Are more diverse parts of the mammalian skull more?labile?

Morphological variation is unevenly distributed within the mammalian skull; some of its parts have diversified more than others. It is commonly thought that this pattern of variation is mainly the result of the structural organization of the skull, as defined by the pattern and magnitude of trait covariation. Patterns of trait covariation can facilitate morphological diversification if they are aligned in the direction of selection, or these patterns can constrain diversification if oriented in a different direction. Within this theoretical framework, it is thought that more variable parts possess patterns of trait covariation that made them more capable of evolutionary change, that is, are more labile. However, differences in the degree of morphological variation among skull traits could arise despite variation in trait lability if, for example, some traits have evolved at a different rate and/or undergone stabilizing selection. Here, we test these hypotheses in the mammalian skull using 2D geometric morphometrics to quantify skull shape and estimating constraint, rates of evolution, and lability. Contrary to the expectations, more variable parts of the skull across mammalian species are less capable of evolutionary change than are less variable skull parts. Our results suggest that patterns of morphological variation in the skull could result from differences in rate of evolution and stabilizing selection.     

Unilateral and bilateral expression of a quantitative trait: asymmetry and symmetry in coronal craniosynostosis

Bilateral symmetry in vertebrates is imperfect and mild asymmetries are found in normal growth and development. However, abnormal development is often characterized by strong asymmetries. Coronal craniosynostosis, defined here as consisting of premature suture closure and a characteristic skull shape, is a complex trait. The premature fusion of the coronal suture can occur unilaterally associated with skull asymmetry (anterior plagiocephaly) or bilaterally associated with a symmetric but brachycephalic skull. We investigated the relationship between coronal craniosynostosis and skull bilateral symmetry. Three-dimensional landmark coordinates were recorded on preoperative computed tomography images of children diagnosed with coronal nonsyndromic craniosynostosis (N = 40) and that of unaffected individuals (N = 20) and analyzed by geometric morphometrics. Our results showed that the fusion pattern of the coronal suture is similar across individuals and types of coronal craniosynostosis. Shape analysis showed that skulls of bilateral coronal craniosynostosis (BCS) and unaffected individuals display low degrees of asymmetry, whereas right and left unilateral coronal craniosynostosis (UCS) skulls are asymmetric and mirror images of one another. When premature fusion of the coronal suture (without taking into account cranial dysmorphology) is scored as a qualitative trait, the expected relationship between trait frequency and trait unilateral expression (i.e. negative correlation) is confirmed. Overall, we interpret our results as evidence that the same biological processes operate on the two sides in BCS skulls and on the affected side in UCS skulls, and that coronal craniosynostosis is a quantitative trait exhibiting a phenotypic continuum with BCS displaying more intense shape changes than UCS.     

Estimating the power of a proposed linkage study for a complex genetic trait.

Many genetic traits have complex modes of inheritance; they may exhibit incomplete or age-dependent penetrance or fail to show any clear Mendelian inheritance pattern. As primary linkage maps for the human genome near completion, it is becoming increasingly possible to map these traits. Prior to undertaking a linkage study, it is important to consider whether the pedigrees available for the proposed study are likely to provide sufficient information to demonstrate linkage, assuming a linked marker is tested. In the current paper, we describe a computer simulation method to estimate the power of a proposed study to detect linkage for a complex genetic trait, given a hypothesized genetic model for the trait. Our method simulates trait locus genotypes consistent with observed trait phenotypes, in such a way that the probability to detect linkage can be estimated by sample statistics of the maximum lod score distribution. The method uses terms available when calculating the likelihood of the trait phenotypes for the pedigree and is applicable to any trait determined by one or a few genetic loci; individual-specific environmental effects can also be dealt with. Our method provides an objective answer to the question, Will these pedigrees provide sufficient information to map this complex genetic trait?     

Heterochronia via procrustean superimposition: application to the skulls of Homonidae primates

The procrustes superimposition method is well adapted to heterochronic studies in the field of evolutionary biology. 1) The procrustes method gives a precise and mathematical definition of two of the three heterochronic variables: size and shape. 2) It allows us to describe complex anatomical structures and thus to analyse the whole structure and not just to proceed trait by trait. 3) The approach is statistical and the different hypotheses and results may be statistically tested. 4) When applied to heterochronies the method allows us to test if there is a common shape change related to allometry. In the present study of three species of Hominoid primates, the procrustes superimposition reveals that various heterochronic processes are simultaneously present. Size-age-shape dissociations between species, already present in the first ontogenetic stage, are amplified with growth until adult stage. As compared with that of the chimpanzee, the growth of the gorilla skull is accelerated in terms of size-shape covariation and size alone. The growth of the human skull is neotenic as compared with that of the apes.     

