Comparative anatomy and 3D geometric morphometrics of the El Sidrón atlases (C1).

The first cervical vertebra (atlas, C1) is an important element of the vertebral column because it connects the cranial base with the cervical column, thus helping to maintain head posture and contributing to neck mobility. However, few atlases are preserved in the fossil record because of the fragility of this vertebra. Consequently, only eight well-preserved atlases from adult Neandertals have been recovered and described. Here, we present nine new atlas remains from the El Sidrón Neandertal site (Asturias, Spain), two of which (SD-1643 and SD-1605/1595) are sufficiently well preserved to allow for a detailed comparative and three-dimensional geometric morphometric analysis. We compared standard linear measurements of SD-1643 and SD-1605/1595 with those of other Neandertal atlases and carried out three-dimensional geometric morphometric analyses to compare size and shape of SD-1643 and SD-1605/1595 with those of 28 Pan (Pan troglodytes and Pan paniscus), a broad comparative sample of 55 anatomically modern humans from African and European populations, and other fossil hominins (Neandertals, Homo antecessor, Paranthropus boisei). The El Sidrón atlas fossils show typical features of the Neandertal atlas morphology, such as caudal projection of the anterior tubercle, gracility of both the posterior tubercle and the tuberosity for the insertion of the transverse ligament, and an anteroposteriorly elongated neural canal. Furthermore, when compared with atlases from the other taxa, Neandertals exhibit species-specific features of atlas morphology including a relatively lower lateral mass height, relatively narrower transverse foramina, and flatter and more horizontally oriented articular facets. Some of these features fit with previous suggestions of shorter overall length of the cervical spine and potential differences in craniocervical posture and mobility. Our results may support a different spinopelvic alignment in this species, as the atlas morphology suggests reduced cervical lordosis.

Three-dimensional geometric morphometrics of thorax-pelvis covariation and its potential for predicting the thorax morphology: A case study on Kebara 2 Neandertal.

The skeletal torso is a complex structure of outstanding importance in understanding human body shape evolution, but reconstruction usually entails an element of subjectivity as researchers apply their own anatomical expertise to the process. Among different fossil reconstruction methods, 3D geometric morphometric techniques have been increasingly used in the last decades. Two-block partial least squares analysis has shown great potential for predicting missing elements by exploiting the covariation between two structures (blocks) in a reference sample: one block can be predicted from the other one based on the strength of covariation between blocks. The first aim of this study is to test whether this predictive approach can be used for predicting thorax morphologies from pelvis morphologies within adult Homo sapiens reference samples with known covariation between the thorax and the pelvis. The second aim is to apply this method to Kebara 2 Neandertal (Israel, ∼60 ka) to predict its thorax morphology using two different pelvis reconstructions as predictors. We measured 134 true landmarks, 720 curve semilandmarks, and 160 surface semilandmarks on 60 3D virtual torso models segmented from CT scans. We conducted three two-block partial least squares analyses between the thorax (block 1) and the pelvis (block 2) based on the H. sapiens reference samples after performing generalized Procrustes superimposition on each block separately. Comparisons of these predictions in full shape space by means of Procrustes distances show that the male-only predictive model yields the most reliable predictions within modern humans. In addition, Kebara 2 thorax predictions based on this model concur with the thorax morphology proposed for Neandertals. The method presented here does not aim to replace other techniques, but to rather complement them through quantitative prediction of a virtual 'scaffold' to articulate the thoracic fossil elements, thus extending the potential of missing data estimation beyond the methods proposed in previous works.

Analyses of the neandertal patellae from El Sidrón (Asturias, Spain) with implications for the evolution of body form in Homo.

