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.     

The Neanderthal "chignon": variation, integration, and homology

The occipital bun ("chignon") is cited widely as a Neanderthal derived trait. It encompasses the posterior projection/convexity of the occipital squama and is associated with lambdoid flattening on the parietal. A 'hemibun' in some Upper Paleolithic Europeans is thought by some authors to indicate interbreeding between Neanderthals and early modern Europeans. However, 'bunning' is difficult to measure, and the term has been applied to a range of morphological patterns. Furthermore, its usefulness in phylogenetic reconstruction and its homologous status across modern and fossil humans have been disputed. We present a geometric morphometric study that quantitatively evaluates the chignon, assesses its usefulness in separating Neanderthals from modern humans, and its degree of similarity to Upper Paleolithic 'hemibuns.' We measured the three-dimensional coordinates of closely spaced points along the midsagittal plane from bregma to inion and of anatomical landmarks in a large series of recent human crania and several Middle and Late Pleistocene European and African fossils. These coordinate data were processed using the techniques of geometric morphometrics and analyzed with relative warps, canonical variates, and singular warps. Our results show no separation between Neanderthals and modern humans, including early modern Europeans, when the shape of the occipital plane midsagittal-profile is considered alone. On the other hand, Neanderthals are well separated from both recent and fossil modern humans when information about the occipital's relative position and relative size are also included. Furthermore, the occurrence of a highly convex and posteriorly projecting midline occipital profile (interpreted as the occipital bun) is highly correlated (>0.8) with a flat parietal midsagittal profile and with antero-superiorly positioned temporal bones across both our recent and our fossil human samples. We conclude that the shape of the occipital profile alone should not be considered an independent trait, as it is very tightly integrated with braincase shape. Our analysis does not support differences in integration of the posterior midsagittal profile and the cranial base in Pleistocene and recent humans.     

Craniometric variation among modern human populations

Previous studies of genetic markers and mitochondrial DNA have found that the amount of variation among major geographic groupings of Homo sapiens is relatively low, accounting for roughly 10% of total variation. This conclusion has had implications for the study of human variation and consideration of alternative models for the origin of modern humans. By contrast, it has often been assumed that the level of among-group variation for morphological traits is much higher. This study examines the level of among-group variation based on Craniometric data from a large sample of modern humans originally collected by W. W. Howells. A multivariate method based on quantitative genetics theory was used to provide an estimate of F_ST — a measure of among-group variation that can be compared with results from studies of genetic markers. Data for 57 Craniometric variables on 1,734 crania were analyzed. These data represent six core areas: Europe, Sub-Saharan Africa, Australasia, Polynesia, the Americas, and the Far East. An additional set of analyses was performed using a three-region subset (Europe, Sub-Saharan Africa, and the Far East) to provide comparability with several genetic studies. The minimum F_ST (assuming complete heritability) for the three-region analysis is 0.065, and the minimum F_ST for the six-region analysis is 0.085. Both of these are less than the average F_ST from genetic studies (average estimates of 0.10–0.11). The smaller value of the minimum F_ST estimates is expected since it provides an estimate of F_ST expected under complete heritability. Using an estimate of average craniometric heritability from the literature provides an estimate of F_ST of 0.112 for the three-region analysis and 0.144 for the six-region analysis. These results show that genetic and craniometric data are in agreement, qualitatively and quantitatively, and that there is limited variation in modern humans among major geographic regions. © 1994 Wiley-Liss, Inc.     

Reexamination of the immature hominid maxilla from Tangier,Morocco

Reexamination of the immature Upper Pleistocene hominid maxilla from Mugharet el-'Aliya (Tangier), Morocco is undertaken in light of new evidence on the growth and development of Upper Pleistocene hominids. Metric and qualitative comparisons were made with 17 immature Upper Pleistocene maxillae, and with a recent Homo sapiens sapiens sample. No unambiguous criteria for aligning the maxilla with Neandertals were found, although one character, the degree of maxillary flexion on the zygoma, strongly suggests that this child could be a representative of H. s. sapiens. The probable lack of a canine fossa in Mugharet el-'Aliya 1, the primary criterion used previously to align it with Neandertals, cannot be accurately extrapolated to its adult form from this juvenile. The present evidence suggests that it is inappropriate to refer to this fossil as “Neandertal-like” or as a North African “neandertaloid.” Thus, the Tangier maxilla should not be cited as evidence for the presence of Neandertal facial features in North Africa during the Upper Pleistocene. © 1993 Wiley-Liss, Inc.     

