Functional integrative analysis of the human hip joint: the three-dimensional orientation of the acetabulum and its relation with the orientation of the femoral neck.

In humans, the hip joint occupies a central place in the locomotor system, as it plays an important role in body support and the transmission of the forces between the trunk and lower limbs. The study of the three-dimensional biomechanics of this joint has important implications for documenting the morphological changes associated with the acquisition of a habitual bipedal gait in humans. Functional integration at any joint has important implications in joint stability and performance. The aim of the study was to evaluate the functional integration at the human hip joint. Both the level of concordance between the three-dimensional axes of the acetabulum and the femoral neck in a bipedal posture, and patterns of covariation between these two axes were analysed. First, inter-individual variations were quantified and significant differences in the three-dimensional orientations of both the acetabulum and the femoral neck were detected. On a sample of 57 individuals, significant patterns of covariation were identified, however, the level of concordance between the axes of both the acetabulum and the femoral neck in a bipedal posture was lower than could be expected for a key joint such as the hip. Patterns of covariation were explored regarding the complex three-dimensional biomechanics of the full pelvic-femoral complex. Finally, we suggest that the lower degree of concordance observed at the human hip joint in a bipedal posture might be partly due to the phylogenetic history of the human species.

Does shape co-variation between the skull and the mandible have functional consequences? A 3D approach for a 3D problem.

Morpho-functional patterns are important drivers of phenotypic diversity given their importance in a fitness-related context. Although modularity of the mandible and skull has been studied extensively in mammals, few studies have explored shape co-variation between these two structures. Despite being developmentally independent, the skull and mandible form a functionally integrated unit. In the present paper we use 3D surface geometric morphometric methods allowing us to explore the form of both skull and mandible in its 3D complexity using the greater white-toothed shrew as a model. This approach allows an accurate 3D description of zones devoid of anatomical landmarks that are functionally important. Two-block partial least-squares approaches were used to describe the co-variation of form between skull and mandible. Moreover, a 3D biomechanical model was used to explore the functional consequences of the observed patterns of co-variation. Our results show the efficiency of the method in investigations of complex morpho-functional patterns. Indeed, the description of shape co-variation between the skull and the mandible highlighted the location and the intensity of their functional relationships through the jaw adductor muscles linking these two structures. Our results also demonstrated that shape co-variation in form between the skull and mandible has direct functional consequences on the recruitment of muscles during biting.

Study of the three-dimensional orientation of the labrum: its relations with the osseous acetabular rim.

Understanding the three-dimensional orientation of the coxo-femoral joint remains a challenge as an accurate three-dimensional orientation ensure an efficient bipedal gait and posture. The quantification of the orientation of the acetabulum can be performed using the three-dimensional axis perpendicular to the plane that passes along the edge of the acetabular rim. However, the acetabular rim is not regular as an important indentation in the anterior rim was observed. An innovative cadaver study of the labrum was developed to shed light on the proper quantification of the three-dimensional orientation of the acetabulum. Dissections on 17 non-embalmed corpses were performed. Our results suggest that the acetabular rim is better represented by an anterior plane and a posterior plane rather than a single plane along the entire rim as it is currently assumed. The development of the socket from the Y-shaped cartilage was suggested to explain the different orientations in these anterior and posterior planes. The labrum forms a plane that takes an orientation in between the anterior and posterior parts of the acetabular rim, filling up inequalities of the bony rim. The vectors V(L) , V(A2) and V(P) , representing the three-dimensional orientation of the labrum, the anterior rim and the posterior rim, are situated in a unique plane that appears biomechanically dependent. The three-dimensional orientation of the acetabulum is a fundamental parameter to understand the hip joint mechanism. Important applications for hip surgery and rehabilitation, as well as for physical anthropology, were discussed.

A three-dimensional axis for the study of femoral neck orientation.

