and Principal Component) comparisons to other Paleoindians and recent populations. RESULTS: WL-2 has a long, narrow braincase, and a short, modestly prognathic face. Compared with other Paleoindians, she is individually similar to several skulls from Brazil, but aligns most closely with pooled samples from the US and Mexico. WL-2 is most similar to recent populations from Europe, Asia, and the Americas, and markedly different to those from Africa and Australia. DISCUSSION: The overall morphology of WL-2 and her association with Asians and Europeans align well with trends identified in other CFM analyses. Her affinity to recent Amerindians contrasts with the findings of many previous CFM studies, but is seemingly consistent with molecular analyses suggesting a close relationship between some Paleoindians and modern American Indians. This study demonstrates the potential for using digital anthropological methods to study other Paleoindian crania whose data value is limited by physical destruction and/or deformation.

Correction: A new, fast method to search for morphological convergence with shape data.

[This corrects the article DOI: 10.1371/journal.pone.0226949.].

Growing old: Do women and men age differently?

Aging of the head and especially the face has been studied intensively, yet questions remain about the timing and rates of aging throughout adulthood and about the extent to which aging differs between men and women. Here we address these issues by developing statistical models of craniofacial aging to describe and compare aging through the life course in both sexes. We selected cranial surface meshes from 254 females and 252 males, aged from 20 to 90 years from the Headspace project, Liverpool, UK. Sixteen anatomical landmarks and 59 semilandmarks on curves and surfaces were used to parameterize these. Modes and degrees of aging throughout adulthood were assessed and compared among sexes using Procrustes-based geometric morphometric methods. Regression analyses of form through the whole age range indicate that age accounts for a small proportion of total variance in both sexes, but form is significantly related to age and males and females age in significantly different ways. Further analyses indicate that aging differs in character, timing, and rates in both sexes between early and later phases of adulthood. Sexual differences in aging are evident in the early and later phases of adulthood. The study adds to knowledge of the aging of adult craniofacial form and sexual dimorphism. It is based on a local population and so the findings are directly applicable to that population. Further studies are needed to assess generalizability and provide better data on population differences to facilitate clinical assessment and treatment planning.

morphomap: An R package for long bone landmarking, cortical thickness, and cross-sectional geometry mapping.

OBJECTIVES: This study describes and demonstrates the functionalities and application of a new R package, morphomap, designed to extract shape information as semilandmarks in multiple sections, build cortical thickness maps, and calculate biomechanical parameters on long bones. METHODS: morphomap creates, from a single input (an oriented 3D mesh representing the long bone surface), multiple evenly spaced virtual sections. morphomap then directly and rapidly computes morphometric and biomechanical parameters on each of these sections. The R package comprises three modules: (a) to place semilandmarks on the inner and outer outlines of each section, (b) to extract cortical thicknesses for 2D and 3D morphometric mapping, and (c) to compute cross-sectional geometry. RESULTS: In this article, we apply morphomap to femora from Homo sapiens and Pan troglodytes to demonstrate its utility and show its typical outputs. morphomap greatly facilitates rapid analysis and functional interpretation of long bone form and should prove a valuable addition to the osteoarcheological analysis software toolkit. CONCLUSIONS: Long bone loading history is commonly retrodicted by calculating biomechanical parameters such as area moments of inertia, analyzing external shape and measuring cortical thickness. morphomap is a software written in the open source R environment, it integrates the main methodological approaches (geometric morphometrics, cortical morphometric maps, and cross-sectional geometry) used to parametrize long bones.

3D Modeling of craniofacial ontogeny and sexual dimorphism in children.

BACKGROUND: The range of normal variation of growth and development of the craniofacial region is of direct clinical interest but incompletely understood. Here we develop a statistical model of craniofacial growth and development to compare craniofacial ontogeny between age groups and sexes and pilot an approach to modeling that is relatively straightforward to apply in the context of clinical research and assessment. METHODS: The sample comprises head surface meshes captured using a 3dMD five-camera system from 65 males and 47 females (range 3-20 years) from the Headspace project, Liverpool, UK. The surface meshes were parameterized using 16 anatomical landmarks and 59 semilandmarks on curves and surfaces. Modes and degrees of growth and development were assessed and compared among ages and sexes using Procrustes based geometric morphometric methods. RESULTS: Regression analyses indicate that 3-10 year olds undergo greater changes than 11-20 year olds and that craniofacial growth and development differs between these age groups. The analyses indicate that males extend growth allometrically into larger size ranges, contributing substantially to adult dimorphism. Comparisons of ontogenetic trajectories between sexes find no significant differences, yet when hypermorphosis is accounted for in the older age group there is a significant residual sexual dimorphism. CONCLUSIONS: The study adds to knowledge of how adult craniofacial form and sexual dimorphism develop. It was carried out using readily available software which facilitates replication of this work in diverse populations to underpin clinical assessment of deformity and the outcomes of corrective interventions.

