Philipp Gunz

Advances in Geometric Morphometrics

Geometric morphometrics is the statistical analysis of form based on Cartesian landmark coordinates. After separating shape from overall size, position, and orientation of the landmark configurations, the resulting Procrustes shape coordinates can be used for statistical analysis. Kendall shape space, the mathematical space induced by the shape coordinates, is a metric space that can be approximated locally by a Euclidean tangent space. Thus, notions of distance (similarity) between shapes or of the length and direction of developmental and evolutionary trajectories can be meaningfully assessed in this space. Results of statistical techniques that preserve these convenient properties—such as principal component analysis, multivariate regression, or partial least squares analysis—can be visualized as actual shapes or shape deformations. The Procrustes distance between a shape and its relabeled reflection is a measure of bilateral asymmetry. Shape space can be extended to form space by augmenting the shape coordinates with the natural logarithm of Centroid Size, a measure of size in geometric morphometrics that is uncorrelated with shape for small isotropic landmark variation. The thin-plate spline interpolation function is the standard tool to compute deformation grids and 3D visualizations. It is also central to the estimation of missing landmarks and to the semilandmark algorithm, which permits to include outlines and surfaces in geometric morphometric analysis. The powerful visualization tools of geometric morphometrics and the typically large amount of shape variables give rise to a specific exploratory style of analysis, allowing the identification and quantification of previously unknown shape features.

Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution

This study addresses some enduring issues of ontogenetic and evolutionary integration in the form of the hominid cranium. Our sample consists of 38 crania: 20 modern adult Homo sapiens, 14 sub-adult H. sapiens, and four archaic Homo. All specimens were CT-scanned except for two infant H. sapiens, who were imaged by MR instead. For each specimen 84 landmarks and semi-landmarks were located on the midsagittal plane and converted to Procrustes shape coordinates. Integration was quantified by the method of singular warps, a new geometric-statistical approach to visualizing correlations among regions. The two classic patterns of integration, evolutionary and ontogenetic, were jointly explored by comparing analyses of overlapping subsamples that span ranges of different hypothetical factors. Evolutionary integration is expressed in the subsample of 24 adult Homo, and ontogenetic integration in the subsample of 34 H. sapiens. In this data set, vault, cranial base, and face show striking and localized patterns of covariation over ontogeny, similar but not identical to the patterns seen over evolution. The principal differences between ontogeny and phylogeny pertain to the cranial base. There is also a component of cranial length to height ratio not reducible to either process. Our methodology allows a separation of these independent processes (and their impact on cranial shape) that conventional methods have not found.

Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes.

Summary Heterochrony, the classic framework in which to study ontogeny and phylogeny, in essence relies on a univariate concept of shape. Though principal component (PC) plots of multivariate shape data seem to resemble classical bivariate allometric plots, the language of heterochrony cannot be translated directly into general multivariate methodology. We simulate idealized multivariate ontogenetic trajectories and explore their appearance in PC plots of shape space and size–shape space. Only if the trajectories of two related species lie along exactly the same path in shape space can the classic terminology of heterochrony apply and pure dissociation of size change against shape change be detected. Regional heterochrony—the variation of apparent heterochrony by region—implies a dissociation of local growth fields and cannot be identified in an overall PC analysis. We exemplify a geometric morphometric approach to these issues using adult and subadult crania of 48 Pan paniscus and 47 Pan troglodytes specimens. On each specimen, we digitized 47 landmarks and 144 semilandmarks on facial curves and the external neurocranial surface. We reject the hypothesis of global heterochrony in the cranium of Pan as well as regional heterochrony for the lower face, the upper face, and the neurocranium.

Brain development after birth differs between Neanderthals and modern humans

Summary Neanderthals had brain sizes comparable to modern humans, but their brain cases were elongated and not globular as in Homo sapiens [1,2]. It has, therefore, been suggested that modern humans and Neanderthals reached large brain sizes along different evolutionary pathways [2]. Here, we assess when during development these adult differences emerge. This is critical for understanding whether differences in the pattern of brain development might underlie potential cognitive differences between these two closely related groups. Previous comparisons of Neanderthal and modern human cranial development have shown that many morphological characteristics separating these two groups are already established at the time of birth [3–5], and that the subsequent developmental patterns of the face are similar, though not identical [6]. Here, we show that a globularization phase seen in the neurocranial development of modern humans after birth is absent from Neanderthals.

Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario

The interpretation of genetic evidence regarding modern human origins depends, among other things, on assessments of the structure and the variation of ancient populations. Because we lack genetic data from the time when the first anatomically modern humans appeared, between 200,000 and 60,000 years ago, instead we exploit the phenotype of neurocranial geometry to compare the variation in early modern human fossils with that in other groups of fossil Homo and recent modern humans. Variation is assessed as the mean-squared Procrustes distance from the group average shape in a representation based on several hundred neurocranial landmarks and semilandmarks. We find that the early modern group has more shape variation than any other group in our sample, which covers 1.8 million years, and that they are morphologically similar to recent modern humans of diverse geographically dispersed populations but not to archaic groups. Of the currently competing models of modern human origins, some are inconsistent with these findings. Rather than a single out-of-Africa dispersal scenario, we suggest that early modern humans were already divided into different populations in Pleistocene Africa, after which there followed a complex migration pattern. Our conclusions bear implications for the inference of ancient human demography from genetic models and emphasize the importance of focusing research on those early modern humans, in particular, in Africa.

Second to fourth digit ratio and face shape

The average human male face differs from the average female face in size and shape of the jaws, cheek-bones, lips, eyes and nose. It is possible that this dimorphism is determined by sex steroids such as testosterone (T) and oestrogen (E), and several studies on the perception of such characteristics have been based on this assumption, but those studies focussed mainly on the relationship of male faces with circulating hormone levels; the corresponding biology of the female face remains mainly speculative. This paper is concerned with the relative importance of prenatal T and E levels (assessed via the 2D : 4D finger length ratio, a proxy for the ratio of T/E) and sex in the determination of facial form as characterized by 64 landmark points on facial photographs of 106 Austrians of college age. We found that (i) prenatal sex steroid ratios (in terms of 2D : 4D) and actual chromosomal sex dimorphism operate differently on faces, (ii) 2D : 4D affects male and female face shape by similar patterns, but (iii) is three times more intense in men than in women. There was no evidence that these effects were confounded by allometry or facial asymmetry. Our results suggest that studies on the perception of facial characteristics need to consider differential effects of prenatal hormone exposure and actual chromosomal gender in order to understand how characteristics have come to be rated ‘masculine’ or ‘feminine’ and the consequences of these perceptions in terms of mate preferences.

The pattern of endocranial ontogenetic shape changes in humans

Humans show a unique pattern of brain growth that differentiates us from all other primates. In this study, we use virtual endocasts to provide a detailed description of shape changes during human postnatal ontogeny with geometric morphometric methods. Using CT scans of 108 dried human crania ranging in age from newborns to adults and several hundred landmarks and semi‐landmarks, we find that the endocranial ontogenetic trajectory is curvilinear with two bends, separating three distinct phases of shape change. We test to what extent endocranial shape change is driven by size increase and whether the curved ontogenetic trajectory can be explained by a simple model of modular development of the endocranial base and the endocranial vault. The hypothesis that endocranial shape change is driven exclusively by brain growth is not supported; we find changes in endocranial shape after adult size has been attained and that the transition from high rates to low rates of size increase does not correspond to one of the shape trajectory bends. The ontogenetic trajectory of the endocranial vault analyzed separately is nearly linear; the trajectory of the endocranial base, in contrast, is curved. The endocranial vault therefore acts as one developmental module during human postnatal ontogeny. Our data suggest that the cranial base comprises several submodules that follow their own temporally and/or spatially disjunct growth trajectories.

