Relationship of cranial robusticity to cranial form,geography and climate in Homo sapiens

Variation in cranial robusticity among modern human populations is widely acknowledged but not well‐understood. While the use of “robust” cranial traits in hominin systematics and phylogeny suggests that these characters are strongly heritable, this hypothesis has not been tested. Alternatively, cranial robusticity may be a response to differences in diet/mastication or it may be an adaptation to cold, harsh environments. This study quantifies the distribution of cranial robusticity in 14 geographically widespread human populations, and correlates this variation with climatic variables, neutral genetic distances, cranial size, and cranial shape. With the exception of the occipital torus region, all traits were positively correlated with each other, suggesting that they should not be treated as individual characters. While males are more robust than females within each of the populations, among the independent variables (cranial shape, size, climate, and neutral genetic distances), only shape is significantly correlated with inter‐population differences in robusticity. Two‐block partial least‐squares analysis was used to explore the relationship between cranial shape (captured by three‐dimensional landmark data) and robusticity across individuals. Weak support was found for the hypothesis that robusticity was related to mastication as the shape associated with greater robusticity was similar to that described for groups that ate harder‐to‐process diets. Specifically, crania with more prognathic faces, expanded glabellar and occipital regions, and (slightly) longer skulls were more robust than those with rounder vaults and more orthognathic faces. However, groups with more mechanically demanding diets (hunter‐gatherers) were not always more robust than groups practicing some form of agriculture. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans

Recent studies have demonstrated that the shape of the human temporal bone is particularly strongly correlated with neutral genetic expectation, when compared against other cranial regions, such as the vault, face, and basicranium. In turn, this has led to suggestions that the temporal bone is particularly reliable in analyses of primate phylogeny and human population history. While several reasons have been suggested to explain the temporal bone's strong fit with neutral expectation, the temporal bone has never systematically been compared against other individual cranial bones defined using the same biological criteria. Therefore, it is currently unknown whether the shapes of all cranial bones possess reliable information regarding neutral genetic evolution, or whether the temporal bone is unique in this respect. This study tests the hypothesis that the human temporal bone is more congruent with neutral expectation than six other individual cranial bones by correlating population affinity matrices generated using neutral genetic and 3D craniometric data. The results demonstrate that while the temporal bone shows the absolute strongest correlation with neutral genetic data compared with all other bones, it is not statistically differentiated from the sphenoid, frontal, and parietal bones in this regard. Potential reasons for the temporal bone's consistently strong fit with neutral expectation, such as its overall anatomical complexity and/or its contribution to the architecture of the basicranium, are examined. The results suggest that future phylogenetic and taxonomic studies would benefit from considering the shape of the entire cranium minus those regions that deviate most from neutrality. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Common features of sexual dimorphism in the cranial airways of different human populations

Sexual dimorphism in the human craniofacial system is an important feature of intraspecific variation in recent and fossil humans. Although several studies have reported different morphological patterns of sexual dimorphism in different populations, this study searches for common morphological aspects related to functional anatomy of the respiratory apparatus. 3D geometric morphometrics were used to test the hypothesis that due to higher daily energy expenditure and associated greater respiratory air consumption as well as differences in body composition, males should have absolutely and relatively greater air passages in the bony cranial airways than females. We measured 25 3D landmarks in five populations (N = 212) of adult humans from different geographic regions. Male average cranial airways were larger in centroid sizes than female ones. Males tended to show relatively taller piriform apertures and, more consistently, relatively taller internal nasal cavities and choanae than females. Multivariate regressions and residual analysis further indicated that after standardizing to the same size, males still show relatively larger airway passages than females. Because the dimensions of the choanae are limiting factors for air transmission towards the noncranial part of the respiratory system, the identified sex-specific differences in cranial airways, possibly shared among human populations, may be linked with sex-specific differences in body size, composition, and energetics. These findings may be important to understanding trends in hominin facial evolution.     

