Technical Note: Virtual reconstruction of KNM‐ER 1813 Homo habilis cranium

A very limiting factor for paleoanthropological studies is the poor state of preservation of the human fossil record, where fragmentation and deformation are considered normal. Although anatomical information can still be gathered from a distorted fossil, such specimens must typically be excluded from advanced morphological and morphometric analyses, thus reducing the fossil sample size and, ultimately, our knowledge of human evolution. In this contribution we provide the first digital reconstruction of the KNM‐ER 1813 Homo habilis cranium. Based on state of‐the‐art three‐dimensional digital modeling and geometric morphometric (GM) methods, the facial portion was aligned to the neurocranium, the overall distortion was removed, and the missing regions were restored. The reconstructed KNM‐ER 1813 allows for an adjustment of the anthropometric measurements gathered on the original fossil. It is suitable for further quantitative studies, such as GM analyses focused on skull morphology or for finite element analysis to explore the mechanics of early Homo feeding behavior and diet. Am J Phys Anthropol 153:154–160, 2014. © 2013 Wiley Periodicals, Inc.     

Variation among early North American crania

The limited morphometric work on early American crania to date has treated them as a single, temporally defined group. This paper addresses the question of whether there is significant variability among ancient American crania. A sample of 11 crania (Spirit Cave, Wizards Beach, Browns Valley, Pelican Rapids, Prospect, Wet Gravel male, Wet Gravel female, Medicine Crow, Turin, Lime Creek, and Swanson Lake) dating from the early to mid Holocene was available. Some have recent accelerator mass spectrometry (AMS) dates, while others are dated geologically or archaeologically. All are in excess of 4500 BP, and most are 7000 BP or older. Measurements follow the definitions of Howells [(1973) Cranial variation in man, Cambridge: Harvard University). Some crania are incomplete, but 22 measurements were common to all fossils. Cranial variation was examined by calculating the Mahalanobis distance between each pair of fossils, using a pooled within sample covariance matrix estimated from the data of Howells. The distance relationships among crania suggest the presence of at least three distinct groups: 1) a middle Archaic Plains group (Turin and Medicine Crow), 2) a Paleo/Early Archaic Great Lakes/Plains group (Browns Valley, Pelican Rapids, Lime Creek), and 3) a spatially and temporally heterogeneous group that includes the Great Basin/Pacific Coast (Spirit Cave, Wizards Beach, Prospect) and Nebraska (Wet Gravel specimens and Swanson Lake). These crania were also compared to Howells' worldwide recent sample, which was expanded by including six additional American Indian samples. None of the fossils, except for the Wet Gravel male, shows any particular affinity to recent Native Americans; their greatest similarities are with Europe, Polynesia, or East Asia. Several crania would be atypical in any recent population for which we have data. Browns Valley, Pelican Rapids, and Lime Creek are the most distinctive. They provide evidence for the presence of an early population that bears no similarity to the morphometric pattern of recent American Indians or even to crania of comparable date in other regions of the continent. The heterogeneity among early American crania makes it inadvisable to pool them for purposes of morphometric analysis. Whether this heterogeneity results from different early migrations or one highly differentiated population cannot be established from our data. Our results are inconsistent with hypotheses of an ancestor-descendent relationship between early and late Holocene American populations. They suggest that the pattern of cranial variation is of recent origin, at least in the Plains region.     

Discrimination of the sibling species Apodemus flavicollis and A. sylvaticus (Rodentia,Muridae)

Karyotyping and several molecular methods have allowed successful identification of two morphologically similar wide-ranging Western Palearctic species, the yellow-necked field mouse Apodemus flavicollis (Melchior, 1934) and the long-tailed wood mouse A. sylvaticus (Linnaeus, 1758), but reliable species diagnosis on the basis of morphometric characters is particularly problematic. Although they are easily morphologically distinguishable in Central and Northern Europe, this is not the case in southern parts of their distribution areas. Despite that, we have successfully discriminated A. flavicollis and A. sylvaticus from Serbia (Southern Europe) using geometric and traditional morphometric methods on a data set for ventral crania of specimens previously genotyped by the Inter Simple Sequence Repeat-PCR (ISSR-PCR). Discrimination power of applied approaches was more or less similar. The majority of our results were consistent with those obtained for specimens collected across the Czech Republic (Central Europe). Morphological differences observed herein, as well as those already reported between A. flavicollis and A. sylvaticus from the central and northern parts of their distribution areas, could be the outcome of their biology, i.e. ecological discrepancies, different assumed evolutionary scenarios considering biogeography, phylogeny, history and ontogeny.     

