Three-dimensional geometric morphometric analysis of cranio-facial sexual dimorphism in a Central European sample of known sex

This article presents an approach for estimating the sexual dimorphism of adult crania using three-dimensional geometric morphometric methods. The study sample consisted of 139 crania of known sex (73 males and 66 females) belonging to persons who lived during the first half of the 20th century in Bohemia. The three-dimensional co-ordinates of 82 ecto-cranial landmarks and 39 semi-landmarks covering the midsagittal curve of the cranial vault were digitised using a MicroScribe G2X contact digitiser. The purposes of the investigation were to define the regions of the cranium where sexual dimorphism is most pronounced and to investigate the effectiveness of this method for determining sex from the shape of the cranium. The results demonstrate that it is better to analyse apportionable parts of the cranium rather than the cranium as a whole. Significant sexual differences (significance was determined using multivariate analysis of variance) were noted in the shape of the midsagittal curve of the vault, upper face, the region of the nose, orbits, and palate. No differences were recorded either in the shape of the cranium as a whole or in the regions of the base and the neurocranium. The greatest accuracy in determining sex was found in the region of the upper face (100% of study subjects correctly classified) and the midsagittal curve of the vault (99% of study subjects correctly classified).     

Sexual dimorphism in Southeast Asian crania: A geometric morphometric approach

Despite a number of studies stating that sexual dimorphism is population specific, sexual differences in Southeast Asian populations have received little attention. Previous studies in this region have focused on samples from Thailand or East Asian populations from China and Japan, examining sexual dimorphism predominantly of the postcranial bones, teeth and mandible with comparatively few cranial studies. These earlier studies have used traditional methods to metrically assess differences between the sexes. The aim of this study is to use geometric morphometric methods for the first time to quantify sexual dimorphism of Southeast Asian crania and extend knowledge of cranial sexual dimorphism beyond China, Japan and Thailand. A total of 35 unilateral and midline landmark coordinates were collected from 144 mainland and island Southeast Asian crania (89 male, 55 female). Using the shape analysis software Morphologika, principal components analysis and thin plate splines allowed for the statistical and visual exploration of shape differences. Differences included relative facial breadth, particularly across the zygomatic and postorbital regions and cranial vault breadth. Significant size dimorphism was also apparent. Overall expected accuracies were highest in the discriminant analysis using both shape and centroid size (86.8%).     

Exploring sexual dimorphism of human occipital and temporal bones through geometric morphometrics in an identified Western-European sample

Sex estimation is a paramount step of bioprofiling in both forensic anthropology and osteoarchaeology. When the pelvis is not optimally preserved, anthropologists commonly rely on the cranium to accurately estimate sex. Over the last decades, the geometric morphometric (GM) approach has been used to determine sexual dimorphism of the crania, in size and shape, overcoming some difficulties of traditional visual and metric methods. This article aims to investigate sexual dimorphism of the occipital and temporal region through GM analysis in a metapopulation of 50 Western-European identified individuals. Statistical analyses were performed to compare centroid size and shape data between sexes through the examination of distinct functional modules. Regression and Procrustes ANOVA were used to examine allometric and asymmetrical implications. Discriminant functions, combining size and shape data, were established. Significant dimorphism in size was found, with males having larger crania, confirming the major influence size has on cranial morphology. Allometric relationships were found to be statistically significant in both right and left temporal bones while shape differences between sexes were only significant on the right temporal bone. The visualization of the mean consensus demonstrated that males displayed a larger mastoid process associated with a reduced mastoid triangle and less projected occipital condyles. This exploratory study confirms that GM analysis represents an effective way to quantitatively capture shape of dimorphic structures, even on complex rounded ones such as the mastoid region. Further examination in a larger sample would be valuable to design objective visualization tools that can improve morphoscopic sex estimation methods.     

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.     