The evolution of the body form in Homo and its potential morphological connection to the arrangement of different skeletal systems is of major interest in human evolution. Patella morphology as part of the knee is potentially influenced by body form. Here, we describe for the first time the patellae remains recovered at El Sidrón Neandertal site and analyze them in a comparative evolutionary framework. We aim to clarify whether morphometric features frequently observed in Neandertal and modern human patellae are retained from a primitive anatomical arrangement or whether they represent derived features (apomorphies). For this purpose, we combine analyses of discrete features, classic anthropological measurements, and 3D geometric morphometrics based on generalized Procrustes analysis, mean size and shape comparisons, and principal components analysis. We found a size increment of the patella in hominin evolution, with large species showing a larger patella. Modern humans and Neandertals exhibit overall larger patellae, with maximum values observed in the latter, likely as a consequence of their broader body shape. Also, some Neandertals display a thicker patella, which has been linked to larger quadriceps muscles. However, Neandertals retain a primitive morphology in their patellar articular surfaces, with similar-sized lateral and medial articular facets, leading to a more symmetrical internal face. This feature is inherited from a primitive Homo ancestor and suggests a different configuration of the knee in Neandertals. Conversely, Homo sapiens exhibits an autoapomorphic patellar anatomy with expanded lateral articular facets. We propose that these distinct configurations of the patella within Homo may be a consequence of different body forms rather than specific functional adaptations of the knee. Thus, the slender body form of modern humans may entail a medial reorientation of the tibial tuberosity (patellar ligament), allowing lateral surface expansion. These anatomical evolutionary variations may involve subtle secondary differences in bipedalism within Homo.

Three-dimensional analysis of sexual dimorphism in the soft tissue morphology of the upper airways in a human population.

OBJECTIVES: Several studies have analyzed the sexual dimorphism of the skeletal cranial airways. This study aimed to quantify the three-dimensional (3D) morphology of the soft tissues of the upper airways in a human population. We addressed hypotheses about morphological features related to respiratory and energetic aspects of nasal sexual dimorphism. METHODS: We reconstructed 3D models of 41 male and female soft tissue nasal airways from computed tomography data. We measured 280 landmarks and semilandmarks for 3D-geometric morphometric analyses to test for differences in size and 3D morphology of different functional compartments of the soft tissue airways. RESULTS: We found statistical evidence for sexual dimorphism: Males were larger than females. 3D features indicated taller and wider inflow tracts, taller outflow tracts and slightly taller internal airways in males. These characteristics are compatible with greater airflow in males. DISCUSSION: The differences in 3D nasal airway morphology are compatible with the respiratory-energetics hypothesis according to which males differ from females because of greater energetic demands. Accordingly, structures related to inflow and outflow of air show stronger signals than structures relevant for air-conditioning.

Assessing thoraco-pelvic covariation in Homo sapiens and Pan troglodytes: A 3D geometric morphometric approach.

OBJECTIVES: Understanding thoraco-pelvic integration in Homo sapiens and their closest living relatives (genus Pan) is of great importance within the context of human body shape evolution. However, studies assessing thoraco-pelvic covariation across Hominoidea species are scarce, although recent research would suggest shared covariation patterns in humans and chimpanzees but also species-specific features, with sexual dimorphism and allometry influencing thoraco-pelvic covariation in these taxa differently. MATERIAL AND METHODS: N = 30 adult H. sapiens and N = 10 adult Pan troglodytes torso 3D models were analyzed using 3D geometric morphometrics and linear measurements. Effects of sexual dimorphism and allometry on thoraco-pelvic covariation were assessed via regression analyses, and patterns of thoraco-pelvic covariation in humans and chimpanzees were computed via Two-Block Partial Least Squares analyses. RESULTS: Results confirm the existence of common aspects of thoraco-pelvic covariation in humans and chimpanzees, and also species-specific covariation in H. sapiens that is strongly influenced by sexual dimorphism and allometry. Species-specific covariation patterns in chimpanzees could not be confirmed because of the small sample size, but metrics point to a correspondence between the most caudal ribs and iliac crest morphology that would be irrespective of sex. CONCLUSIONS: This study suggests that humans and chimpanzees share common aspects of thoraco-pelvic covariation but might differ in others. In humans, torso integration is strongly influenced by sexual dimorphism and allometry, whilst in chimpanzees it may not be. This study also highlights the importance not only of torso widths but also of torso depths when describing patterns of thoraco-pelvic covariation in primates. Larger samples are necessary to support these interpretations.