Evaluation of a New Method of Fossil Retrodeformation by Algorithmic Symmetrization: Crania of Papionins (Primates,Cercopithecidae) as a Test Case

Diagenetic distortion can be a major obstacle to collecting quantitative shape data on paleontological specimens, especially for three-dimensional geometric morphometric analysis. Here we utilize the recently -published algorithmic symmetrization method of fossil reconstruction and compare it to the more traditional reflection & averaging approach. In order to have an objective test of this method, five casts of a female cranium of Papio hamadryas kindae were manually deformed while the plaster hardened. These were subsequently “retrodeformed” using both algorithmic symmetrization and reflection & averaging and then compared to the original, undeformed specimen. We found that in all cases, algorithmic retrodeformation improved the shape of the deformed cranium and in four out of five cases, the algorithmically symmetrized crania were more similar in shape to the original crania than the reflected & averaged reconstructions. In three out of five cases, the difference between the algorithmically symmetrized crania and the original cranium could be contained within the magnitude of variation among individuals in a single subspecies of Papio. Instances of asymmetric distortion, such as breakage on one side, or bending in the axis of symmetry, were well handled, whereas symmetrical distortion remained uncorrected. This technique was further tested on a naturally deformed and fossilized cranium of Paradolichopithecus arvernensis. Results, based on a principal components analysis and Procrustes distances, showed that the algorithmically symmetrized Paradolichopithecus cranium was more similar to other, less-deformed crania from the same species than was the original. These results illustrate the efficacy of this method of retrodeformation by algorithmic symmetrization for the correction of asymmetrical distortion in fossils. Symmetrical distortion remains a problem for all currently developed methods of retrodeformation.     

Midsagittal cranial shape variation in the genus Homo by geometric morphometrics

Midsagittal profiles of crania referred to different taxa of the genus Homo have been analyzed by geometric morphometric techniques. Comparisons between single specimens using the thin-plate-spline function suggest a generalized reduction of the lower face, associated with antero-posterior development of the braincase occurring (possibly in parallel evolution) along distinct human lineages. Furthermore, Neandertals display a projection of the midface, and modern humans show a derived globularity of the vault associated with midsagittal parietal bulging. Principal Component Analysis demonstrates a bimodal pattern of variation, which describes an "archaic" pole (rather heterogeneous in terms of taxonomy) clearly distinguishable from the modern one. The first two principal components - that explain together 80% of the total variance in shape - involve respectively fronto-parietal expansion and midfacial prognathism. These results contribute to identify different structural patterns in human evolution, supporting discontinuity rather than continuity of cranial shape among different taxa of the genus Homo, especially when considering the differences between Neandertals and early modern humans.     

Are geometric morphometric analyses replicable? Evaluating landmark measurement error and its impact on extant and fossil Microtus classification

Geometric morphometric analyses are frequently employed to quantify biological shape and shape variation. Despite the popularity of this technique, quantification of measurement error in geometric morphometric datasets and its impact on statistical results is seldom assessed in the literature. Here, we evaluate error on 2D landmark coordinate configurations of the lower first molar of five North American Microtus (vole) species. We acquired data from the same specimens several times to quantify error from four data acquisition sources: specimen presentation, imaging devices, interobserver variation, and intraobserver variation. We then evaluated the impact of those errors on linear discriminant analysis‐based classifications of the five species using recent specimens of known species affinity and fossil specimens of unknown species affinity. Results indicate that data acquisition error can be substantial, sometimes explaining >30% of the total variation among datasets. Comparisons of datasets digitized by different individuals exhibit the greatest discrepancies in landmark precision, and comparison of datasets photographed from different presentation angles yields the greatest discrepancies in species classification results. All error sources impact statistical classification to some extent. For example, no two landmark dataset replicates exhibit the same predicted group memberships of recent or fossil specimens. Our findings emphasize the need to mitigate error as much as possible during geometric morphometric data collection. Though the impact of measurement error on statistical fidelity is likely analysis‐specific, we recommend that all geometric morphometric studies standardize specimen imaging equipment, specimen presentations (if analyses are 2D), and landmark digitizers to reduce error and subsequent analytical misinterpretations.     