Epistatic pleiotropy and the genetic architecture of covariation within early and late-developing skull trait complexes in mice

The role of epistasis as a source of trait variation is well established, but its role as a source of covariation among traits (i.e., as a source of "epistatic pleiotropy") is rarely considered. In this study we examine the relative importance of epistatic pleiotropy in producing covariation within early and late-developing skull trait complexes in a population of mice derived from an intercross of the Large and Small inbred strains. Significant epistasis was found for several pairwise combinations of the 21 quantitative trait loci (QTL) affecting early developing traits and among the 20 QTL affecting late-developing traits. The majority of the epistatic effects were restricted to single traits but epistatic pleiotropy still contributed significantly to covariances. Because of their proportionally larger effects on variances than on covariances, epistatic effects tended to reduce within-group correlations of traits and reduce their overall degree of integration. The expected contributions of single-locus and two-locus epistatic pleiotropic QTL effects to the genetic covariance between traits were analyzed using a two-locus population genetic model. The model demonstrates that, for single-locus or epistatic pleiotropy to contribute to trait covariances in the study population, both traits must show the same pattern of single-locus or epistatic effects. As a result, a large number of the cases where loci show pleiotropic effects do not contribute to the covariance between traits in this population because the loci show a different pattern of effect on the different traits. In general, covariance patterns produced by single-locus and epistatic pleiotropy predicted by the model agreed well with actual values calculated from the QTL analysis. Nearly all single-locus and epistatic pleiotropic effects contributed positive components to covariances between traits, suggesting that genetic integration in the skull is achieved by a complex combination of pleiotropic effects.     

The craniomandibular mechanics of being human

Diminished bite force has been considered a defining feature of modern Homo sapiens, an interpretation inferred from the application of two-dimensional lever mechanics and the relative gracility of the human masticatory musculature and skull. This conclusion has various implications with regard to the evolution of human feeding behaviour. However, human dental anatomy suggests a capacity to withstand high loads and two-dimensional lever models greatly simplify muscle architecture, yielding less accurate results than three-dimensional modelling using multiple lines of action. Here, to our knowledge, in the most comprehensive three-dimensional finite element analysis performed to date for any taxon, we ask whether the traditional view that the bite of H. sapiens is weak and the skull too gracile to sustain high bite forces is supported. We further introduce a new method for reconstructing incomplete fossil material. Our findings show that the human masticatory apparatus is highly efficient, capable of producing a relatively powerful bite using low muscle forces. Thus, relative to other members of the superfamily Hominoidea, humans can achieve relatively high bite forces, while overall stresses are reduced. Our findings resolve apparently discordant lines of evidence, i.e. the presence of teeth well adapted to sustain high loads within a lightweight cranium and mandible.     

Evolution of morphological integration in the skull of Carnivora (Mammalia): Changes in Canidae lead to increased evolutionary potential of facial traits

Morphological integration refers to the fact that different phenotypic traits of organisms are not fully independent from each other, and tend to covary to different degrees. The covariation among traits is thought to reflect properties of the species' genetic architecture and thus can have an impact on evolutionary responses. Furthermore, if morphological integration changes along the history of a group, inferences of past selection regimes might be problematic. Here, we evaluated the stability and evolution of the morphological integration of skull traits in Carnivora by using evolutionary simulations and phylogenetic comparative methods. Our results show that carnivoran species are able to respond to natural selection in a very similar way. Our comparative analyses show that the phylogenetic signal for pattern of integration is lower than that observed for morphology (trait averages), and that integration was stable throughout the evolution of the group. That notwithstanding, Canidae differed from other families by having higher integration, evolvability, flexibility, and allometric coefficients on the facial region. These changes might have allowed canids to rapidly adapt to different food sources, helping to explain not only the phenotypic diversification of the family, but also why humans were able to generate such a great diversity of dog breeds through artificial selection.     