Three-dimensional analysis of sexual dimorphism in ribcage kinematics of modern humans.

OBJECTIVES: Sexual dimorphism is an important biological factor underlying morphological variation in the human skeleton. Previous research found sex-related differences in the static ribcage, with males having more horizontally oriented ribs and a wider lower ribcage than females. Furthermore, a recent study found sex-related differences in the kinematics of the human lungs, with cranio-caudal movements of the caudal part of the lungs accounting for most of the differences between sexes. However, these movements cannot be quantified in the skeletal ribcage, so we do not know if the differences observed in the lungs are also reflected in sex differences in the motion of the skeletal thorax. MATERIALS AND METHODS: To address this issue, we quantified the morphological variation of 42 contemporary human ribcages (sex-balanced) in both maximal inspiration and expiration using 526 landmarks and semilandmarks. Thoracic centroid size differences between sexes were assessed using a t test, and shape differences were assessed using Procrustes shape coordinates, through mean comparisons and dummy regressions of shape on kinematic status. A principal components analysis was used to explore the full range of morphological variation. RESULTS: Our results show significant size differences between males and females both in inspiration and expiration (p < .01) as well as significant shape differences, with males deforming more than females during inspiration, especially in the mediolateral dimension of the lower ribcage. Finally, dummy regressions of shape on kinematic status showed a small but statistically significant difference in vectors of breathing kinematics between males and females (14.78°; p < .01). DISCUSSION: We support that sex-related differences in skeletal ribcage kinematics are discernible, even when soft tissues are not analyzed. We hypothesize that this differential breathing pattern is primarily a result of more pronounced diaphragmatic breathing in males, which might relate to differences in body composition, metabolism, and ultimately greater oxygen demand in males compared to females. Future research should further explore the links between ribcage morphological variation and basal metabolic rate.

3D geometric morphometric analysis of variation in the human lumbar spine.

OBJECTIVES: The shape of the human lumbar spine is considered to be a consequence of erect posture. In addition, several other factors such as sexual dimorphism and variation in genetic backgrounds also influence lumbar vertebral morphology. Here we use 3D geometric morphometrics (GM) to analyze the 3D morphology of the lumbar spine in different human populations, exploring those potential causes of variation. MATERIAL AND METHODS: We collected 390 (semi) landmarks from 3D models of the CT scans of lumbar spines of seven males and nine females from a Mediterranean population (Spain, Israel) and seven males and either females from a South African population for geometric morphometric (GM) analysis. We carried out Generalized Procrustes Analysis, Principal Components, and Regression analyses to evaluate shape variation; and complemented these analyses with the Cobb Method. RESULTS: The Mediterranean sample was considerably more lordotic than the South African sample. In both populations, female lumbar spines showed proportionally narrower and more craniocaudally elongated lumbar segments than in males. In addition, the point of maximum curvature in females tended to be located more inferiorly than in males. DISCUSSION: Our results show that sexual dimorphism is an important factor of lumbar spine variation that mainly affects features of lumbar spine robustness (height proportions) and the structure-but not the degree-of its curvature. Differences in lordosis, however, are clearer at the inter-population level. This reflects previous conflicting studies casting doubts on pregnancy as an adaptive factor influencing lordosis. Other factors, for example, shape of the individual lumbar vertebrae and intervertebral discs and their relative proportions within the lumbar spine should be considered when exploring variation in vertebral column morphology.

3D analysis of sexual dimorphism in size, shape and breathing kinematics of human lungs.