Into Eurasia: A geometric morphometric re-assessment of the Upper Cave (Zhoukoudian) specimens

Since the discovery of the human remains from the Upper Cave of Zhoukoudian in the 1930s there has been speculation over their affinities. In particular, the degree to which the three adult crania exhibit recent East Asian morphology, as well as their degree of within-group variability, has long been debated. Several early researchers described a resemblance to East Asian populations, but these findings have been for the most part rejected by more recent metric and non-metric analyses. Nevertheless, the Upper Cave specimens have not been classified conclusively into any recent modern human population to which they have been compared, and classification results differ for each cranium. Here, the question of the affinities of Upper Cave 101 and 103, the two better-preserved crania, is examined from the perspective of the Late Pleistocene human fossil record using the methodology of 3-D geometric morphometrics. The degree of morphological variation between the two specimens is also evaluated within the context of recent population variability. Neurocranial and facial morphology are analyzed separately so as to maximize comparative samples. Results show a morphological resemblance of the Upper Cave material to Upper Paleolithic Europeans. It is proposed that the Upper Cave specimens retain important aspects of modern human ancestral morphology, and possibly share a recent common ancestral population with Upper Paleolithic Europeans, in accordance with the Single Origin model of modern human origins.     

Nonhuman primate hybridization and the taxonomic status of Neanderthals

The present study examines the taxonomic status of Middle Paleolithic Neanderthals by comparing their observed minimum genetic divergence from Upper Paleolithic modern humans in Europe with that observed between macaque species from Sulawesi that are known to hybridize and fully intergrade in the wild. The genetic divergence, and differentiation between Neanderthals and Upper Paleolithic modern humans, as indicated by pairwise minimum genetic distances and F(ST) values calculated from the estimated minimum genetic relationship (R) matrix derived from craniometric data, are significantly greater than those observed both between hybridizing and noninterbreeding Sulawesi macaque species, suggesting that mate recognition and the possibility of gene flow between Neanderthals and Upper Paleolithic modern humans might have been greatly reduced. These results support a species-level taxonomic distinction for the Neanderthals as suggested by proponents of the replacement model. Furthermore, assumptions regarding the monophyletic origin of modern humans from outside Europe are likely valid.     

The taxonomic implications of cranial shape variation in Homo erectus

The taxonomic status of Homo erectus sensu lato has been a source of debate since the early 1980s, when a series of publications suggested that the early African fossils may represent a separate species, H. ergaster. To gain further resolution regarding this debate, 3D geometric morphometric data were used to quantify overall shape variation in the cranial vault within H. erectus using a new metric, the sum of squared pairwise Procrustes distances (SSD). Bootstrapping methods were used to compare the H. erectus SSD to a broad range of human and nonhuman primate samples in order to ascertain whether variation in H. erectus most clearly resembles that seen in one or more species. The reference taxa included relevant phylogenetic, ecological, and temporal analogs including humans, apes, and both extant and extinct papionin monkeys. The mean cranial shapes of different temporogeographic subsets of H. erectus fossils were then tested for significance using exact randomization tests and compared to the distances between regional groups of modern humans and subspecies/species of the ape and papionin monkey taxa. To gauge the influence of sexual dimorphism on levels of variation, comparisons were also made between the mean cranial shapes of single-sex samples for the reference taxa. Results indicate that variation in H. erectus is most comparable to single species of papionin monkeys and the genus Pan, which included two species. However, H. erectus encompasses a limited range of variation given its extensive geographic and temporal range, leading to the conclusion that only one species should be recognized. In addition, there are significant differences between the African/Georgian and Asian H. erectus samples, but not between H. ergaster (Georgia+Africa, excluding OH 9 and Daka) and H. erectus sensu stricto. This finding is in line with expectations for intraspecific variation in a long-lived species with a wide, but probably discontinuous, geographic distribution.     