Sexual differences in European Neanderthal crania with special reference to the Krapina remains

Problems relating to the identification of sex in Neanderthal specimens are discussed. Three morphological features—morphology of the mastoid process and surrounding area, form of the supraorbital torus at glabella and the superciliary region, and the rugosity of the nuchal plane—were selected as most indicative of sex in Neanderthal crania based on observations from the Krapina collection and on those European specimens with pelvicly determined sex. Thirteen Neanderthal crania (eight males, five females) are sexed on the basis of these criteria, and the pattern and degree of sexual dimorphism determined for this sample is compared to those exhibited by other samples of more recent European hominids. It is concluded that the degree of sexual dimorphism in Neanderthal crania, as defined by this study, is consistent with that observed in the other fossil samples and that Neanderthals exhibit slightly more cranial sexual dimorphism than more recent Europeans. Models for explaining this are discussed as is the difference in pattern of change and degree of sexual dimorphism between the cranium and postcranium during later prehistoric hominid evolution in Europe.     

Geometric morphometrics of the skull of Tinamidae (Aves, Palaeognathae)

The Tinamidae comprise exclusively Neotropical palaegnathous birds, with homogeneous body morphology and no sexual dimorphism. The goal of this work was to explore the variation in skull morphology between taxa and its possible correspondence with features such as diet or gender using geometric morphometric tools. Eleven landmarks were analyzed in 53 skulls of 4 genera that inhabit grasslands: Nothoprocta, Eudromia, Nothura and Rhynchotus. Intrageneric and intergeneric variability was analyzed. The genera studied here can be distinguished based on the geometric shape of their skull, with prenarial region length and neurocranium shape as the most outstanding features. In the genus Eudromia, males and females could be differentiated, while in the genus Nothoprocta, the species differentiated according to their trophic habits. This study allows establishing that genera and, in some cases, the gender of the Tinamidae can be differentiated based on cranial shape.     

Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae,Caimaninae)

Melanosuchus niger is a caimanine alligatorid widely distributed in the northern region of South America. This species has been the focus of several ecological, genetic and morphological studies. However, morphological studies have generally been limited to examination of interspecific variation among extant species of South American crocodylians. Here, we present the first study of intraspecific variation in the skull of M. niger using a two‐dimensional geometric morphometric approach. The crania of 52 sexed individuals varying in size were analysed to quantify shape variation and to assign observed shape changes to different types of intraspecific variation, that is, ontogenetic variation and sexual dimorphism. Most of the variation in this species is ontogenetic variation in snout length, skull depth, orbit size and the width of the postorbital region. These changes are correlated with bite force performance and probably dietary changes. However, a comparison with previous functional studies reveals that functional adaptations during ontogeny seem to be primarily restricted to the postrostral region, whereas rostral shape changes are more related to dietary shifts. Furthermore, the skulls of M. niger exhibit a sexual dimorphism, which is primarily size‐related. The presence of non‐size‐related sexual dimorphism has to be tested in future examinations.     

Variation in cranial morphology of bottlenose dolphins (genus Tursiops) off South Africa

Taxonomy plays an important role in conservation biology. Despite the variety of methods used to differentiate units, some groups, such as Delphinidae within the Cetacea have proven difficult to untangle. This study aimed to shed light on morphological variation of the genus Tursiops in South African waters using geometric morphometrics and to distinguish morphological groups and variation in these groups. A total of 241 crania of Tursiops spp. were analyzed using a suite of 2‐dimensional landmarks defined on photographs of the specimens. Results revealed two distinct morphological groups, with the smaller cluster comprised mainly of specimens from the cold temperate region off the west coast and the larger cluster comprised of specimens mainly from the warm temperate and subtropical regions off the south and east coast, respectively. We suggest that these groups correspond to different species of Tursiops, but this result requires further support. These groups were treated as separate entities and sexual dimorphism and geographic variation were assessed within each group. While sexual dimorphism and geographic variation were not significant within Cluster D1 and V1, they were significant within Clusters D2 and V2. The few Cluster 1 specimens found in the warm temperate and subtropical regions, relative to the number of Cluster 2 specimens, could be an indication of an offshore distribution for this group in these regions. Alternatively, the smaller cluster may also be indicative of a potentially small population size.     