A common problem in the quantification of the orientation of the femoral neck is the difficulty to determine its true axis; however, this axis is typically estimated visually only. Moreover, the orientation of the femoral neck is commonly analysed using angles that are dependent on anatomical planes of reference and only quantify the orientation in two dimensions. The purpose of this study is to establish a method to determine the three-dimensional orientation of the femoral neck using a three-dimensional model. An accurate determination of the femoral neck axis requires a reconsideration of the complex architecture of the proximal femur. The morphology of the femoral neck results from both the medial and arcuate trabecular systems, and the asymmetry of the cortical bone. Given these considerations, two alternative models, in addition to the cylindrical one frequently assumed, were tested. The surface geometry of the femoral neck was subsequently used to fit one cylinder, two cylinders and successive cross-sectional ellipses. The model based on successive ellipses provided a significantly smaller average deviation than the two other models (P < 0.001) and reduced the observer-induced measurement error. Comparisons with traditional measurements and analyses on a sample of 91 femora were also performed to assess the validity of the model based on successive ellipses. This study provides a semi-automatic and accurate method for the determination of the functional three-dimensional femoral neck orientation avoiding the use of a reference plane. This innovative method has important implications for future studies that aim to document and understand the change in the orientation of the femoral neck associated with the acquisition of a bipedal gait in humans. Moreover, the precise determination of the three-dimensional orientation has implications in current research involved in developing clinical applications in diagnosis, hip surgery and rehabilitation.

Technical note: Shape variability induced by reassembly of human pelvic bones.

In traditional as well as in geometric morphometric studies, the shape of the pelvis is often quantified after the reassembly of the two hip bones and the sacrum. However, on dry bones, the morphology of the cartilaginous tissues that form the two sacroiliac joints and the pubic symphysis before death remains unknown, leading to potential inaccuracies and errors during the reassembly process. A protocol was established to investigate the effects of reassembly on the quantification of pelvis shape. The shape of fresh pelves obtained after dissection, in which the three bones are in an anatomically relevant position, was compared with the shape of different reassemblies based on the individual dry bones of the same individuals. Our results demonstrated a significant effect of the reassembly. Variation in the reassembly process is likely related, first, to the complete absence of cartilaginous tissues on dry bones and, second, to the morphology of the sacroiliac joint which, in vivo, allows physiological movements, resulting in different potential positions of the two sacroiliac surfaces relative to one another. However, the artificial variation introduced by the reassembly process appears small compared with the biological variation between the different individuals.

Extreme male leg polymorphic asymmetry in a new empidine dance fly (Diptera: Empididae).

A new dance fly (Empididae: Empidinae) with hugely modified male fore tarsus, either on the right, left, both or neither sides, is described from Japan. Such massive polymorphic asymmetry occurring with so high an incidence in a population is previously unreported. In view of the courtship behaviour of other Empidinae, we hypothesize that the oversized tarsus is a secondary sexual character employed by males for attracting females. Alternative hypotheses are also discussed. We suggest that this extraordinary new species is a potential model for the study of mating biology in Empidinae and the evolution of mating systems in general.

Geometric morphometrics as a tool for improving the comparative study of behavioural postures.

Describing postures has always been a central concern when studying behaviour. However, attempts to compare postures objectively at phylogenetical, populational, inter- or intra-individual levels generally either rely upon a few key elements or remain highly subjective. Here, we propose a novel approach, based on well-established geometric morphometrics, to describe and to analyse postures globally (i.e. considering the animal's body posture in its entirety rather than focusing only on a few salient elements, such as head or tail position). Geometric morphometrics is concerned with describing and comparing variation and changes in the form (size and shape) of organisms using the coordinates of a series of homologous landmarks (i.e. positioned in relation to skeletal or muscular cues that are the same for different species for every variety of form and function and that have derived from a common ancestor, i.e. they have a common evolutionary ancestry, e.g. neck, wings, flipper/hand). We applied this approach to horses, using global postures (1) to characterise behaviours that correspond to different arousal levels, (2) to test potential impact of environmental changes on postures. Our application of geometric morphometrics to horse postures showed that this method can be used to characterise behavioural categories, to evaluate the impact of environmental factors (here human actions) and to compare individuals and groups. Beyond its application to horses, this promising approach could be applied to all questions involving the analysis of postures (evolution of displays, expression of emotions, stress and welfare, behavioural repertoires…) and could lead to a whole new line of research.

Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup.

BACKGROUND: Sexual dimorphism of body size has been the subject of numerous studies, but few have examined sexual shape dimorphism (SShD) and its evolution. Allometry, the shape change associated with size variation, has been suggested to be a main component of SShD. Yet little is known about the relative importance of the allometric and non-allometric components for the evolution of SShD. RESULTS: We investigated sexual dimorphism in wing shape in the nine species of the Drosophila melanogaster subgroup. We used geometric morphometrics to characterise wing shape and found significant SShD in all nine species. The amount of shape difference and the diversity of the shape changes evolved across the group. However, mapping the divergence of SShD onto the phylogeny of the Drosophila melanogaster subgroup indicated that there is little phylogenetic signal. Finally, allometry accounted for a substantial part of SShD, but did not explain the bulk of evolutionary divergence in SShD because allometry itself was found to be evolutionarily plastic. CONCLUSION: SShD in the Drosophila wing can evolve rapidly and therefore shows only weak phylogenetic structure. The variable contribution of allometric and non-allometric components to the evolutionary divergence of SShD and the evolutionary plasticity of allometry suggest that SShD and allometry are influenced by a complex interaction of processes.