Sexual dimorphism in the human respiratory system has been previously reported at the skeletal (cranial and thoracic) level, but also at the pulmonary level. Regarding lungs, foregoing studies have yielded sex-related differences in pulmonary size as well as lung shape details, but different methodological approaches have led to discrepant results on differences in respiratory patterns between males and females. The purpose of this study is to analyse sexual dimorphism in human lungs during forced respiration using 3D geometric morphometrics. Eighty computed tomographies (19 males and 21 females) were taken in maximal forced inspiration (FI) and expiration (FE), and 415 (semi)landmarks were digitized on 80 virtual lung models for the 3D quantification of pulmonary size, shape and kinematic differences. We found that males showed larger lungs than females (P < 0.05), and significantly greater size and shape differences between FI and FE. Morphologically, males have pyramidal lung geometry, with greater lower lung width when comparing with the apices, in contrast to the prismatic lung shape and similar widths at upper and lower lungs of females. Multivariate regression analyses confirmed the effect of sex on lung size (36.26%; P < 0.05) and on lung shape (7.23%; P < 0.05), and yielded two kinematic vectors with a small but statistically significant angle between them (13.22°; P < 0.05) that confirms sex-related differences in the respiratory patterns. Our 3D approach shows sexual dimorphism in human lungs likely due to a greater diaphragmatic action in males and a predominant intercostal muscle action in females during breathing. These size and shape differences would lead to different respiratory patterns between sexes, whose physiological implications need to be studied in future research.

The torso integration hypothesis revisited in Homo sapiens: Contributions to the understanding of hominin body shape evolution.

OBJECTIVES: Lower thoracic widths and curvatures track upper pelvic widths and iliac blades curvatures in hominins and other primates (torso integration hypothesis). However, recent studies suggest that sexual dimorphism could challenge this assumption in Homo sapiens. We test the torso integration hypothesis in two modern human populations, both considering and excluding the effect of sexual dimorphism. We further assess covariation patterns between different thoracic and pelvic levels, and we explore the allometric effects on torso shape variation. MATERIAL AND METHODS: A sex-balanced sample of 50 anatomically connected torsos (25 Mediterraneans, 25 Sub-Saharan Africans) was segmented from computed tomography scans. We compared the maximum medio-lateral width at seventh-ninth rib levels with pelvic bi-iliac breadth in males and females within both populations. We measured 1,030 (semi)landmarks on 3D torso models, and torso shape variation, mean size and shape comparisons, thoraco-pelvic covariation and allometric effects were quantified through 3D geometric morphometrics. RESULTS: Females show narrow thoraces and wide pelves and males show wide thoraces and narrow pelves, although this trend is more evident in Mediterraneans than in Sub-Saharans. Equal thoracic and pelvic widths, depths and curvatures were found in absence of sexual dimorphism. The highest strength of covariation was found between the lowest rib levels and the ilia, and allometric analyses showed that smaller torsos were wider than larger torsos. CONCLUSIONS: This is the first study testing statistically the torso integration hypothesis in anatomically connected torsos. We propose a new and more complex torso integration model in H. sapiens with sexual dimorphism leading to different thoracic and pelvic widths and curvatures. These findings have important implications in hominin body shape reconstructions.

Morphological and functional implications of sexual dimorphism in the human skeletal thorax.

OBJECTIVES: The human respiratory apparatus is characterized by sexual dimorphism, the cranial airways of males being larger (both absolutely and relatively) than those of females. These differences have been linked to sex-specific differences in body composition, bioenergetics, and respiratory function. However, whether morpho-functional variation in the thorax is also related to these features is less clear. We apply 3D geometric morphometrics to study these issues and their implications for respiratory function. MATERIAL AND METHODS: Four hundred two landmarks and semilandmarks were measured in CT-reconstructions of rib cages from adult healthy subjects (Nmale = 18; Nfemale = 24) in maximal inspiration (MI) and maximal expiration (ME). After Procrustes registration, size and shape data were analyzed by mean comparisons and regression analysis. Respiratory function was quantified through functional size, which is defined as the difference of rib cage size between MI and ME. RESULTS: Males showed significantly larger thorax size (p < .01) and functional size (p < .05) than females. In addition, the 3D-shape differed significantly between sexes (p < .01). Male rib cages were wider (particularly caudally) and shorter, with more horizontally oriented ribs when compared to females. While thorax widening and rib orientation were unrelated to allometry, thorax shortening showed a slight allometric signal. CONCLUSIONS: Our findings are in line with previous research on sexual dimorphism of the respiratory system. However, we add that thorax shortening observed previously in males is the only feature caused by allometry. The more horizontally oriented ribs and the wider thorax of males may indicate a greater diaphragmatic contribution to rib cage kinematics than in females, and differences in functional size fit with the need for greater oxygen intake in males.