山顶洞101号男性头骨的三维颅面复原

山顶洞101号头骨化石是东亚地区保存最为完整的化石之一,是探讨东亚地区现代人起源的重要研究材料。本文依据数据集中现生人的面部软组织平均分布,提出了计算机三维颅面复原方法,实现了101号头骨生前面貌的预测复原。主要包括三个步骤：首先使用CT完成了101号男性头骨和下颌骨仿制模型的三维重建。然后,利用计算机技术将现生人的面部软组织分布作为101号头骨的面部软组织分布,实现了颅面虚拟复原,并采用手工绘画技巧再现了复原面貌的形态特征。最后,提出了一种基于面部软组织分布和面貌统计形状模型的形态分析方法,实现了颅面复原结果的评估。山顶洞101号头骨的复原面貌具有头部较长、额头前倾、眉弓粗壮等特征,与101号头骨的几何形态基本一致。该技术再现了更新世晚期人类的脑颅及面部的形态特征,为古人类颅面复原的研究提供了技术支持和参考资料。     

Pervasive genetic integration directs the evolution of human skull shape

It has long been unclear whether the different derived cranial traits of modern humans evolved independently in response to separate selection pressures or whether they resulted from the inherent morphological integration throughout the skull. In a novel approach to this issue, we combine evolutionary quantitative genetics and geometric morphometrics to analyze genetic and phenotypic integration in human skull shape. We measured human skulls in the ossuary of Hallstatt (Austria), which offer a unique opportunity because they are associated with genealogical data. Our results indicate pronounced covariation of traits throughout the skull. Separate simulations of selection for localized shape changes corresponding to some of the principal derived characters of modern human skulls produced outcomes that were similar to each other and involved a joint response in all of these traits. The data for both genetic and phenotypic shape variation were not consistent with the hypothesis that the face, cranial base, and cranial vault are completely independent modules but relatively strongly integrated structures. These results indicate pervasive integration in the human skull and suggest a reinterpretation of the selective scenario for human evolution where the origin of any one of the derived characters may have facilitated the evolution of the others.     

Linkage disequilibrium analysis of biallelic DNA markers, human quantitative trait loci, and threshold-defined case and control subjects

Linkage disequilibrium (LD) mapping has been applied to many simple, monogenic, overtly Mendelian human traits, with great success. However, extensions and applications of LD mapping approaches to more complex human quantitative traits have not been straightforward. In this article, we consider the analysis of biallelic DNA marker loci and human quantitative trait loci in settings that involve sampling individuals from opposite ends of the trait distribution. The purpose of this sampling strategy is to enrich samples for individuals likely to possess (and not possess) trait-influencing alleles. Simple statistical models for detecting LD between a trait-influencing allele and neighboring marker alleles are derived that make use of this sampling scheme. The power of the proposed method is investigated analytically for some hypothetical gene-effect scenarios. Our studies indicate that LD mapping of loci influencing human quantitative trait variation should be possible in certain settings. Finally, we consider possible extensions of the proposed methods, as well as areas for further consideration and improvement.     

Phenotypic integration of neurocranium and brain

Evolutionary history of Mammalia provides strong evidence that the morphology of skull and brain change jointly in evolution. Formation and development of brain and skull co-occur and are dependent upon a series of morphogenetic and patterning processes driven by genes and their regulatory programs. Our current concept of skull and brain as separate tissues results in distinct analyses of these tissues by most researchers. In this study, we use 3D computed tomography and magnetic resonance images of pediatric individuals diagnosed with premature closure of cranial sutures (craniosynostosis) to investigate phenotypic relationships between the brain and skull. It has been demonstrated previously that the skull and brain acquire characteristic dysmorphologies in isolated craniosynostosis, but relatively little is known of the developmental interactions that produce these anomalies. Our comparative analysis of phenotypic integration of brain and skull in premature closure of the sagittal and the right coronal sutures demonstrates that brain and skull are strongly integrated and that the significant differences in patterns of association do not occur local to the prematurely closed suture. We posit that the current focus on the suture as the basis for this condition may identify a proximate, but not the ultimate cause for these conditions. Given that premature suture closure reduces the number of cranial bones, and that a persistent loss of skull bones is demonstrated over the approximately 150 million years of synapsid evolution, craniosynostosis may serve as an informative model for evolution of the mammalian skull.     

The Developmental Basis of Quantitative Craniofacial Variation in Humans and Mice

The human skull is a complex and highly integrated structure that has long held the fascination of anthropologists and evolutionary biologists. Recent studies of the genetics of craniofacial variation reveal a very complex and multifactorial picture. These findings contrast with older ideas that posit much simpler developmental bases for variation in cranial morphology such as the growth of the brain or the growth of the chondrocranium relative to the dermatocranium. Such processes have been shown to have major effects on cranial morphology in mice. It is not known, however, whether they are relevant to explaining normal phenotypic variation in humans. To answer this question, we obtained vectors of shape change from mutant mouse models in which the developmental basis for the craniofacial phenotype is known to varying degrees, and compared these to a homologous dataset constructed from human crania obtained from a single population with a known genealogy. Our results show that the shape vectors associated with perturbations to chondrocranial growth, brain growth, and body size in mice do largely correspond to axes of covariation in humans. This finding supports the view that the developmental basis for craniofacial variation funnels down to a relatively small number of key developmental processes that are similar across mice and humans. Understanding these processes and how they influence craniofacial shape provides fundamental insights into the developmental basis for evolutionary change in the human skull as well as the developmental-genetic basis for normal phenotypic variation in craniofacial form.     