Comprehensive evolutionary analysis of the Anthroherpon radiation (Coleoptera, Leiodidae, Leptodirini).

The genus Anthroherpon Reitter, 1889 exhibits the most pronounced troglomorphic characters among Coleoptera, and represents one of the most spectacular radiations of subterranean beetles. However, radiation, diversification, and biogeography of this genus have never been studied in a phylogenetic context. This study provides a comprehensive evolutionary analysis of the Anthroherpon radiation, using a dated molecular phylogeny as a framework for understanding Anthroherpon diversification, reconstructing the ancestral range, and exploring troglomorphic diversity. Based on 16 species and 22 subspecies, i.e. the majority of Anthroherpon diversity, we reconstructed the phylogeny using Bayesian analysis of six loci, both mitochondrial and nuclear, comprising a total of 4143 nucleotides. In parallel, a morphometric analysis was carried out with 79 landmarks on the body that were subjected to geometric morphometrics. We optimized morphometric features to phylogeny, in order to recognize the way troglomorphy was expressed in different clades of the tree, and did character evolution analyses. Finally, we reconstructed the ancestral range of the genus using BioGeoBEARS. Besides further elucidating the suprageneric classification of the East-Mediterranean Leptodirini, our main findings also show that Anthroherpon dates back to the Early Miocene (ca. 22 MYA) and that the genus diversified entirely underground. Biogeographic reconstruction of the ancestral range shows the origin of the genus in the area comprising three high mountains in western Montenegro, which is in the accordance with the available data on the paleogeography of the Balkan Peninsula. Character evolution analysis indicates that troglomorphic morphometric traits in Anthroherpon mostly evolve neutrally but may diverge adaptively under syntopic competition.

Shape patterns of genital papillae in pinworms (Enterobiinae, Oxyurida, Nematoda) parasite of primates: a landmark analysis.

The Enterobiinae includes 47 species of pinworms parasite of primates. A previous cladistic analysis of this subfamily supported its monophyly and its subdivision into three genera. Based on morphological characters, this cladistic analysis excluded characters describing the shape of the genital papillae of male pinworms, because the corresponding patterns could not be described using discrete characters. In this study, the shape of the genital papillae of the males of 35 within the 47 species is analyzed using geometric morphometric approaches. The aims of this study are to investigate: (i) the relationships between the phylogeny and the shape patterns of the caudal bursa, (ii) the shape differences between and within monophyletic groups, and (iii) the functional implications of the shape patterns observed within the subfamily. Results demonstrate that different patterns of evolution of the caudal bursa, each one characterized by a particular spatial distribution of the phasmids and genital papillae may be recognized, which are consistent with the classification of the Enterobiinae into three groups. On the whole, these patterns may be related to particular mating behavior of the pinworms. When incongruence is observed between shape patterns distribution and species distribution into monophyletic groups, they are found to correspond to homoplasic events. This suggests that convergent selective pressures are involved in the evolution of the shape of the genital papillae. This analysis also confirms that morphometric shape patterns cannot be interpreted unequivocally without the support of a pre-existing phylogenetic framework.

Geographic variation of melanisation patterns in a hornet species: genetic differences, climatic pressures or aposematic constraints?

Coloration of stinging insects is often based on contrasted patterns of light and black pigmentations as a warning signal to predators. However, in many social wasp species, geographic variation drastically modifies this signal through melanic polymorphism potentially driven by different selective pressures. To date, surprisingly little is known about the geographic variation of coloration of social wasps in relation to aposematism and melanism and to genetic and developmental constraints. The main objectives of this study are to improve the description of the colour variation within a social wasp species and to determine which factors are driving this variation. Therefore, we explored the evolutionary history of a polymorphic hornet, Vespa velutina Lepeletier, 1836, using mitochondrial and microsatellite markers, and we analysed its melanic variation using a colour space based on a description of body parts coloration. We found two main lineages within the species and confirmed the previous synonymy of V. auraria Smith, 1852, under V. velutina, differing only by the coloration. We also found that the melanic variation of most body parts was positively correlated, with some segments forming potential colour modules. Finally, we showed that the variation of coloration between populations was not related to their molecular, geographic or climatic differences. Our observations suggest that the coloration patterns of hornets and their geographic variations are determined by genes with an influence of developmental constraints. Our results also highlight that Vespa velutina populations have experienced several convergent evolutions of the coloration, more likely influenced by constraints on aposematism and Müllerian mimicry than by abiotic pressures on melanism.