Testing the reliability of the rearticulation of osteological primate pelves in comparative morphological studies.

The evolution of human pelvic form is primarily studied using disarticulated osteological material of living and fossil primates that need rearticulation to approximate anatomical position. To test whether this technique introduces errors that impact biological signals, virtual rearticulations of the pelvis in anatomical position from computed tomography scans were compared with rearticulated models from the same individuals for one female and one male of Homo sapiens, Pan troglodytes, Macaca mulatta, Lepilemur mustelinus, Galago senegalensis, and Nycticebus pygmaeus. "Cadaveric" pelvic bones were first analyzed in anatomical position, then the three bones were segmented individually, intentionally scattered, and "rearticulated" to test for rearticulation error. Three-dimensional landmarks and linear measurements were used to characterize the overall pelvis shape. Cadaveric and rearticulated pelves were not identical, but inter-specific and intra-specific shape differences were higher than the landmarking error in the cadaveric individuals and the landmarking/rearticulation error in the rearticulated pelves, demonstrating that the biological signal is stronger than the noise introduced by landmarking and rearticulation. The rearticulation process, however, underestimates the medio-lateral pelvic measurements in species with a substantial pubic gap (e.g., G. senegalensis, N. pygmaeus) possibly because the greater contribution of soft tissue to the pelvic girdle introduces higher uncertainty during rearticulation. Nevertheless, this discrepancy affects only the caudal-most part of the pelvis. This study demonstrates that the rearticulation of pelvic bones does not substantially affect the biological signal in comparative 3D morphological studies but suggests that anatomically connected pelves of species with wide pubic gaps should be preferentially included in these studies.

Association between ribs shape and pulmonary function in patients with Osteogenesis Imperfecta.

The aim of the present study was to test the hypothesis that ribs shape changes in patients with OI are more relevant for respiratory function than thoracic spine shape. We used 3D geometric morphometrics to quantify rib cage morphology in OI patients and controls, and to investigate its relationship with forced vital capacity (FVC) and forced expiratory volume in 1 s (FEV1), expressed as absolute value and as percentage of predicted value (% pred). Regression analyses on the full sample showed a significant relation between rib shape and FEV1, FVC and FVC % pred whereas thoracic spine shape was not related to any parameter. Subsequent regression analyses on OI patients confirmed significant relations between dynamic lung volumes and rib shape changes. Lower FVC and FEV1 values are identified in OI patients that present more horizontally aligned ribs, a greater antero-posterior depth due to extreme transverse curve at rib angles and a strong spine invagination, greater asymmetry, and a vertically short, thoraco-lumbar spine, which is relatively straight in at levels 1-8 and shows a marked kyphosis in the thoraco-lumbar transition. Our research seems to support that ribs shape is more relevant for ventilator mechanics in OI patients than the spine shape.

Rib cage anatomy in Homo erectus suggests a recent evolutionary origin of modern human body shape.

The tall and narrow body shape of anatomically modern humans (Homo sapiens) evolved via changes in the thorax, pelvis and limbs. It is debated, however, whether these modifications first evolved together in African Homo erectus, or whether H. erectus had a more primitive body shape that was distinct from both the more ape-like Australopithecus species and H. sapiens. Here we present the first quantitative three-dimensional reconstruction of the thorax of the juvenile H. erectus skeleton, KNM-WT 15000, from Nariokotome, Kenya, along with its estimated adult rib cage, for comparison with H. sapiens and the Kebara 2 Neanderthal. Our three-dimensional reconstruction demonstrates a short, mediolaterally wide and anteroposteriorly deep thorax in KNM-WT 15000 that differs considerably from the much shallower thorax of H. sapiens, pointing to a recent evolutionary origin of fully modern human body shape. The large respiratory capacity of KNM-WT 15000 is compatible with the relatively stocky, more primitive, body shape of H. erectus.