Constructing cranial ontogenetic trajectories: A comparison of growth,development, and chronological age proxies using a known‐age sample of Macaca mulatta

Recent morphometric research has generated opposing conclusions regarding the ontogenetic trajectories of catarrhine crania, possibly due to the ontogenetic proxies used to calculate them. Therefore, we used three surrogates: size, molar eruption, and chronological age to generate trajectories in a known‐age sample to produce ontogenetic trajectories and determine the similarities and differences between them. Forty‐three landmarks from an ontogenetic series of 160 Macaca mulatta crania, with associated ages at death, were used to produce ontogenetic trajectories of cranial shape change. These were computed by sex through multivariate regression of Procrustes aligned coordinates against three surrogates for ontogeny: natural log of centroid size (growth), molar eruption stage (development), and chronological age. These trajectories were compared by calculating the angles between them. Each trajectory was also used to produce simulated adults from juveniles, which were then compared with each other and actual adults. The different trajectories are nearly parallel as each of the surrogates track similar aspects of ontogenetic cranial shape change, but chronological age was the most divergent. Simulated adults produced using the developmental stage trajectories were most similar to actual adults. When simulated adults were produced from opposite sex trajectories, they resembled the sex from which the trajectory was produced, not the sex of the juvenile specimen. We discuss properties of the trajectories produced from each of the surrogates, the possible reasons for previously opposing conclusions, how these properties can inform future investigations, and how our investigation bears on analyses of heterochrony.     

Genetic, geographic, and environmental correlates of human temporal bone variation

Temporal bone shape has been shown to reflect molecular phylogenetic relationships among hominoids and offers significant morphological detail for distinguishing taxa. Although it is generally accepted that temporal bone shape, like other aspects of morphology, has an underlying genetic component, the relative influence of genetic and environmental factors is unclear. To determine the impact of genetic differentiation and environmental variation on temporal bone morphology, we used three-dimensional geometric morphometric techniques to evaluate temporal bone variation in 11 modern human populations. Population differences were investigated by discriminant function analysis, and the strength of the relationships between morphology, neutral molecular distance, geographic distribution, and environmental variables were assessed by matrix correlation comparisons. Significant differences were found in temporal bone shape among all populations, and classification rates using cross-validation were relatively high. Comparisons of morphological distances to molecular distances based on short tandem repeats (STRs) revealed a significant correlation between temporal bone shape and neutral molecular distance among Old World populations, but not when Native Americans were included. Further analyses suggested a similar pattern for morphological variation and geographic distribution. No significant correlations were found between temporal bone shape and environmental variables: temperature, annual rainfall, latitude, or altitude. Significant correlations were found between temporal bone size and both temperature and latitude, presumably reflecting Bergmann's rule. Thus, temporal bone morphology appears to partially follow an isolation by distance model of evolution among human populations, although levels of correlation show that a substantial component of variation is unexplained by factors considered here.     

Combining ecological niche modelling and morphology to assess the range‐wide population genetic structure of bobcats (Lynx rufus)

Despite a broad distribution, general habitat requirements, and a large dispersal potential, bobcats (Lynx rufus) exhibit a genetic division that longitudinally transects central North America. We investigated (1) whether the climate of the Last Glacial Maximum (LGM; 21 kya) isolated bobcats into refugia and also whether the current climate influences gene flow between the segregate populations and (2) whether the geographical patterns in cranial morphology reflect population identity. We created ecological niche models (ENMs) to evaluate climatic suitability and to estimate distributions of the disparate populations under both historical (LGM) and contemporary conditions. We used two‐dimensional geometric morphometric methods to evaluate variations in the cranium and mandible. These variations were then regressed across geographical variables to assess morphological differences throughout the range of the bobcat. ENMs projected onto LGM climate provided evidence of refugia during the LGM via increased suitability in the north‐west and south‐east portions of this species' range. Contemporarily, our models suggest that the Great Plains may be restricting bobcat migration and gene flow, effectively maintaining disparate populations. Morphological analyses identified a significant linear trend in shape variation across latitudinal and longitudinal gradients rather than distinct morphological divergence between lineages. Similar shape variations, however, did converge in approximate locations of assumed refugia. The findings of the present study provide a robust assessment of the biogeographical considerations for the population genetic structure of bobcats.     

Carnivory maintains cranial dimorphism between males and females: Evidence for niche divergence in extant Musteloidea

The evolution and maintenance of sexual dimorphism has long been attributed to sexual selection. Niche divergence, however, serves as an alternative but rarely tested selective pressure also hypothesized to drive phenotypic disparity between males and females. We reconstructed ancestral social systems and diet and used Ornstein–Uhlenbeck (OU) modeling approaches to test whether niche divergence is stronger than sexual selection in driving the evolution of sexual dimorphism in cranial size and bite force across extant Musteloidea. We found that multipeak OU models favored different dietary regimes over social behavior and that the greatest degree of cranial size and bite force dimorphism were found in terrestrial carnivores. Because competition for terrestrial vertebrate prey is greater than other dietary groups, increased cranial size and bite force dimorphism reduces dietary competition between the sexes. In contrast, neither dietary regime nor social system influenced the evolution of sexual dimorphism in cranial shape. Furthermore, we found that the evolution of sexual dimorphism in bite force is influenced by the evolution of sexual dimorphism in cranial size rather than cranial shape. Overall, our results highlight niche divergence as an important mechanism that maintains the evolution of sexual dimorphism in musteloids.     