Frontal bone virtual reconstruction and geometric morphometric analysis of the mid-Pleistocene hominin KNM-OG 45500 (Olorgesailie, Kenya).

KNM-OG 45500 is a hominin fossil composed of parts of a frontal bone, left temporal bone, and cranial vault pieces. Since its discovery along the Olorgesailie Formation (Kenya) in 2003, it has been associated with the Homo erectus hypodigm. The specimen, derived from a geological context dated to ca. 900 Ka BP, has been described as a very small individual of probable female sex. However, despite its status as an important hominin specimen, it has not been used in a quantitative comparative framework because of its fragmentary condition. Here, we undertake a virtual reconstruction of the better-preserved fragment, the frontal bone. We additionally apply geometric morphometric analyses, using a geographically diverse fossil and modern human sample, in order to investigate the morphological affinities of KNM-OG 45500. Our results show that the frontal shape of KNM-OG 45500 exhibits similarities with Early Pleistocene fossils from Eurasia and Africa that are assigned to H. erectus sensu lato (s.l.). Its size, on the other hand, is notably smaller than most other Homo erectus fossils and modern humans and similar to the specimens from Dmanisi (Georgia) and to Homo naledi. Taken together, our analyses of the frontal bone suggest a taxonomic attribution of KNM-OG 45500 to H. erectus s.l. and extend even further the range of size variability associated with this taxon around 900 Ka BP.

In situ observations on the dentition and oral cavity of the Neanderthal skeleton from Altamura (Italy).

The Neanderthal specimen from Lamalunga Cave, near Altamura (Apulia, Italy), was discovered during a speleological survey in 1993. The specimen is one of the most complete fossil hominins in Europe and its state of preservation is exceptional, although it is stuck in calcareous concretions and the bones are mostly covered by calcite depositions. Nevertheless, it is possible to carry out some observations on craniodental features that have not previously been described. In this work, we present an account of the oral cavity, made possible by the use of a videoscope, which allowed us to reach some hidden parts of the mandible and palate. This is the first detailed overview of the teeth and maxillary bones of the Neanderthal skeleton from Altamura. The dentition is almost complete. However, two teeth (upper right P3 and upper left M1) were lost ante mortem and four teeth (lower right I1 and P3 and lower left I1 and I2) were lost most probably post mortem. Dental wear is marked. The erupted M3s and the inversion of the compensating curve of Wilson in the M1s and M2s but not in the M3s suggest that the individual is fully adult, but not old. Although most of the teeth have their roots exposed for several millimeters, the periodontal bone appears to be in good condition overall, except in correspondence of the two ante-mortem tooth losses. X-rays of the anterior teeth show a periapical lesion, probably linked to the advanced dental wear. We also observed a weak expression of taurodontism in the posterior dentition and the presence of a retromolar space, features consistent with an attribution to the Neanderthal hypodigm; this attribution is also supported by aspects of the cranial morphology, the morphometric analysis of the scapula and preliminary mtDNA data. There is also a well-developed palatine torus, to the best of our knowledge a feature not previously described in Neanderthals.

A Major Change in Rate of Climate Niche Envelope Evolution during Hominid History.

Homo sapiens is the only species alive able to take advantage of its cognitive abilities to inhabit almost all environments on Earth. Humans are able to culturally construct, rather than biologically inherit, their occupied climatic niche to a degree unparalleled within the animal kingdom. Precisely, when hominins acquired such an ability remains unknown, and scholars disagree on the extent to which our ancestors shared this same ability. Here, we settle this issue using fine-grained paleoclimatic data, extensive archaeological data, and phylogenetic comparative methods. Our results indicate that whereas early hominins were forced to live under physiologically suitable climatic conditions, with the emergence of H. heidelbergensis, the Homo climatic niche expanded beyond its natural limits, despite progressive harshening in global climates. This indicates that technological innovations providing effective exploitation of cold and seasonal habitats predated the emergence of Homo sapiens.