The Vindija Neanderthal scapular glenoid fossa: comparative shape analysis suggests evo-devo changes among Neanderthals

Although the shape of the scapular glenoid fossa (SGF) may be influenced by epigenetic and developmental factors, there appears to be strong genetic control over its overall form, such that variation within and between hominin taxa in SGF shape may contain information about their evolutionary histories. Here we present the results of a geometric morphometric study of the SGF of the Neanderthal Vi-209 from Vindjia Cave (Croatia), relative to samples of Plio-Pleistocene, later Pleistocene, and recent hominins. Variation in overall SGF shape follows a chronological trend from the plesiomorphic condition seen in Australopithecus to modern humans, with pre-modern species of the genus Homo exhibiting intermediate morphologies. Change in body size across this temporal series is not linearly directional, which argues against static allometry as an explanation. However, life history and developmental rates change directionally across the series, suggesting an ontogenetic effect on the observed changes in shape (ontogenetic allometry). Within this framework, the morphospace occupied by the Neanderthals exhibits a discontinuous distribution. The Vindija SGF and those of the later Near Eastern Neanderthals (Kebara and Shanidar) approach the modern condition and are somewhat segregated from both northwestern European (Neandertal and La Ferrassie) and early Mediterranean Neanderthals (Krapina and Tabun). Although more than one scenario may account for the pattern seen in the Neanderthals, the data is consistent with palaeogenetic evidence suggesting low levels of gene flow between Neanderthals and modern humans in the Near East after ca. 120-100 ka (thousands of years ago) (with subsequent introgression of modern human alleles into eastern and central Europe). Thus, in keeping with previous analyses that document some modern human features in the Vindija Neanderthals, the Vindija G₃ sample should not be seen as representative of ‘classic’ - that is, unadmixed, pre-contact - Neanderthal morphology.     

Ontogeny of robusticity of craniofacial traits in modern humans: A study of South American populations

To date, differences in craniofacial robusticity among modern and fossil humans have been primarily addressed by analyzing adult individuals; thus, the developmental basis of such differentiation remains poorly understood. This article aims to analyze the ontogenetic development of craniofacial robusticity in human populations from South America. Geometric morphometric methods were used to describe cranial traits in lateral view by using landmarks and semilandmarks. We compare the patterns of variation among populations obtained with subadults and adults to determine whether population‐specific differences are evident at early postnatal ontogeny, compare ontogenetic allometric trajectories to ascertain whether changes in the ontogeny of shape contribute to the differentiation of adult morphologies, and estimate the amount of size change that occurs during growth along each population‐specific trajectory. The results obtained indicate that the pattern of interpopulation variation in shape and size is already established at the age of 5 years, meaning that processes acting early during ontogeny contribute to the adult variation. The ontogenetic allometric trajectories are not parallel among all samples, suggesting the divergence in the size‐related shape changes. Finally, the extension of ontogenetic trajectories also seems to contribute to shape variation observed among adults. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Comparison of dental measurement systems for taxonomic assignment of Neanderthal and modern human lower second deciduous molars

Traditional morphometric approaches for taxonomic assignment of Neanderthal and modern human dental remains are mainly characterized by caliper measurements of tooth crowns. Several studies have recently described differences in dental tissue proportions and enamel thickness between Neanderthal and modern human teeth. At least for the lower second deciduous molar (dm₂), a three-dimensional lateral relative enamel thickness index has been proposed for separating the two taxa. This index has the advantage over other measurements of being applicable to worn teeth because it ignores the occlusal aspect of the crown. Nevertheless, a comparative evaluation of traditional crown dimensions and lateral dental tissue proportion measurements for taxonomic assignment of Neanderthal and modern human dm₂s has not yet been performed.In this study, we compare various parameters gathered from the lateral aspects of the crown. These parameters include crown diameters, height of the lateral wall of the crown (lateral crown height = LCH), lateral enamel thickness, and dentine volume of the lateral wall, including the volume of the coronal pulp chamber (lateral dentine plus pulp volume = LDPV), in a 3D digital sample of Neanderthal and modern human dm₂s to evaluate their utility in separating the two taxa.The LDPV and the LCH allow us to discriminate between Neanderthals and modern humans with 88.5% and 92.3% accuracy, respectively. Though our results confirm that Neanderthal dm₂s have lower relative enamel thickness (RET) index compared with modern humans (p = 0.005), only 70% of the specimens were correctly classified on the basis of the RET index. We also emphasize that results of the lateral enamel thickness method depend on the magnitude of the interproximal wear. Accordingly, we suggest using the LCH or the LDPV to discriminate between Neanderthal and modern human dm₂s. These parameters are more independent of interproximal wear and loss of lateral enamel.     