Technical note: A new method for measuring long bone curvature using 3D landmarks and semi‐landmarks

Here we describe and evaluate a new method for quantifying long bone curvature using geometric morphometric and semi‐landmark analysis of the human femur. The technique is compared with traditional ways of measuring subtense and point of maximum curvature using either coordinate calipers or projection onto graph paper. Of the traditional methods the graph paper method is more reliable than using coordinate calipers. Measurement error is consistently lower for measuring point of maximum curvature than for measuring subtense. The results warrant caution when comparing data collected by the different traditional methods. Landmark data collection proves reliable and has a low measurement error. However, measurement error increases with the number of semi‐landmarks included in the analysis of curvature. Measurements of subtense can be estimated more reliably using 3D landmarks along the curve than using traditional techniques. We use equidistant semi‐landmarks to quantify the curve because sliding the semi‐landmarks masks the curvature signal. Principal components analysis of these equidistant semi‐landmarks provides the added benefit of describing the shape of the curve. These results are promising for functional and forensic analysis of long bone curvature in modern human populations and in the fossil record. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Changes in the sexual dimorphism of the human mandible during the last 1200 years in Central Europe

According to many investigations, changes in mandibular morphology can occur synchronously with changes in the environment, and sexual dimorphism of the mandible can be influenced by the environment. Sexual dimorphism during the last 1200 years was evaluated using geometric morphometric analysis of virtual cranial models. The method of geometric morphometrics allows differences in size and shape to be assessed separately. We analyzed groups of adult individuals dating to Early Middle Ages, High Middle Ages, Early Modern Ages and from a modern Czech population (21st century). Significant sexual dimorphism in mandibular size was found in all populations. A trend in the sexual dimorphism of size was seen, with differences between the sexes increasing gradually over time. Size changes in female mandibles were a better reflection of environmental conditions and climate than size changes in male mandibles. Regarding changes in the sexual dimorphism of shape, significant dimorphism was found in all four samples. However, the pattern of mandibular shape dimorphism was different and varied considerably between samples. There was only one stable shape trait showing sexual dimorphism across all four samples in our study: the gonion lies more laterally in male than in female mandibles and male mandibles are relatively wider than female mandibles. Sexual dimorphism of shape is not influenced by the climate; instead sexual selection might play a role. This research supports earlier studies that have found that the degree and pattern of sexual dimorphism is population-specific and the factors regulating sexual dimorphism today may not be the same as those in the past.     

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.     

Sexual dimorphism and discriminant function sexing in indigenous South African crania

This study aimed to examine sexual dimorphism in, and to produce a practical discriminant function for determining the sex of indigenous, Bantu-speaking, South African crania. The types of data to be used were a small number of traditional, or mathematically transformed three-dimensional, linear measurements, comparable to those in use by most physical and forensic anthropologists. The samples to be examined, separately and pooled, were of the Cape Nguni, Natal Nguni and Sotho subgroups. In addition, three local populations (‘tribes’—Zulu, Xhosa and Southern Sotho) within these subgroups were also studied.

Univariate male/female ratios indicate significant sexual dimorphism in the pooled South African crania. Canonical variates analysis of the pooled sample showed that facial width is the strongest discriminating morphometric variable; cranial length and basi-bregmatic height are the next most significant features. Eight measurements derived from the three-dimensional data were used to produce a series of discriminant functions for sex determination in the pooled sample, for which an accuracy of 77–80% was attained. Analysis of the calvaria and face, separately, has shown that the sex of damaged material can be diagnosed with a reasonable degree of accuracy (75–76%).

The new functions for the pooled indigenous South African sample provide improved sex discrimination accuracy compared to those obtained by employing the commonly utilised statistics of Giles & Elliot (1963), even when a modified sectioning point is used. Functions calculated for the separate local populations gave variable and fairly low improvements in sexing accuracy. As the subdivisions at all levels are at present quite rapidly disappearing in South Africa, for most purposes it is now best to simply apply the pooled data functions for sexing crania.     