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

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

Cranial morphological variation of Dromiciops gliroides (Microbiotheria) along its geographical distribution in south-central Chile: A three-dimensional analysis

We analyzed the variation in cranial morphology of the marsupial Dromiciops gliroides along its distribution in south-central Chile. We evaluated whether the cranial morphological variation is congruent with the phylogeographic structure previously observed in this species. We built three-dimensional models of 69 crania on which we digitized 30 landmarks. We used standard geometric morphometric methods to extract and analyze the shape and size components of the crania. Our data showed a subtle but consistent cranial size and shape variation along the studied distributional range, suggesting a geographic variation pattern rather than a phylogeographic structuring. Indeed, our multivariate analyses recovered a subtle morphological differentiation between island and mainland populations, contrary to what is suggested by a former phylogeographic study. We detected that either the cranial size variation, as well as the insularity and the latitude could be important factors underlying the cranial shape changes. We suggest that an interplay of historical and contemporary processes could be shaping the morphological pattern observed in this marsupial.     

Using geometric morphometric visualizations of directional selection gradients to investigate morphological differentiation

Researchers studying extant and extinct taxa are often interested in identifying the evolutionary processes that have lead to the morphological differences among the taxa. Ideally, one could distinguish the influences of neutral evolutionary processes (genetic drift, mutation) from natural selection, and in situations for which selection is implicated, identify the targets of selection. The directional selection gradient is an effective tool for investigating evolutionary process, because it can relate form (size and shape) differences between taxa to the variation and covariation found within taxa. However, although most modern morphometric analyses use the tools of geometric morphometrics (GM) to analyze landmark data, to date, selection gradients have mainly been calculated from linear measurements. To address this methodological gap, here we present a GM approach for visualizing and comparing between‐taxon selection gradients with each other, associated difference vectors, and “selection” gradients from neutral simulations. To exemplify our approach, we use a dataset of 347 three‐dimensional landmarks and semilandmarks recorded on the crania of 260 primate specimens (112 humans, 67 common chimpanzees, 36 bonobos, 45 gorillas). Results on this example dataset show how incorporating geometric information can provide important insights into the evolution of the human braincase, and serve to demonstrate the utility of our approach for understanding morphological evolution.     

三维几何形态测量方法在石制品分析中的应用

几何形态测量方法是生物学研究中用于形态特征分析和形态比较研究的一种常用方法。其核心思想是利用空间坐标点获取研究对象的形态数据,再通过坐标数据的多元统计分析,定量探讨研究对象的形态特征及影响其形态变异的因素。近年来,随着三维扫描技术的广泛应用以及对于石制品形态特征量化分析要求的提高,基于三维模型的几何形态测量方法开始出现在相关的旧石器考古研究中。本文首先对三维几何形态测量分析方法及其在石制品研究中的应用情况进行介绍,随后具体阐述了该方法的分析流程。为便于国内学者更好地了解这一方法,本文进一步以广西百色盆地南坡山遗址发现的手斧为例,利用三维几何形态测量方法对这些手斧的几何形态特征进行了初步探讨。三维几何形态测量方法为石制品形态研究提供了新思路和新视角,有望成为今后中国旧石器考古研究中一个重要的发展方向。     

Endocranial volume of Australopithecus africanus: new CT-based estimates and the effects of missing data and small sample size