Convergent Traits in Mammals Associated with Divergent Behaviors: the Case of the Continuous Dental Replacement in Rock-Wallabies and African Mole-Rats

The study of convergences in mammals is crucial to understand the evolutionary processes underlying the origin of shared traits. A classic example is the independent evolution in the pygmy rock-wallaby, the silvery mole-rat, and manatees of continuous dental replacement to compensate for high dental wear. The origins of continuous dental replacement in mammals remain unresolved. As the functional study of a trait may permit pinpointing the adaptive nature of its independent evolution, we aimed at comparing first the morpho-functional characteristics of the masticatory apparatus between the pygmy rock-wallaby and their closest relatives, and then with some published data on the silvery mole-rat. 3D geometric morphometric and biomechanical analyses were complemented by dental microwear analyses. Our results showed that the pygmy rock-wallaby clearly departs from its relatives in having a wider skull, a shorter snout, and a dentition situated more distally. These cranial modifications, previously observed in the silvery mole-rat, are probably linked with a neotenic development. Because of higher developmental constraints on marsupial skulls, such adjustment in the pygmy rock-wallaby may have improved the force generated by adductor muscles at molars for comminution of tough and abrasive plants. In contrast, the strong attrition combined with the ingestion of dust during high activity of digging and feeding might contribute to both molar damage and high wear in the silvery mole-rat. Our results stress the importance of combining morphological, developmental, and functional data to show that different behaviors related to ecology can explain the convergent occurrence of continuous dental replacement in mammals.     

第三臼齿退化及其在人类演化上的意义

对第三臼齿退化在世界范围内各人类群体分类数据的分析表明：人类第三臼齿先天缺失是伴随整个人类进化而发生的牙齿退化现象的一部分,这一特片在居住于不同的地理区域的人类始发的时间及增加的速率不尽一致。     

Craniometrical variability and developmental stability. Two useful tools for assessing the population viability of Eurasian otter (Lutra lutra) populations in Europe.

Morphometrical univariate analyses of otter skulls collected over the past hundred years in European countries from presumed healthy populations were compared with skulls from presumed endangered populations. The average degree of sexual dimorphism of die European populations was found to be directly correlated to die skull size of die male otters. Fluctuating asymmetry (FA) in metric skull traits was analysed as an estimator of developmental stability. There was evidence for increased FA in different traits over time in some of the presumed endangered populations, and for a reduction in size of skull traits. In contrast, the healthy populations did not show any significant changes in the same traits during the same period. The reduced sexual dimorphism of the endangered populations is suggested to be a product of relaxed sexual selection and deteriorated habitat conditions. Environmental and genetic forces that may have shaped these patterns are discussed.     

Don'T fall off the adaptation cliff: when asymmetrical fitness selects for suboptimal traits

The cliff-edge hypothesis introduces the counterintuitive idea that the trait value associated with the maximum of an asymmetrical fitness function is not necessarily the value that is selected for if the trait shows variability in its phenotypic expression. We develop a model of population dynamics to show that, in such a system, the evolutionary stable strategy depends on both the shape of the fitness function around its maximum and the amount of phenotypic variance. The model provides quantitative predictions of the expected trait value distribution and provides an alternative quantity that should be maximized ("genotype fitness") instead of the classical fitness function ("phenotype fitness"). We test the model's predictions on three examples: (1) litter size in guinea pigs, (2) sexual selection in damselflies, and (3) the geometry of the human lung. In all three cases, the model's predictions give a closer match to empirical data than traditional optimization theory models. Our model can be extended to most ecological situations, and the evolutionary conditions for its application are expected to be common in nature.     