A complete survey of normal pores on a smooth shell ostracod (Crustacea): Landmark‐based versus outline geometric morphometrics

Pores and sensilla on ostracod shell have often been used in studies of ontogeny, taxonomy, and phylogeny of the group. However, an analysis of sexual dimorphism and variation between valves in the number and distribution of pores is lacking. Also, such studies have never been done on a widely distributed, morphologically variable, and weakly ornamented freshwater ostracod. Here, we survey pores in one such species, Physocypria kraepelini . We choose 27 homologous pores as landmarks for 2D‐geometric morphometric analysis, with the aim to assess intersexual and between valves variation in size and shape relative to the Fourier outline analysis. This species has only simple (Type A) pores with and without a lip, and each pore carries an undivided sensory seta. Our results show that the total number of pores varies (from 270 to 296), but this is not associated with a specific valve. Males carry fewer pores than females, however no sex specific pores are found. Small intrapopulation divergence of the Cyt b molecular marker (1%) indicates that morphological variability is not species related. We found that P. kraepelini exhibits directional asymmetry of size and shape, sexual size dimorphism (SSD) but lacks sexual shape dimorphism (SShD). Two geometric morphometrics methods were congruent in the estimation of SSD, SShD, and directional asymmetry of shape but differ in the statistical evaluation of directional asymmetry of size. Contrary to other animal groups, our study suggests that ostracods have more pronounced directional asymmetry of shape compared to directional asymmetry of size.     

Ontogeny of facial dimorphism and patterns of individual development within one human population

Based on a longitudinal study of radiographs of the Denver Growth Study, we investigated the morphological development of individual and gender differences in the anterior neurocranium, face, and basicranium. In total, 500 X-rays of 14 males and 14 females, each with 18 landmarks and semilandmarks, were digitized and analyzed using geometric morphometric methods. Sexual dimorphism in shape and form is already present at the earliest age stage included in the analysis. However, the nature of dimorphism changes with age. Four factors apper to contribute to cranial sexual dimorphism in human postnatal development: 1) initial, possibly prenatal, differences in shape; 2) differences in the association of size and shape; 3) male hypermorphosis; and 4) some degree of difference in the direction of male and female growth trajectories. Studying changes in individuals, we find a low correlation between newborn and adult morphology, while 3-year-olds already show a high correlation with their adult form. We conclude that the adult pattern of interindividual difference in facial form in a single human population is established within the first few years of life.     

Sexual dimorphism in the baboon facial skeleton

Baboons exhibit marked sexual dimorphism in many aspects of their morphology. Dimorphism is especially pronounced in the face. We use finite-element analysis to investigate the ontogeny of sexual dimorphism in a cross-sectional sample of baboon (Papio sp.) faces. This method provides detailed quantitative information about size and shape changes at anatomical landmarks in the face during growth. Allometric results suggest that sexual dimorphism in facial size and shape is produced by ontogenetic scaling: males and females share a common ontogenetic trajectory. Analyses of growth in time, which complement allometric analyses, show that female growth slows much earlier than male growth, accounting for the differences between sexes. Local size and local shape follow similar patterns of growth, but changes in these variables are slower in females. Local and global facial size are much more dimorphic than local and global facial shape.     

Differential sexual dimorphism: size and shape in the cranium and pelvis of grey foxes (Urocyon)

Patterns of sexual size dimorphism (SSD) and cranial dimorphism are well documented. However, limited examinations exist of the contrasts in the patterns and nature of dimorphism across body regions (e.g. cranium, pelvis), particularly when these regions have different sex-specific functions (e.g. display in mating, locomotion, and reproduction). Using landmark-based morphometric techniques, we investigated size and shape dimorphism variation in the crania and pelves of two closely-related fox species within the genus Urocyon . Although we found no significant size and shape dimorphism in the crania of either species, we did find significant dimorphism in the pelvis: its size was dimorphic in Urocyon littoralis (but not in Urocyon cinereoargenteus ) and its shape was dimorphic in both species (though more pronounced in U. littoralis ). The observation of greater dimorphism in the pelvis than in the cranium suggests that factors such as offspring size and locomotor mode play a greater role in sexual dimorphism than simple 'whole body' allometric affects associated with dimorphism in body size.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 339–353.     

