Craniofacial sexual dimorphism patterns and allometry among extant hominids

Craniofacial sexual dimorphism in primates varies in both magnitude and pattern among species. In the past two decades, there has been an increasing emphasis in exploring the correlations of these patterns with taxonomy and the variation in patterns within and among the craniofacial regions.

Scrutinising these relationships for hominids, we decompose the craniofacial morphology in five taxa: Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. 3D coordinates of 35 traditional landmarks and 61 semilandmarks, covering five ridge curves, are measured for each of 268 adult and sub-adult specimens and analysed using geometric morphometric methods.

A multivariate analysis in size-shape space shows that ontogenetic scaling contributes to the development of sexual dimorphism in all five taxa, but to a varying extent. In absolute as well as in relative terms P. pygmaeus shows the greatest allometric component, followed by G. gorilla. Homo is intermediate, while in Pan the non-allometric constituent part contributes a large fraction to the actual sexual dimorphism, most markedly in the pygmy chimpanzee. An eigendecomposition of the five vectors of sexual dimorphism reveals two dimensions independent of allometry. One separates orang-utan sexual dimorphism from the African apes and Homo, and the other differentiates between the great apes and Homo with Pan mediating.

We discuss these patterns and speculate on their use as characters for taxonomic analysis in the fossil record.     

Breaking Symmetry: A Quantitative Analysis of Facial Skeleton Disharmony in Children Born with Bilateral Cleft Lip and Palate

Bilateral cleft lip and palate (BCLP) occurs when craniofacial precursors fail to form or fuse properly during development. The aim of this retrospective, cross-sectional investigation was to quantify directional asymmetry (DA) of the facial skeleton of children born with Veau Class IV nonsyndromic BCLP. To accomplish this goal, coordinate values of anatomical landmarks were acquired from three-dimensional cone beam computed tomographic images of the craniofacial skeleton of middle- to late-aged children born with BCLP and age- and sex-matched controls and used to compare patterns of asymmetry variation. Multivariate analyses revealed different patterns of DA variation across samples and identified approximately 30% of DA measures as significantly different. Magnitudes of statistically significant linear distances differ in the craniofacial region, with most smaller DA differences located near the orbits and frontal bone, while larger differences were localized mostly to the midface, alveolar ridge, and nasal borders. Generally, areas of the craniofacial skeleton derived from the maxillary and nasal prominences demonstrated the highest magnitudes of DA. The methods and results presented will be useful to biomedical researchers when identifying the extent to which patients with BCLP diverge from typical developmental expectations. Quantifying DA and assessing local differences across the craniofacial complex can aid medical practitioners when developing treatments to improve BCLP surgical algorithms and outcomes. Anat Rec, 302:1726–1732, 2019. © 2019 American Association for Anatomy     

Ontogenetic Patterns of Morphological Variation in the Ectocranial Human Vault

The skull is considered a modular structure in which different parts are influenced by different factors and, as a result, achieve adult shape at different ages. Previous studies have suggested that the basicranium presents a modular pattern that distinguishes sagittal and lateral parts, probably affected by the brain and masticatory structures, respectively. The vault of modern humans, in contrast, has been considered as a highly integrated system mainly influenced by brain growth. Here, we explored developmental shape variation in sagittal and lateral ectocranial vault in humans in order to assess if both regions are ontogenetically dissociated. We used a sample of 135 cranial computed tomography images from 0 to 31 ages. Landmarks and semilandmarks were collected on sagittal and lateral regions and geometric morphometric techniques were applied separately for each region. On the shape coordinates, we used Goodall's F‐test in order to assess the age when the adult configuration is attained. Principal component analysis enabled us to evaluate shape variation during ontogeny. Results indicated that both sagittal and lateral structures attain adult shape at early adolescence. Both regions express coordinated shape modifications probably due to shared developmental factors. It is concluded that masticatory muscles may not exert a strong enough influence to produce independent variation in the lateral traits. Thus, it is likely that the brain integrates sagittal and lateral parts of the vault across human ontogeny. Anat Rec, 296:1008–1015, 2013. © 2013 Wiley Periodicals, Inc.     