Allometry in the distribution of material properties and geometry of the felid skull: why larger species may need to change and how they may achieve it

Extant members of the cat family (Felidae) have been considered behaviourally and morphologically conservative, i.e., despite great differences in size, there is relatively little variation in either the shape of the felid skull and dentition across species, or in the way in which these structures are used to kill and dismember prey. Consequently felids have been considered an appropriate focus for a number of investigations into the influence of allometry on craniomandibular mechanics and morphology. However, although previous treatments have considered the role of shape, they have not investigated the influence of differences in the distribution of relatively stiff cortical and more compliant cancellous bone on performance. Here, using models that incorporate material properties for both cortical and cancellous bone, we apply three-dimensional (3D) finite element analysis (FEA) to models representing the skulls of seven extant felid species. Our objectives being to determine allometric trends regarding both overall geometry and the relative distributions of cortical and cancellous bone tissue. We also more comprehensively assess variation in the efficiency with which muscular force is converted to bite force and the capacity to resist associated stresses. Our results show that the cheetah (Acinonyx jubatus) may be exceptional regarding both the efficiency with which muscular force is converted to bite force and the distribution of stress. We found a negative allometric trend between cortical bone volume and total skull bone volume, and positive allometry between the total skull bone volume and skull surface area. Results gained from mathematical modelling of beam analogies suggest that these trends reflect a need for larger species to respond to physical challenges associated with increased size, and, that changes in skull shape, bone composition, or a combination of both may be required to accommodate these challenges. With geometrical scaling stress increases by the same factor, and displacement by the same factor squared, but the ultimate failure stress of the material is invariant. We find that as species become larger, overall skull bone volume relative to surface area increases by adding a higher proportion of less dense and more compliant cancellous bone. This results in an increased cross-sectional area and second moment of inertia, which acts to reduce the overall stresses. An overall saving in mass is a likely additional consequence. Although we do find evidence that skull stiffness does diminish with size, we also argue that this is at least in part mitigated through the influence of these allometric trends. We further suggest that these trends and the explanations for them may be universal for vertebrates.     

Structural Constraints in the Evolution of the Tetrapod Skull Complexity: Williston’s Law Revisited Using Network Models

Ever since the appearance of the first land vertebrates, the skull has undergone a simplification by loss and fusion of bones in all major groups. This well-documented evolutionary trend is known as “Williston’s Law”. Both loss and fusion of bones are developmental events that generate, at large evolutionary scales, a net reduction in the number of skull bones. We reassess this evolutionary trend by analyzing the patterns of skull organization captured in network models in which nodes represent bones and links represent suture joints. We also evaluate the compensatory process of anisomerism (bone specialization) suggested to occur as a result of this reduction by quantifying the heterogeneity and the ratio of unpaired bones in real skulls. Finally, we perform simulations to test the differential effect of bone losses in skull evolution. We show that the reduction in bone number during evolution is accompanied by a trend toward a more complex organization, rather than toward simplification. Our results indicate that the processes by which bones are lost or fused during development are central to explain the evolution of the morphology of the skull. Our simulations suggest that the evolutionary trend of increasing morphological complexity can be caused as a result of a structural constraint, the systematic loss of less connected bones during development.     

Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities

Aim

Rare species typically contribute more to functional diversity than common species. However, humans have altered the occupancy and abundance patterns of many species—the basis upon which we define “rarity.” Here, we use a globally unique dataset from hydrothermal vents—an untouched ecosystem—to test whether rare species over‐contribute to functional diversity.

Location

Juan de Fuca Ridge hydrothermal vent fields, Northeast Pacific Ocean.

Methods

We first conduct a comprehensive review to set up expectations for the relative contributions of rare and common species to functional diversity. We then quantify the rarity and commonness of 37 vent species with relevant trait information to assess the relationship between rarity and functional distinctiveness—a measure of the uniqueness of the traits of a species relative to traits of coexisting species. Next, we randomly assemble communities to test whether rare species over‐contribute to functional diversity in artificial assemblages ranging in species richness. Then, we test whether biotic interactions influence functional diversity contributions by comparing the observed contribution of each species to a null expectation. Finally, we identify traits driving functional distinctiveness using a distance‐based redundancy analysis.

Results

Across functional diversity metrics and species richness levels, we find that both rare and common species can contribute functional uniqueness. Some species always offer unique trait combinations, and these species host bacterial symbionts and provide habitat complexity. Moreover, we find that contributions of species to functional diversity may be influenced by biotic interactions.

Main conclusions

Our findings show that many common species make persistent, unique contributions to functional diversity. Thus, it is key to consider whether the abundance and occupancy of species have been reduced, relative to historical baselines, when interpreting the contributions of rare species to functional diversity. Our work highlights the importance of testing ecological theory in ecosystems unaffected by human activities for the conservation of biodiversity.