Geometric morphometric analysis reveals that the shells of male and female siphon whelks Penion chathamensis are the same size and shape

Secondary sexual dimorphism can make the discrimination of intra and interspecific variation difficult, causing the identification of evolutionary lineages and classification of species to be challenging, particularly in palaeontology. Yet sexual dimorphism is an understudied research topic in dioecious marine snails. We use landmark-based geometric morphometric analysis to investigate whether there is sexual dimorphism in the shell morphology of the siphon whelk Penion chathamensis. In contrast to studies of other snails, results strongly indicate that there is no difference in the shape or size of shells between the sexes. A comparison of P. chathamensis and a related species demonstrates that this result is unlikely to reflect a limitation of the method. The possibility that sexual dimorphism is not exhibited by at least some species of Penion is advantageous from a palaeontological perspective as there is a rich fossil record for the genus across the Southern Hemisphere.     

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.     

Sexual Dimorphism in Sturnira lilium (Chiroptera,Phyllostomidae): Can Pregnancy and Pup Carrying Be Responsible for Differences in Wing Shape?

Competition is one of the most cited mechanisms to explain secondary sexual dimorphism in animals. Nonetheless, it has been proposed that sexual dimorphism in bat wings is also a result of adaptive pressures to compensate additional weight caused by fetus or pup carrying during the reproductive period of females. The main objective of this study is to verify the existence of sexual dimorphism in Sturnira lilium wings. We employed geometric morphometrics techniques using anatomical landmarks superimposition to obtain size (Centroid Size) and shape variables of wings, which were reduced by Linear Discriminant Analysis (LDA). We also employed classical morphometrics using wing length measurements to compare efficiency between these two morphometric approaches and make comparisons using wing area measurements. LDA indicated significant differences between wing shapes of males and females, with 91% (stepwise classification) and 80% (leave-one-out cross validation) of correct classification. However, the size variable obtained did not contribute to such classifications. We have observed larger areas in female wings, but we found no differences in wing length measurements and no allometric effects in wing length, shape and area measurements. Interestingly, our study has provided evidences of morphological differences where classical morphometrics have failed. LDA and area measurements analyses revealed that females have a different area distribution in distinct portions of the wing, with wider dactylopatagia and plagiopatagia, and wingtips more triangular than males. No differences in body length or relative wing length were observed between the sexes, but pregnant females have more body weight than non-pregnant females and males. Our findings suggest that sexual dimorphism in the wing shape of S. lilium is probably related to the increase in flight efficiency of females during reproductive period. It decreases wing loading in specific portions of the wing and reduces energy cost to maintain a faster and maneuverable flight.     

Principles for the virtual reconstruction of hominin crania

Fossils are usually discovered broken or distorted, therefore reconstruction is inevitably the first step towards any comparative analysis. We outline a general methodological framework by which missing information about biological specimens can be estimated using geometric morphometric methods and discuss how this relates to effective paleoanthropological use of incomplete and distorted crania.Combining digital data resources with geometric morphometrics, we go beyond the assembly of fragments on the computer. As in a three-dimensional jigsaw puzzle, we first assemble the virtual pieces manually. Then we use landmarks, several hundred semilandmarks, and information from complete specimens to estimate missing coordinates and correct for distortion simultaneously. One can thus incorporate information from incomplete specimens in a comparative morphometric analysis while keeping track of the uncertainties that result from partial preservation or deformation. We exemplify our approach by reconstructing the fossil crania Arago XXI, Taung, and KNM-WT 15000. As different assumptions and algorithms lead to different estimations, there exists no “all-purpose” reconstruction. Instead one creates multiple reconstructions—a posterior distribution in a Bayesian sense. This distribution reflects uncertainty due to missing data values and sensitivity to prior assumptions. While there will typically be shape differences among equally plausible reconstructions, these different estimates might still support a single conclusion.