Spatially dense morphometrics of craniofacial sexual dimorphism in 1‐year‐olds

Recent advances in the field of geometric morphometrics allow for powerful statistical hypothesis testing for effects of biological and environmental variables on anatomical shape. This study used partial least‐squares regression (PLSR) and the recently developed bootstrapped response‐based imputation modelling (BRIM) algorithm to test for sexual dimorphism in the craniofacial shape of 1‐year‐old humans. We observed a recession of the forehead in boys relative to girls, and differences in the nose, consistent with adult dimorphism. Results also suggest that the degree to which individuals express dimorphic traits is continuous throughout the population. This is also seen in adult dimorphism but in 1‐year‐olds the amount of overlap between groups is much higher, indicating the strength of dimorphism between sexes is lower. Our results demonstrate early sexual dimorphism that is not attributable to the influx of sex hormones at puberty. This highlights the need to look at very early ontogeny for the origins of sexual dimorphism. We suggest that future work look at potential mediating effects of this early dimorphism on the later impact of puberty. The subtle shape differences we have detected, may also be applied to sexing fossilised crania. A common artefact in 3D images of faces of young children is that they often have their mouths open to varying degrees, introducing variability in the data unrelated to anatomy. We describe two PLSR‐based methods of correcting this. These methods may facilitate surgical planning and assessment of young children based on 3D images.     

The use of a sociobiological questionnaire (SQ) for the assessment of sexual dimorphism

A sociobiology questionnaire (SQ) (Thiessen and Kittrell, 1980) was administered to 527 undergraduate males and females. Twenty-seven predictions were tested. Sixteen of the predictions were statistically confirmed, and eight were in the expected direction. Overall, females appeared to be more interested in their mate's success than their own and were more selective in the choice of mates. Males gave more evidence of competitiveness and tended to mate polygamously. The results are compatible with theoretical expectations about mating strategies (Buss, 1987; Rushtonet al., 1984; Thiessen and Gregg, 1980). A number of problems with regard to the application of sociobiological and sociocultural theories to human behavior are discussed.Animal work leading to our interest in the sociobiological questionnaire was supported by NIMH grant MH 14076-20, awarded to the senior author.     

Radiological and Microsurgical Anatomy for Variation of the Mandible: Comparative Study of Human and Macaca fascicularis

Recent studies using cone‐beam computer tomography (CBCT) have added to our understanding of anatomical variation in the mandible of humans. However, the distribution of nerves cannot be revealed by CBCT. There have been investigations of the distribution of nerves relating to the mandible, but some proposed causes of these variations remain controversial. In this study, we observed a total of 10 sides from five mandibles of Macaca fascicularis of unknown age and sex using CBCT and dissection under stereomicroscopy. Nine of the 10 sides had two mental foramina in each side. Innervation by the mental nerves depended on the locations of those foramina. The long branch to the mandibular angle ran with a branch of the facial artery, which joined the mental artery in all 10 sides. Five specimens had a median perforating canal in the mandibular bone. In addition, a branch of the sublingual artery, which joined with the small branches of the submental artery, entered the mandibular bone from the median lingual foramen. This foramen was located in the lower part of the mandibular symphysis and passed via the median perforating canal to exit from the median labial foramen, also located in the lower part of the mandibular symphysis. We speculate that the median perforating canal of the mandible, rarely found in humans, is the remnant of the feeding artery of the fetal mandible, and in M. fascicularis is seen in all specimens because they have no mental protuberance. Anat Rec, 300:1464–1471, 2017. © 2017 Wiley Periodicals, Inc.     

基于非线性估计的CBCT几何标定算法

针对传统的几何标定算法由标定模体位姿误差导致的CBCT成像系统参数标定精度不高的问题,提出一种基于解析几何和非线性优化的CBCT几何标定算法。首先,设计一种插帧追踪的方法,提取特征点的坐标,使得标定模体与投影图像中的特征点实现一一对应。然后,利用投影图片与设计的标定模体之间的空间几何关系,计算相关参数。最后,对检测的特征点进行非线性估计,进一步提高几何参数的计算精度。仿真数据实验表明,本文算法能够较为精确地计算出CBCT成像系统的几何参数,并在标定模体出现位姿偏差时仍然保持较高的计算精度。通过非线性估计模型,本文所提出的算法突破了现有算法标定模体位于等中心点的限制,提高了CBCT成像系统中参数标定的精度。     

Sexual dimorphism in multiple aspects of 3D facial symmetry and asymmetry defined by spatially dense geometric morphometrics