Enamel-dentine junction (EDJ) morphology distinguishes the lower molars of Australopithecus africanus and Paranthropus robustus

Tooth crown morphology plays a central role in hominin systematics, but the removal of the original outer enamel surface by dental attrition often eliminates from consideration the type of detailed crown morphology that has been shown to discriminate among hominin taxa. This reduces the size of samples available for study. The enamel-dentine junction (EDJ) is the developmental precursor and primary contributor to the morphology of the unworn outer enamel surface, and its morphology is only affected after considerable attrition. In this paper, we explore whether the form of the EDJ can be used to distinguish between the mandibular molars of two southern African fossil hominins: Paranthropus (or Australopithecus) robustus and Australopithecus africanus. After micro-computed tomographic scanning the molar sample, we made high-resolution images of the EDJ and used geometric morphometrics to compare EDJ shape differences between species, in addition to documenting metameric variation along the molar row within each species. Landmarks were collected along the marginal ridge that runs between adjacent dentine horns and around the circumference of the cervix. Our results suggest that the morphology of the EDJ can distinguish lower molars of these southern African hominins, and it can discriminate first, second, and third molars within each taxon. These results confirm previous findings that the EDJ preserves taxonomically valuable shape information in worn teeth. Mean differences in EDJ shape, in particular dentine horn height, crown height, and cervix shape, are more marked between adjacent molars within each taxon than for the same molar between the two taxa.

The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach

The bony labyrinth in the temporal bone houses the sensory systems of balance and hearing. While the overall structure of the semicircular canals and cochlea is similar across therian mammals, their detailed morphology varies even among closely related groups. As such, the shape of the labyrinth carries valuable functional and phylogenetic information. Here we introduce a new, semilandmark‐based three‐dimensional geometric morphometric approach to shape analysis of the labyrinth, as a major improvement upon previous metric studies based on linear measurements and angles. We first provide a detailed, step‐by‐step description of the measurement protocol. Subsequently, we test our approach using a geographically diverse sample of 50 recent modern humans and 30 chimpanzee specimens belonging to Pan troglodytes troglodytes and P. t. verus. Our measurement protocol can be applied to CT scans of different spatial resolutions because it primarily quantifies the midline skeleton of the bony labyrinth. Accurately locating the lumen centre of the semicircular canals and the cochlea is not affected by the partial volume and thresholding effects that can make the comparison of the outer border problematic. After virtually extracting the bony labyrinth from CT scans of the temporal bone, we computed its midline skeleton by thinning the encased volume. On the resulting medial axes of the semicircular canals and cochlea we placed a sequence of semilandmarks. After Procrustes superimposition, the shape coordinates were analysed using multivariate statistics. We found statistically significant shape differences between humans and chimpanzees which corroborate previous analyses of the labyrinth based on traditional measurements. As the geometric relationship among the semilandmark coordinates was preserved throughout the analysis, we were able to quantify and visualize even small‐scale shape differences. Notably, our approach made it possible to detect and visualize subtle, yet statistically significant (P = 0.009), differences between two chimpanzee subspecies in the shape of their semicircular canals. The ability to discriminate labyrinth shape at the subspecies level demonstrates that the approach presented here has great potential in future taxonomic studies of fossil specimens.

Discrimination of extant Pan species and subspecies using the enamel–dentine junction morphology of lower molars

Previous research has demonstrated that species and subspecies of extant chimpanzees and bonobos can be distinguished on the basis of the shape of their molar crowns. Thus, there is potential for fossil taxa, particularly fossil hominins, to be distinguished at similar taxonomic levels using molar crown morphology. Unfortunately, due to occlusal attrition, the original crown morphology is often absent in fossil teeth, and this has limited the amount of shape information used to discriminate hominin molars. The enamel-dentine junction (EDJ) of molar teeth preserves considerable shape information, particularly in regard to the original shape of the crown, and remains present through the early stages of attrition. In this study, we investigate whether the shape of the EDJ of lower first and second molars can distinguish species and subspecies of extant Pan. Micro-computed tomography was employed to non-destructively image the EDJ, and geometric morphometric analytical methods were used to compare EDJ shape among samples of Pan paniscus (N = 17), Pan troglodytes troglodytes (N = 13), and Pan troglodytes verus (N = 18). Discriminant analysis indicates that EDJ morphology distinguishes among extant Pan species and subspecies with a high degree of reliability. The morphological differences in EDJ shape among the taxa are subtle and relate to the relative height and position of the dentine horns, the height of the dentine crown, and the shape of the crown base, but their existence supports the inclusion of EDJ shape (particularly those aspects of shape in the vertical dimension) in the systematic analysis of fossil hominin lower molars.