Technical note: A novel geometric morphometric approach to the study of long bone shape variation

Procrustes‐based geometric morphometrics (GM) is most often applied to problems of craniofacial shape variation. Here, we demonstrate a novel application of GM to the analysis of whole postcranial elements in a study of 77 hominoid tibiae. We focus on two novel methodological improvements to standard GM approaches: 1) landmark configurations of tibiae including 15 epiphyseal landmarks and 483 semilandmarks along articular surfaces and muscle insertions along the tibial shaft and 2) an artificial affine transformation that sets moments along the shaft equal to the sum of the moments estimated in the other two anatomical directions. Diagrams of the principal components of tibial shapes support most differences between human and non‐human primates reported previously. The artificial affine transformation proposed here results in an improved clustering of the great apes that may prove useful in future discriminant or clustering studies. Since the shape variations observed may be related to different locomotor behaviors, posture, or activity patterns, we suggest that this method be used in functional analyses of tibiae or other long bones in modern populations or fossil specimens. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Variation in cross‐sectional horn shape within and among rhinoceros beetle species

Sexual selection has equipped male rhinoceros beetles with large horns on their head and prothorax to aid in battle over access to females. Horns are used to pry and dislodge opponents from resource sites that attract females, so an optimal horn should be able both to withstand the high stresses imposed during fights, and to resist deflection in response to these loads. We examined the cross‐sectional morphology of horns using micro‐computed tomography scanning to determine how horn structure changes with horn length to withstand the different fighting loads. Specifically, we measured the second moment of area of horns within and among rhinoceros beetle species to assess whether changes in cross‐sectional morphology accompany changes in body size in order to maintain high strength and stiffness during fights. We find that the second moment of area of horns increases with body size both intra‐specifically and inter‐specifically, and that these relationships closely fit those predicted if horns have been selected to be strong and stiff fighting structures. Our results therefore support the hypothesis that rhinoceros beetle horns are structurally adapted for combat.     

Periosteal versus true cross‐sectional geometry: A comparison along humeral,femoral, and tibial diaphyses

Cross‐sectional geometric (CSG) properties of human long bone diaphyses are typically calculated from both periosteal and endosteal contours. Though quantification of both is desirable, periosteal contours alone have provided accurate predictions of CSG properties at the midshaft in previous studies. The relationship between CSG properties calculated from external contours and “true” (endosteal and periosteal) CSG properties, however, has yet to be examined along the whole diaphysis. Cross‐sectional computed tomography scans were taken from 21 locations along humeral, femoral, and tibial diaphyses in 20 adults from a late prehistoric central Illinois Valley cemetery. Mechanical properties calculated from images with (a) artificially filled medullary cavities (“solid”) and (b) true unaltered cross‐sections were compared at each section location using least squares regression. Results indicate that, in this sample, polar second moments of area (J), polar section moduli (Z_p), and cross‐sectional shape (I_max/I_min) calculated from periosteal contours correspond strongly with those calculated from cross‐sections that include the medullary cavity. Correlations are high throughout most of the humeral diaphysis and throughout large portions of femoral and tibial diaphyses (R² = 0.855–0.998, all P < 0.001, %SEE ≤ 8.0, %PE ≤ 5.0), the major exception being the proximal quarter of the tibial diaphysis for J and Z_p. The main source of error was identified as variation in %CA. Results reveal that CSG properties quantified from periosteal contours provide comparable results to (and are likely to detect the same differences among individuals as) true CSG properties along large portions of long bone diaphyses. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys

Aim To examine and visualize clines in size and shape of Cercopithecus aethiops Linneus, 1758 (Primate, Cercopithecidae) skulls, and to investigate environmental factors which might best explain the observed variation. Location Sub‐Saharan Africa. Methods Eighty‐six three‐dimensional anatomical landmarks were used to describe 306 skulls of adult C. aethiops sampled over its entire distribution. Geometric morphometric methods for the quantitative analysis of form variation were applied. Size and shape variables were computed and regressed onto geographical coordinates and environmental variables (elevation, temperature, rainfall, moisture and Shannon rainfall diversity index) using both linear and curvilinear models. Components (geographical, environmental, spatially structured environmental and residual) of ecogeographical variation in skull form were partitioned using partial regression. A novel approach for summarizing and visualizing nonlinear patterns of clinal variation using surface rendering of three‐dimensional shapes is presented. Results Clinal variation in size and shape was highly significant, and was best described by curvilinear models. There were strong similarities between females and males. The cline in size was especially pronounced, explaining up to about 40% of observed variation, and was mainly longitudinal rather than latitudinal. A major trend of clinal shape variation also occurred from west to east, and corresponded to an expansion of the face relative to the neurocranium in the west. In the east, skulls also tended to be deeper and with narrower zygomatic arches. Geography and the spatially structured environmental component were the major contributors to the explained variance in size in both sexes, but the proportion of variance explained by the latter was smaller in females. In contrast, geography and environment explained similar amounts of variation in shape and their contribution was about twice that of the spatially structured environmental component. About 60–80% of variation in skull form was not explained by any variable in the analysis. The main factors influencing skull size differed in females and males, with rainfall being very influential in males. Both female and male skull shapes were strongly affected by average annual rainfall. Main conclusions A strong spatial and environmental basis to variations in African vervet monkey skull form was evident. However, the observed pattern did not conform to predictions based on Bergmann's rule. Rainfall consistently emerged as an important predictor, which may contribute to intraspecific variation in the size and shape of vervet monkey skulls through its effect on habitat productivity.     

A 3D geometric morphometric analysis of digging ability in the extant and fossil cingulate humerus

Digging ability in armadillos has been shown to be closely related to the relative length of the olecranon process of the ulna. This study uses geometric morphometrics to examine the relationship between humeral shape, digging ability and size in a range of living and fossil cingulates. The extant species in the sample include representatives of 11 species of armadillo, while the fossil specimens include three species of fossil armadillos ( Peltephilus, Proeutatus and Eutatus ) and three Glyptodonts ( Propalaeohoplophorus, Glyptodon and Neosclerocalyptus ). The results show that in general, living species with good digging ability have larger sites for muscle attachment, particularly the proximal tubercles and the crests descending therefrom, and the epicondylar region at the distal end of the humerus. Some differences were found in the smallest armadillo ( Chlamyphorus truncatus ), which seems to have a different method of digging. The proportions of the olecranon process would indicate good digging ability in some glyptodonts, but humeral features do not fit with this interpretation and the differences may be related to large size. The relationship between cingulate phylogeny and humeral morphology is also examined, and it seems that while cingulates are to some extent constrained by their phylogeny, many of the humeral features are directly related to digging.     

A geometric morphometric approach to the analysis of skull shape in Triassic dicynodonts (Therapsida,Anomodontia) from South America

Dicynodont therapsids were a major component of the Permo-Triassic terrestrial ecosystems across Pangea and have been regarded as specialized herbivores. In South America, the group was represented by several taxa of the clade Kannemeyeriiformes spanning from the Middle to the Late Triassic. In order to evaluate if cranial differences among taxa are potentially related to differences in feeding function, we performed a geometric morphometric analysis on 28 South American dicynodont crania. We digitized 19 cranial landmarks and conducted generalized Procrustes analysis, principal component analysis (PCA), principal component analysis between groups (bg-PCA), and a branch weighted squared-change parsimony approach. Phylogenetic inertia was not a significant driver of cranial shape evolution in the group, whereas PCA and bg-PCA support that major morphological shape differences are concentrated in the preorbital region (relative length of the snout and width of the caniniform process), in the position of quadrate condyle in relation to the caniniform process, and in the increase in the intertemporal surface area. In this context, tusked Dinodontosaurus, “Kannemeyeria,” and Vinceria have relatively smaller adductor attachment areas and input moment arm than younger taxa lacking tusks, such as Ischigualastia, Stahleckeria, and Jachaleria. Differences in cranial morphology in later dicynodonts reflect modifications in feeding mechanics, probably due to changes in food resources (vegetation) in their habitats toward the end of the Triassic.     