Accurate measurement of facial sexual dimorphism is useful to understanding facial anatomy and specifically how faces influence, and have been influenced by, sexual selection. An important facial aspect is the display of bilateral symmetry, invoking the need to investigate aspects of symmetry and asymmetry separately when examining facial shape. Previous studies typically employed landmarks that provided only a sparse facial representation, where different landmark choices could lead to contrasting outcomes. Furthermore, sexual dimorphism is only tested as a difference of sample means, which is statistically the same as a difference in population location only. Within the framework of geometric morphometrics, we partition facial shape, represented in a spatially dense way, into patterns of symmetry and asymmetry, following a two-factor anova design. Subsequently, we investigate sexual dimorphism in symmetry and asymmetry patterns separately, and on multiple aspects, by examining (i) population location differences as well as differences in population variance-covariance; (ii) scale; and (iii) orientation. One important challenge in this approach is the proportionally high number of variables to observations necessitating the implementation of permutational and computationally feasible statistics. In a sample of gender-matched young adults (18-25 years) with self-reported European ancestry, we found greater variation in male faces than in women for all measurements. Statistically significant sexual dimorphism was found for the aspect of location in both symmetry and asymmetry (directional asymmetry), for the aspect of scale only in asymmetry (magnitude of fluctuating asymmetry) and, in contrast, for the aspect of orientation only in symmetry. Interesting interplays with hypotheses in evolutionary and developmental biology were observed, such as the selective nature of the force underpinning sexual dimorphism and the genetic independence of the structural patterns of fluctuating asymmetry. Additionally, insights into growth patterns of the soft tissue envelope of the face and underlying skull structure can also be obtained from the results.     

Cervical vertebral body growth and emergence of sexual dimorphism: a developmental study using computed tomography

The size and shape of human cervical vertebral bodies serve as a reference for measurement or treatment planning in multiple disciplines. It is therefore necessary to understand thoroughly the developmental changes in the cervical vertebrae in relation to the changing biomechanical demands on the neck during the first two decades of life. To delineate sex‐specific changes in human cervical vertebral bodies, 23 landmarks were placed in the midsagittal plane to define the boundaries of C2 to C7 in 123 (73 M; 50 F) computed tomography scans from individuals, ages 6 months to 19 years. Size was calculated as the geometric area, from which sex‐specific growth trend, rate, and type for each vertebral body were determined, as well as length measures of local deformation‐based morphometry vectors from the centroid to each landmark. Additionally, for each of the four pubertal‐staged age cohorts, sex‐specific vertebral body wireframes were superimposed using generalized Procrustes analysis to determine sex‐specific changes in form (size and shape) and shape alone. Our findings reveal that C2 was unique in achieving more of its adult size by 5 years, particularly in females. In contrast, C3–C7 had a second period of accelerated growth during puberty. The vertebrae of males and females were significantly different in size, particularly after puberty, when males had larger cervical vertebral bodies. Male growth outpaced female growth around age 10 years and persisted until around age 19–20 years, whereas females completed growth earlier, around age 17–18 years. The greatest shape differences between males and females occurred during puberty. Both sexes had similar growth in the superoinferior height, but males also displayed more growth in anteroposterior depth. Such prominent sex differences in size, shape, and form are likely the result of differences in growth rate and growth duration. Female vertebrae are thus not simply smaller versions of the male vertebrae. Additional research is needed to further quantify growth and help improve age‐ and sex‐specific guidance in clinical practice.     

A Novel Method for Observation of the Mandibular Foramen: Application to a Better Understanding of Dental Anatomy

Cone‐beam computed tomography gives us much useful morphological information about the mandibular bone. Many studies of the mandible include findings from this technique. However, there have been no endoscopic studies of the mandible. Sixteen sides of eight dry mandibles resected from cadavers (age range 38–83 years) were examined by endoscopy. The head of the endoscope was 2.0 mm in diameter. We examined the mandibular foramen, lingula, mylohyoid groove, and mandibular canal. The mylohyoid grooves showed variations such as double grooves and canals. The mandibular lingula was located superior or medial to the the mandibular foramen. In a single case, the medial wall inside the mandibular canal showed a porous surface. The retromolar canal was observed in three sides. None of the images in the present study have been seen in other studies. Observation of the retromolar canal from the mandibular canal in particular can help dental students as well as oral and maxillofacial surgeons to understand its morphology. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 300:1875–1880, 2017. © 2017 Wiley Periodicals, Inc.     