大蹄蝠头骨形态地理变化

本文采用几何形态测量法对中国大蹄蝠9个不同地理种群头骨形态变化进行研究。结果表明,不同地理种群的头骨大小及形状存在显著差异,其中云南思茅种群与海南陵水种群差异最大。回归分析表明头骨形态的地理变化与气候因素相关。随着年均温度、年均湿度的升高以及年均降水量的增多,大蹄蝠头骨变小,上颌、齿、咬肌附着部分以及耳蜗部分的形状发生变化。此外,头骨大小与海拔高度呈正相关,头骨形状变化与纬度显著相关。本研究表明对栖息地生态条件的适应是中国大蹄蝠头骨形态地理变化的重要原因。     

Regional isolation in the Balkan region: an analysis of craniofacial variation

Biological variation is investigated among contemporary Croatians, Bosnians, American whites, and other multitemporal Balkan populations (World War II Croatians, Macedonians, and Greeks) via multivariate statistics and distance measures of the craniofacial complex. This study demonstrates that there is considerable variation among groups of European ancestry. Bosnians and Croatians who are thought to be relatively homogenous and historically to originate from the same Slav ancestry show local variations. While environmental plasticity has been used to explain cranial changes among human groups, it does not adequately explain the variation observed between Bosnians and Croatians. It is an oversimplification to exclusively attribute the vast range of variability observed among local as well as geographic populations to environmental adaptations.     

人类股骨断面面积与形状的不对称性——基于三维激光扫描的形态测量分析

人类股骨横断面面积、形状及其左右侧差异记载的人类演化、人群差异及生存活动的重要信息一直为古人类学研究所关注。多年来, 对股骨断面的研究通常采用破坏性地切割或者制作模型的方法。本文利用三维激光表面扫描技术, 无损、快捷、方便地获取了20对现代中国人左右侧股骨外轮廓的三维数据, 采用CAD软件及几何形态测量方法对两侧股骨断面轮廓的大小及形状进行了对比和分析。初步研究结果发现: 两侧股骨的横断面相对面积差异极其显著, 绝对面积差异不显著, 不对称方式表现为波动不对称性, 而不是偏向不对称性; 个体之间两侧股骨横断面外轮廓形状的波动不对称性极其显著, 偏向不对称性虽有差异但不显著; 平均形状和面积分析结果似乎表明股骨稍有偏左侧优势。虽然本文所采用的标本量有限, 所得出的结论需要更多标本的进一步验证, 但是, 本文的研究结果提示利用三维激光扫描技术获取股骨横断面外轮廓数据, 并采用形态测量方法分析确实能够揭示出一些以往研究方法不能发现的重要信息, 这种研究骨骼不对称性的新方法值得进一步的应用。     

Femoral curvature in Neanderthals and modern humans: a 3D geometric morphometric analysis

Since their discovery, Neanderthals have been described as having a marked degree of anteroposterior curvature of the femoral shaft. Although initially believed to be pathological, subsequent discoveries of Neanderthal remains lead femoral curvature to be considered as a derived Neanderthal feature. A recent study on Neanderthals and middle and early Upper Palaeolithic modern humans found no differences in femoral curvature, but did not consider size-corrected curvature. Therefore, the objectives of this study were to use 3D morphometric landmark and semi-landmark analysis to quantify relative femoral curvature in Neanderthals, Upper Palaeolithic and recent modern humans, and to compare adult bone curvature as part of the overall femoral morphology among these populations.Comparisons among populations were made using geometric morphometrics (3D landmarks) and standard multivariate methods. Comparative material involved all available complete femora from Neanderthal and Upper Palaeolithic modern human, archaeological (Mesolithic, Neolithic, Medieval) and recent human populations representing a wide geographical and lifestyle range. There are significant differences in the anatomy of the femur between Neanderthals and modern humans. Neanderthals have more curved femora than modern humans. Early modern humans are most similar to recent modern humans in their anatomy. Femoral curvature is a good indicator of activity level and habitual loading of the lower limb, indicating higher activity levels in Neanderthals than modern humans. These differences contradict robusticity studies and the archaeological record, and would suggest that femoral morphology, and curvature in particular, in Neanderthals may not be explained by adult behavior alone and could be the result of genetic drift, natural selection or differences in behavior during ontogeny.