Evolution of skull and body shape in Triturus newts reconstructed from three‐dimensional morphometric data and phylogeny

To explore the relationship between morphological change and species diversification, we reconstructed the evolutionary changes in skull size, skull shape, and body elongation in a monophyletic group of eight species that make up salamander genus Triturus. Their well‐studied phylogenetic relationships and the marked difference in ecological preferences among five species groups makes this genus an excellent model system for the study of morphological evolution. The study involved three‐dimensional imagery of the skull and the number of trunk vertebrae, in material that represents the morphological, spatial, and molecular diversity of the genus. Morphological change largely followed the pattern of descent. The reconstruction of ancestral skull shape indicated that morphological change was mostly confined to two episodes, corresponding to the ancestral lineage that all crested newts have in common and the Triturus dobrogicus lineage. When corrected for common descent, evolution of skull shape was correlated to change in skull size. Also, skull size and shape, as well as body shape, as inferred from the number of trunk vertebrae, were correlated, indicating a marked impact of species' ecological preferences on morphological evolution, accompanied by a series of niche shifts, with the most pronounced one in the T. dobrogicus lineage. The presence of phylogenetic signal and correlated evolutionary changes in skull and body shape suggested complex interplay of niche shifts, natural selection, and constraints by a common developmental system. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 243–255.     

A 3-D geometric morphometric study of intraspecific variation in the ontogeny of the temporal bone in modern Homo sapiens

This study addresses how the human temporal bone develops the population-specific pattern of morphology observed among adults and at what point in ontogeny those patterns arise. Three-dimensional temporal bone shape was captured using 15 landmarks on ontogenetic series of specimens from seven modern human populations. Discriminant function analysis revealed that population-specific temporal bone morphology is evident early in ontogeny, with significant shape differences among many human populations apparent prior to the eruption of the first molar. As early as five years of age, temporal bone shape reflects population history and can be used to reliably sort populations, although those in closer geographic proximity and molecular affinity are more likely to be misclassified. The deviation of cold-adapted populations from this general pattern of congruence between temporal bone morphology and genetic distances, identified in previous work, was confirmed here in adult and subadult specimens, and was revealed to occur earlier in ontogeny than previously recognized. Significant differences exist between the ontogenetic trajectories of some pairs of populations, but not among others, and the angles of these trajectories do not reflect genetic relationships or final adult temporal bone size. Significant intrapopulation differences are evident early in ontogeny, with differences becoming amplified by divergent trajectories in some groups. These findings elucidate how the congruence between adult human temporal bone morphology and population history develops, and reveal that this pattern corresponds closely to that described previously for facial ontogeny.     

The Mousterian child from Teshik‐Tash is a Neanderthal: A geometric morphometric study of the frontal bone

In the 1930s subadult hominin remains and Mousterian artifacts were discovered in the Teshik‐Tash cave in South Uzbekistan. Since then, the majority of the scientific community has interpreted Teshik‐Tash as a Neanderthal. However, some have considered aspects of the morphology of the Teshik‐Tash skull to be more similar to fossil modern humans such as those represented at Skhūl and Qafzeh, or to subadult Upper Paleolithic modern humans. Here we present a 3D geometric morphometric analysis of the Teshik‐Tash frontal bone in the context of developmental shape changes in recent modern humans, Neanderthals, and early modern humans. We assess the phenetic affinities of Teshik‐Tash to other subadult fossils, and use developmental simulations to predict possible adult shapes. We find that the morphology of the frontal bone places the Teshik‐Tash child close to other Neanderthal children and that the simulated adult shapes are closest to Neanderthal adults. Taken together with genetic data showing that Teshik‐Tash carried mtDNA of the Neanderthal type, as well as its occipital bun, and its shovel‐shaped upper incisors, these independent lines of evidence firmly place Teshik‐Tash among Neanderthals. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

A three‐dimensional geometric morphometric study of the development of sulcus versus shell outline in Permian neospiriferine brachiopods