Role of sexual dimorphism in the pharmacologic effect of ethimizole

Laboratory of Experimental Therapy, Odessa Research Institute of Balneology, Ministry of Health of the Ukrainian SSR. (Presented by Academician of the Academy of Medical Sciences of the USSR, A. V. Val'dman.) Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 108, No. 7, pp. 91–93, July, 1989.     

Morphology of the tympanic-basicranial region in Mirounga leonina (Phocidae,Carnivora), postnatal ontogeny and sexual dimorphism

The auditory region of pinnipeds has seldom been described. Here we describe and analyze the ontogenetic trajectory of the tympanic bulla of the southern elephant seal, Mirounga leonina (Phocidae, Mammalia). This species is extremely sexually dimorphic and highly polygynous (organized in harems). We examined 118 specimens, arranged in three age classes (CI, CII, and CIII), ranging from newborn to adults (males and females). To analyze the overall size and shape of the tympanic bulla we performed a geometric morphometric analysis including 87 skulls. Females reach definitive shape and size of the bulla at earlier ontogenetic stages than males, in agreement with their earlier involvement in reproductive activities. The internal anatomy of the tympanic region (e.g. form and extension of the paries) does not show remarkable differences between sexes or age classes. The greatest differences between age classes are related to bone thickness, resulting from the apposition of new annual layers. An examination of possible sex-related external differences among age classes shows significant shape differences between males and females in CIII. The morphology observed in neonates is conserved across all individuals from CI, which included specimens up to 1 year old. Clear morphological differences were observed between CI individuals, on one hand, and CII individuals plus CIII females on the other. During cranial development of both male and females, the glenoid cavity expands and compresses the bulla; this condition reaches its maximum expression in CIII males. CIII males showed the greatest morphological differences, with respect to both CI and CII individuals, and CIII females.     

Pararenal angiosarcoma as a manifestation of sexual dimorphism in carcinogenesis

Pararenal angiosarcomas appeared in 42% of male CBA mice receiving 1,2-dimethylhydrazine (DMH) subcutaneously in a dose of 8 mg/kg for 30 weeks. These tumors did not appear in any of the 176 female mice of the same line receiving DMH by the same scheme. Histologically the tumors were variants of angiosarcomas with marked invaive growth into kidney tissue.Laboratory of Carcinogens, Department of Carcinogenic Agents, Oncologic Scientific Center, Academy of Medical Sciences of the USSR, Moscow. (Presented by Academician of the Academy of Medical Sciences of the USSR L. M. Shabad.) Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 88, No. 7, pp. 74–75, July, 1979.     

A morphometric analysis of developmental instability in children born with unilateral cleft lip and palate

Unilateral cleft lip and palate (UCLP) is a congenital deformity that occurs due to inadequate merging of the nasal and maxillary prominences during fetal development. Randomly distributed bilateral asymmetries known as fluctuating asymmetry (FA) occur in normally symmetric organisms when evolved mechanisms of developmental stability or equilibrium are disturbed by genetic, environmental, or unknown factors. Here, we hypothesize that facial skeleton FA will be increased in a sample of individuals born with UCLP (n = 24) relative to sex‐ and age‐matched controls (n = 24). To test this hypothesis, 23 anatomical landmarks were measured on individual anonymized cone‐beam computerized tomography (CBCT) images in children and adolescents (7–17 years). For each individual, 81 pairs of linear distances were used to estimate FAs across the face. To explore sample variation and statistical differences, a principal components analysis and Euclidean Distance Matrix Analysis multivariate bootstrap approach were carried out. Samples show some separation in multivariate space with 44.44% of FA differences being significantly different. The magnitude of FA was larger in the UCLP sample for every significant measurement. The magnitude of significant FA is highest near regions derived from the maxillary and nasal prominences, such as the nasal aperture. These results are useful for medical and dental practitioners when developing treatment options for children and adolescents with UCLP. Clin. Anat. 32:206–211, 2019. © 2018 Wiley Periodicals, Inc.     