Workflows in a Virtual Morphology Lab: 3D scanning, measuring, and printing.

The aim of this paper is to give a practical overview, showing how recent available digital technology can be combined to build a laboratory capable to produce 3D (and reproduce in 3D) anatomical models for research, teaching and museum exhibitions on topics related to anatomy, morphology in natural sciences, biology and medicine. We present workflows in our Virtual Morphology Lab that can be used for research, training (museum, academic), and external service. We first review different surface scanning equipment and post-processing techniques that are useful for scanning in museum collections and provide technical recommendations for hard- and software as well as storing media on the web. This section is followed by an overview of available software packages for rigorous and effective 3D measurements of landmarks and sliding semi-landmarks, providing extensive supplementary information with guiding manuals for self-teaching in these cutting-edge but complicated research methods. We review briefly most recent work on virtual GM and describe ways for representing results in form of 3D images and 3D prints (outputs). The last part is dedicated to a summary of our experience in 3D-printing using FDM technology of differently sized printers and thermoplastic materials. Finally, we discuss the above-described workflows and its potential applications in research (paleo, biomedical), teaching and museums pedagogics.

Ribcage measurements indicate greater lung capacity in Neanderthals and Lower Pleistocene hominins compared to modern humans.

Our most recent fossil relatives, the Neanderthals, had a large brain and a very heavy body compared to modern humans. This type of body requires high levels of energetic intake. While food (meat and fat consumption) is a source of energy, oxygen via respiration is also necessary for metabolism. We would therefore expect Neanderthals to have large respiratory capacities. Here we estimate the pulmonary capacities of Neanderthals, based on costal measurements and physiological data from a modern human comparative sample. The Kebara 2 male had a lung volume of about 9.04 l; Tabun C1, a female individual, a lung volume of 5.85 l; and a Neanderthal from the El Sidrón site, a lung volume of 9.03 l. These volumes are approximately 20% greater than the corresponding volumes of modern humans of the same body size and sex. These results show that the Neanderthal body was highly sensitive to energy supply.

In Vivo 3D Analysis of Thoracic Kinematics: Changes in Size and Shape During Breathing and Their Implications for Respiratory Function in Recent Humans and Fossil Hominins.

The human ribcage expands and contracts during respiration as a result of the interaction between the morphology of the ribs, the costo-vertebral articulations and respiratory muscles. Variations in these factors are said to produce differences in the kinematics of the upper thorax and the lower thorax, but the extent and nature of any such differences and their functional implications have not yet been quantified. Applying geometric morphometrics we measured 402 three-dimensional (3D) landmarks and semilandmarks of 3D models built from computed tomographic scans of thoraces of 20 healthy adult subjects in maximal forced inspiration (FI) and expiration (FE). We addressed the hypothesis that upper and lower parts of the ribcage differ in kinematics and compared different models of functional compartmentalization. During inspiration the thorax superior to the level of the sixth ribs undergoes antero-posterior expansion that differs significantly from the medio-lateral expansion characteristic of the thorax below this level. This supports previous suggestions for dividing the thorax into a pulmonary and diaphragmatic part. While both compartments differed significantly in mean size and shape during FE and FI the size changes in the lower compartment were significantly larger. Additionally, for the same degree of kinematic shape change, the pulmonary thorax changes less in size than the diaphragmatic thorax. Therefore, variations in the form and function of the diaphragmatic thorax will have a strong impact on respiratory function. This has important implications for interpreting differences in thorax shape in terms of respiratory functional differences within and among recent humans and fossil hominins. Anat Rec, 300:255-264, 2017. © 2016 Wiley Periodicals, Inc.