The influence of artificial cranial vault deformation on the expression of cranial nonmetric traits: its importance in the study of evolutionary relationships

Nonmetric cranial traits have been commonly used in evolutionary relationship studies. They develop during the growth and development of an individual, and for this reason its expression presents different sources of genetic and nongenetic variation. However, the use of these features in evolutionary relationship studies carries the implicit assumption that much of the nonmetric trait variation is essentially genetic. Among the nonheritable factors, cranial vault deformation has been the most studied in human populations. Because of the widespread distribution and elevated rate of artificial cranial vault deformation found in America, and the importance of nonmetric traits in evolutionary relationship studies in this area, the objectives of this paper are as follows: (a) to study the influence of artificial cranial vault deformation on the presence of nonmetric traits within samples of human craniofacial remains; and (b) to establish artificial cranial vault deformation influence on evolutionary relationships between local populations on a regional scale. Our results indicate that artificial cranial vault deformations alter the variation and covariation of metric and nonmetric traits in some samples. Wormian bones, placed in cranial vault sutures, are the most influenced by this factor. However, our results suggest that when all nonmetric traits were used the artificial cranial vault deformation did not influence the basic pattern of variation among samples. The exclusion or inclusion of wormians bones in evolutionary relationships analysis did not modify the results, but using only wormians bones lead to inconsistent results indicating that these traits have little value on these kind of studies.     

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.     

The impact of digging on craniodental morphology and integration

The relationship between the form and function of the skull has been the subject of a great deal of research, much of which has concentrated on the impact of feeding on skull shape. However, there are a number of other behaviours that can influence craniodental morphology. Previous work has shown that subterranean rodents that use their incisors to dig (chisel‐tooth digging) have a constrained cranial shape, which is probably driven by a necessity to create high bite forces at wide gapes. Chisel‐tooth‐digging rodents also have an upper incisor root that is displaced further back into the cranium compared with other rodents. This study quantified cranial shape and upper incisors of a phylogenetically diverse sample of rodents to determine if chisel‐tooth‐digging rodents differ in craniodental morphology. The study showed that the crania of chisel‐tooth‐digging rodents shared a similar place in morphospace, but a strong phylogenetic signal within the sample meant that this grouping was nonsignificant. It was also found that the curvature of the upper incisor in chisel‐tooth diggers was significantly larger than in other rodents. Interestingly, most subterranean rodents in the sample (both chisel‐tooth and scratch diggers) had upper incisors that were better able to resist bending than those of terrestrial rodents, presumably due to their similar diets of tough plant materials. Finally, the incisor variables and cranial shape were not found to covary consistently in this sample, highlighting the complex relationship between a species’ evolutionary history and functional morphology.     

No relationship between canalization and developmental stability of the skull in a natural population of Mastomys natalensis (Rodentia: Muridae)

The aim of the present work was to investigate the relationship between canalization and developmental stability under varying environmental conditions. Three different cohorts of Mastomys natalensis (Rodentia, Muridae), displaying different growth trajectories, were analysed by means of geometric morphometrics. A set of 23 landmarks was digitalized on the dorsal skull of 292 specimens from Morogoro (Tanzania). Patterns of among‐ and within‐individual (measured as fluctuating asymmetry, FA) variation were assessed and compared among and within the three groups to test for the presence of a common mechanism between canalization and developmental stability. Results showed that there was no congruence between canalization and developmental stability: (1) levels of FA and among‐individual variation varied in a discordant fashion, (2) no correspondence between the variance–covariance matrix of among‐ and within individual variation was found, and (3) environmental effects were able to alter the covariance structure of among‐individual variation leaving patterns associated with fluctuating asymmetry unaffected. These findings support the view of multiple mechanisms underlying developmental buffering of shape variation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 207–216.     

Evolutionary persistence of phenotypic integration: influence of developmental and functional relationships on complex trait evolution

Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.