Estimation of endocranial volume in Australopithecus africanus is important in interpreting early hominin brain evolution. However, the number of individuals available for investigation is limited and most of these fossils are, to some degree, incomplete and/or distorted. Uncertainties of the required reconstruction (‘missing data uncertainty’) and the small sample size (‘small sample uncertainty’) both potentially bias estimates of the average and within-group variation of endocranial volume in A. africanus.We used CT scans, electronic preparation (segmentation), mirror-imaging and semilandmark-based geometric morphometrics to generate and reconstruct complete endocasts for Sts 5, Sts 60, Sts 71, StW 505, MLD 37/38, and Taung, and measured their endocranial volumes (EV). To get a sense of the reliability of these new EV estimates, we then used simulations based on samples of chimpanzees and humans to: (a) test the accuracy of our approach, (b) assess missing data uncertainty, and (c) appraise small sample uncertainty.Incorporating missing data uncertainty of the five adult individuals, A. africanus was found to have an average adult endocranial volume of 454-461 ml with a standard deviation of 66-75 ml. EV estimates for the juvenile Taung individual range from 402 to 407 ml. Our simulations show that missing data uncertainty is small given the missing portions of the investigated fossils, but that small sample sizes are problematic for estimating species average EV. It is important to take these uncertainties into account when different fossil groups are being compared.     

Left,right or both? Estimating and improving accuracy of one‐side‐only geometric morphometric analyses of cranial variation

Procrustes‐based geometric morphometric analyses of bilaterally symmetric structures are often performed using only one side. This is particularly common in studies of cranial variation in mammals and other vertebrates. When one is not interested in quantifying asymmetry, landmarking one side, instead of both, reduces the number of variables as well as the time and costs of data collection. It is assumed that the loss of information in the other half, on which landmarks are not digitized, is negligible, but this has seldom been tested. Using 10 samples of mammalian crania and a total of more than 500 specimens, and five different landmark configurations, I demonstrate that this assumption is indeed easily met for size. For shape, in contrast, one‐side landmarking has potentially more severe consequences on the estimates of similarity relationships in a sample. In this respect, microevolutionary analyses of small differences are particularly affected, whereas macroevolutionary studies are fairly robust. In almost all instances, however, a simple preliminary operation improves accuracy by making one‐side‐only shape data more similar to those obtained by landmarking both sides. The same operation also makes estimates of allometry more accurate and improves the visualization. This operation consists in estimating the missing side by a mirror reflection of bilateral landmarks. In the Supporting Information, I exemplify how this can be easily done using free user‐friendly software. I also provide an example data set for readers to repeat and learn the steps of this simple procedure.     

Accuracy of femur reconstruction from sparse geometric data using a statistical shape model

Sparse geometric information from limited field-of-view medical images is often used to reconstruct the femur in biomechanical models of the hip and knee. However, the full femur geometry is needed to establish boundary conditions such as muscle attachment sites and joint axes which define the orientation of joint loads. Statistical shape models have been used to estimate the geometry of the full femur from varying amounts of sparse geometric information. However, the effect that different amounts of sparse data have on reconstruction accuracy has not been systematically assessed. In this study, we compared shape model and linear scaling reconstruction of the full femur surface from varying proportions of proximal and distal partial femur geometry in combination with morphometric and landmark data. We quantified reconstruction error in terms of surface-to-surface error as well as deviations in the reconstructed femur’s anatomical coordinate system which is important for biomechanical models. Using a partial proximal femur surface, mean shape model-based reconstruction surface error was 1.8 mm with 0.15° or less anatomic axis error, compared to 19.1 mm and 2.7–5.6° for linear scaling. Similar results were found when using a partial distal surface. However, varying amounts of proximal or distal partial surface data had a negligible effect on reconstruction accuracy. Our results show that given an appropriate set of sparse geometric data, a shape model can reconstruct full femur geometry with far greater accuracy than simple scaling.     

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.     

Comparison of cranial ontogenetic trajectories among great apes and humans

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

A comparative study of adult facial morphology and its ontogeny in the fossil macaque Macaca majori from Capo Figari, Sardinia, Italy

This study examines the morphology of the face in the fossil macaque Macaca majori from Capo Figari (north-eastern Sardinia, Italy) in a comparative ontogenetic context. Thus, a fairly complete face from an adult representative of this fossil species is compared with 3 extant macaque species: Macaca sylvanus (of which species it is questioned whether it is a subspecies, M. sylvanus majori), Macaca mulatta and Macaca fascicularis. Additional incomplete subadult and adult specimens are also examined in order to compare their facial ontogeny with that of the same living species. The comparisons are based on facial landmark data and are undertaken using geometric morphometric methods. These studies indicate that the adult facial morphology and ontogeny of face size and shape in M. majori share much in common with extant macaque species. However, the adult M. majori face displays some unique morphological features, in particular with regard to lateral flaring and relative size of the zygomatic roots. From the study of a limited sample of fossils there is an indication that this flaring arises during postnatal growth, and in consequence the ontogeny of the face of this fossil species may be different from that of M. sylvanus and the other macaque species included in this analysis. From these studies, we conclude that M. majori shows differences in adult facial morphology and possibly in ontogeny from M. sylvanus compatible with a specific rather than subspecific distinction.     