The morphological variation of the sulcal development and shell outline in large Permian neospiriferine brachiopods including Fasciculatia Waterhouse, 2004 is investigated using geometric morphometrics. The sulcal tongues of spiriferide brachiopods can be, in a qualitative sense, categorized into three types according to the degree of their development: short sulcal tongue, long sulcal tongue and geniculated sulcal tongue. All three types have been noted within Fasciculatia striatoparadoxa, regardless of the nature of the substrate which they originally inhabited. To quantify its morphological variation both in sulcal development and shell outline, 51 brachiopod shells were scanned with a three‐dimensional (3‐D) surface imaging device, and their 3‐D models were reconstructed. Using two landmarks and 58 semilandmarks designated on the surface of the reconstructed 3‐D models, a landmark‐based morphometric analysis was performed. Our result demonstrates a significant intraspecific variation of sulcal development in F. striatoparadoxa and its relatives. Local environmental factors, especially the intensity of ambient water flow, are invoked as the most likely cause for this intraspecific variation. Additionally, this study also shows that there are considerable interspecific distinctions in shell outline among Fasciculatia species, independent of the high variation in the sulcal development. The strong stability of overall shell outline at species level implies a decoupled morphological development between sulcal tongue and whole shell outline. The 3‐D morphometric approach applied here demonstrates its great utility as a tool for quantifying and analysing the morphological variation of highly convex brachiopod shells.     

Patterns of morphospace occupation and mechanical performance in extant crocodilian skulls: A combined geometric morphometric and finite element modeling approach

Extant and fossil crocodilians have long been divided into taxonomic and/or ecological groups based on broad patterns of skull shape, particularly the relative length and width of the snout. However, these patterns have not been quantitatively analyzed in detail, and their biomechanical and functional implications are similarly understudied. Here, we use geometric morphometrics and finite element analysis to explore the patterns of variation in crocodilian skull morphology and the functional implications of those patterns. Our results indicate that skull shape variation in extant crocodiles is much more complex than previously recognized. Differences in snout length and width are the main components of shape variation, but these differences are correlated with changes in other regions of the skull. Additionally, there is considerable disparity within general classes such as longirostrine and brevirostrine forms. For example, Gavialis and Tomistoma occupy different parts of morphospace implying a significant difference in skull shape, despite the fact that both are traditionally considered longirostrine. Skull length and width also strongly influence the mechanical performance of the skull; long and narrow morphotypes (e.g., Tomistoma) experience the highest amount of stress during biting, whereas short and broad morphotypes (e.g., Caiman latirostris) experience the least amount of stress. Biomechanical stress and the hydrodynamic properties of the skull show a strong relationship with the distribution of crocodilians in skull morphospace, whereas phylogeny and biogeography show weak or no correlation. Therefore, ecological specializations related to feeding and foraging likely have the greatest influence on crocodilian skull shape. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Cranial ontogeny in the Puma lineage,Puma concolor,Herpailurus yagouaroundi,and Acinonyx jubatus (Carnivora: Felidae): a three‐dimensional geometric morphometric approach

The Puma lineage is a monophyletic group that includes three living species: Puma concolor, Herpailurus yagouaroundi, and Acinonyx jubatus. It has been analysed from ecological and taxonomic perspectives, but their cranial ontogeny has been poorly studied. In this study, we assessed the cranial shape and size variation through three‐dimensional geometric morphometric techniques, and explored the acquisition of definitive shape and size in relation to key life‐history events. Each species occupied different locations in the shape morphospace: A. jubatus and P. concolor showed shorter and wider skulls, with more expanded zygomatic arches, than H. yagouaroundi, which presented the most divergent pattern of change. Ontogeny was more similar between P. concolor and A. jubatus than between the closely related P. concolor and H. yagouaroundi. The evolution of ontogenetic change in the lineage seems to be more influenced by size. Changes detected between juvenile and adult skulls enhanced predatory skills, coincident with the change from a diet of milk to a carnivorous diet. Change patterns suggest that the skull is not morphologically conservative in the lineage, in contrast with other carnivores such as canids and hyaenids. The enlargement of the rostrum observed in some canids and the reinforcement of the bite mechanism of hyaenids were not detected in this group. © 2013 The Linnean Society of London