Growth pattern of the maxillary sinus in the Japanese macaque (Macaca fuscata): reflections on the structural role of the paranasal sinuses

To investigate the claim that the primate paranasal sinuses possess not a functional but a structural role associated with the skull architecture (Blaney, 1990), the relationship between the maxillary sinus and the skull architecture was studied ontogenetically in 30 skulls of male and female Japanese macaques ( Macaca fuscata ). Coronal CT scan series and computerised 3-dimensional images served to evaluate the maxillary sinus. The definitive hemispherical shape of the sinus was already achieved after the completion of the primary dentition. Sinus volume increased with a trend indicating positive allometry. When compared with an ontogenetic data set of orang-utan (Koppe et al. 1995), however, the growth rate of the maxillary sinus of M. fuscata was significantly less. The maxillary sinus both of male and female macaques enlarged according to a common growth pattern. However, no sexual dimorphism could be established for the maxillary sinus size. Although the volume of the right maxillary sinus was normally bigger than that of the left side, the results suggested that asymmetry in maxillary sinus volume is related neither to skull size nor sex. Whereas a correlation analysis showed close relationships between the maxillary sinus volume and external cranial dimensions, the partial correlation coefficients revealed that these relationships were highly influenced by skull size. Although it cannot be ruled out that the paranasal sinuses are to some extent linked to the skull architecture, this study does not support a solely structural role for these air cavities.     

Morphology and Biomechanics of the Pinniped Jaw: Mandibular Evolution Without Mastication

Pinnipeds (seals, sea lions, and walruses) underwent a shift in jaw function away from typical carnivoran mastication to more novel marine behaviors during the terrestrial‐aquatic transition. Here we test the effect of aquatic prey capture and male‐male combat on the morphological evolution of a mammal jaw that does not masticate. Nine three‐dimensional landmarks were taken along the mandible for 25 species (N = 83), and corpus and symphysis external and cortical breadths for a subset of five species (N = 33). Principal components analysis was performed on size‐corrected landmark data to assess variation in overall jaw morphology across pinnipeds. Corpus breadths were input to a beam model to calculate strength properties and estimated bite force of specific species with contrasting behaviors (filter feeding, suction feeding, grip‐and‐tear feeding, and male‐male combat). Results indicate that, although phylogenetic signal in jaw shape is strong, function is also important in determining morphology. Filter feeders display an elongate symphysis and a long toothrow that may play a role in filtering krill. Grip‐and‐tear feeders have a long jaw and large estimated bite force relative to non‐biting species. However, the largest estimated bite forces were observed in males of male‐male combative species, likely due to the high selection pressure associated with male success in highly polygynous species. The suction feeding jaw is weak in biting but has a different morphology in the two suction feeding taxa. In conclusion, familial patterns of pinniped jaw shape due to phylogenetic relatedness have been modified by adaptations to specialized behavior of individual taxa. Anat Rec, 296:1049–1063, 2013. © 2013 Wiley Periodicals, Inc.     

Statistical Shape Analysis of Differences in the Shape of the Corpus Callosum Between Genders

Sexual dimorphic characteristics, which play an important role in human evolution studies and biological research, can be studied morphologically and metrically. Geometric morphometrics allows a better assessment of morphological characteristics. Statistical shape analysis has a long history in neuroanatomical and other research. The aim of this study was to identify shape differences of the corpus callosum between genders. Landmark coordinate data were collected from two‐dimensional magnetic resonance imaging scans of 93 homogeneously aged patients, 45 men and 48 women. These data were analyzed using Euclidean distance matrix analysis and thin plate spline analysis. The general shape variability of the corpus callosum of men was greater than that of women (men, 0.134; women, 0.097). We found no significant difference between sexes in the general shape of the corpus callosum, but we did find significant differences in the distances between some landmarks. Deformation of the corpus callosum between men to women was mainly detected in the posterior of the corpus callosum. These results serve as a reference for future studies on shape alterations of the corpus callosum associated with certain conditions. Anat Rec, 2007. © 2007 Wiley‐Liss, Inc.     

Evaluating sexual dimorphism in the human mastoid process: A viewpoint on the methodology

The mastoid process is one of the most sexually dimorphic features in the human skull, and is therefore often used to identify the sex of skeletons. Numerous techniques for assessing variation in the size and shape of the mastoid process have been proposed and implemented in osteological research, but its complex form still presents difficulties for consistent and effective analysis. In this article, we compare the different techniques and variables that have been used to define, measure, and visually score sexual dimorphism in the mastoid process. We argue that the current protocols fail to capture the full morphological range of this bony projection, and suggest ways of improving and standardizing them, regarding both traditional and 3D‐based approaches. Clin. Anat. 28:593–601, 2015. © 2015 Wiley Periodicals, Inc.