A geometric approach to cranial sexual dimorphism in the orang-utan

Adult craniofacial morphology is quantified and compared using Euclidean distance matrix analysis (EDMA), a three-dimensional morphometric method for the comparison of forms, which localizes form differences between comparative groups. Results indicate that the number and magnitude of differences between male and female crania are striking. The face, basicranium and neurocranium exhibit the most dimorphism, while the palate shows the least. Significant differences also exist between young adult and fully adult individuals, especially males, supporting the delayed onset of sexual maturity and secondary sex characteristics in males. As one of the many new morphometric techniques available, EDMA was useful for identifying local form difference and provides insights into the understanding of sexual dimorphism in this species beyond that obtained from traditional statistical methods based on linear caliper measurements.     

Geometric craniometric analysis of sexual dimorphism and ontogenetic variation: A case study based on two geographically disparate species, Aethomys ineptus from southern Africa and Arvicanthis niloticus from Sudan (Rodentia: Muridae)

Non-geographic morphometric variation, particularly at the level of sexual dimorphism and ontogenetic (age-related) variation, has been documented in rodents, and useful for establishing whether to analyse sexes separately or together, and for selecting adult specimens for subsequent data recording and analysis. However, such studies have largely been based on traditional morphometric analyses of linear measurements that mainly focus on overall size, rather than shape-related morphometric variation. Unit-free, landmark/outline-based geometric morphometric analyses are considered to offer a more appropriate tool for assessing shape-related morphometric variation. In this study, we used geometric cranial morphometric analysis to assess the nature and extent of sexual dimorphism and age variation within the Tete veld rat, Aethomys ineptus (Thomas and Wroughton, 1908) from southern Africa and the African Nile rat, Arvicanthis niloticus (Desmarest, 1822) from Sudan. The results obtained were in turn compared with previously published results based on independent geometric and traditional cranial morphometric data from the same sampled populations examined in the present study. While our geometric morphometric results detected statistically significant sexual dimorphism in cranial shape within Ar. niloticus only, previously published results based on traditional morphometric data failed to detect significant sexual dimorphism within this species. However, similar to previously published traditional morphometric data, our geometric morphometric results detected statistically significant age-related variation in cranial shape and size within both Ae. ineptus and Ar. niloticus, with individuals of age classes 5 and 6 being considered to represent adult specimens. Our results highlight the importance of carefully evaluating both size- and shape-related non-geographic morphometric variation prior to the analysis of geographic variation and the delineation of species. Erroneous conclusions of non-geographic variation may have implications in the interpretation of geographic and evolutionary processes that may be responsible for morphological differences at both the inter- and intra-specific levels.     

Determining best complete subsets of specimens and characters for multivariate morphometric studies in the presence of large amounts of missing data

Missing data are frequent in morphometric studies of both fossil and recent material. A common method of addressing the problem of missing data is to omit combinations of characters and specimens from subsequent analyses; however, omitting different subsets of characters and specimens can affect both the statistical robustness of the analyses and the resulting biological interpretations. We describe a method of examining all possible subsets of complete data and of scoring each subset by the 'condition' (ratio of first eigenvalue to second, or of second to first, depending on context) of the corresponding covariance or correlation matrix, and subsequently choosing the submatrix that either optimizes one of these criteria or matches the estimated condition of the original data matrix. We then describe an extension of this method that can be used to choose the 'best' characters and specimens for which some specified proportion of missing data can be estimated using standard imputation techniques such as the expectation-maximization algorithm or multiple imputation. The methods are illustrated with published and unpublished data sets on fossil and extant vertebrates. Although these problems and methods are discussed in the context of conventional morphometric data, they are applicable to many other kinds of data matrices.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 309–328.