Nasal bone shape is under complex epistatic genetic control in mouse interspecific recombinant congenic strains.

BACKGROUND: Genetic determinism of cranial morphology in the mouse is still largely unknown, despite the localization of putative QTLs and the identification of genes associated with Mendelian skull malformations. To approach the dissection of this multigenic control, we have used a set of interspecific recombinant congenic strains (IRCS) produced between C57BL/6 and mice of the distant species Mus spretus (SEG/Pas). Each strain has inherited 1.3% of its genome from SEG/Pas under the form of few, small-sized, chromosomal segments. RESULTS: The shape of the nasal bone was studied using outline analysis combined with Fourier descriptors, and differential features were identified between IRCS BcG-66H and C57BL/6. An F2 cross between BcG-66H and C57BL/6 revealed that, out of the three SEG/Pas-derived chromosomal regions present in BcG-66H, two were involved. Segments on chromosomes 1 (∼32 Mb) and 18 (∼13 Mb) showed additive effect on nasal bone shape. The three chromosomal regions present in BcG-66H were isolated in congenic strains to study their individual effect. Epistatic interactions were assessed in bicongenic strains. CONCLUSIONS: Our results show that, besides a strong individual effect, the QTL on chromosome 1 interacts with genes on chromosomes 13 and 18. This study demonstrates that nasal bone shape is under complex genetic control but can be efficiently dissected in the mouse using appropriate genetic tools and shape descriptors.

Exploration of the genetic organization of morphological modularity on the mouse mandible using a set of interspecific recombinant congenic strains between C57BL/6 and mice of the Mus spretus species.

Morphological integration and modularity within semi-autonomous modules are essential mechanisms for the evolution of morphological traits. However, the genetic makeup responsible for the control of variational modularity is still relatively unknown. In our study, we tested the hypothesis that the genetic variation for mandible shape clustered into two morphogenetic components: the alveolar group and the ascending ramus. We used the mouse as a model system to investigate genetics determinants of mandible shape. To do this, we used a combination of geometric morphometric tools and a set of 18 interspecific recombinant congenic strains (IRCS) derived from the distantly related species, Mus spretus SEG/Pas and Mus musculus C57BL/6. Quantitative trait loci (QTL) analysis comparing mandible morphometry between the C57BL/6 and the IRCSs identified 42 putative SEG/Pas segments responsible for the genetic variation. The magnitude of the QTL effects was dependent on the proportion of SEG/Pas genome inherited. Using a multivariate correlation coefficient adapted for modularity assessment and a two-block partial least squares analysis to explore the morphological integration, we found that these QTL clustered into two well-integrated morphogenetic groups, corresponding to the ascending ramus and the alveolar region. Together, these results provide evidence that the mouse mandible is subjected to genetic coordination in a modular manner.

Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between C57BL/6 and mice of the mus spretus species.

To assess the genetic basis of the skull shape variation and morphological integration in mice, we have used a tool based on the cross between the distantly related mouse species Mus spretus (SEG/Pas strain) and the laboratory strain C57BL/6 called interspecific recombinant congenic strains (IRCSs). The genome of each IRCS consists on average of 1.3% of SEG/Pas derived sequences, located on multiple chromosomes as small-sized, DNA segments. Quantitative trait loci (QTL) on the skull shape, separated into dorsal and ventral sides, were analyzed in 17 IRCSs by a Procrustes superimposition method using 3D landmarks. The shapes of 16 strains differed significantly from C57BL/6. Discrepancy in the QTLs effects was found between the dorsal side and the anterior region of the ventral side due to a differential effect of the SEG/Pas alleles on the skull shape. A comprehensive analysis of all allelic combinations of the BCG-66H strain showed strong epistatic interactions between SEG/Pas segment acting on both skull sides. Epistatic pleiotropy and covariation between sides were dependent in SEG/Pas alleles direction and contributed to the strong morphological integration between sides. Introduction of Mus spretus alleles in a C57BL/6 background induced strong morphological changes mostly in SEG/Pas alleles direction and provided evidence for high level of morphological integration.

Exploring artificial cranial deformation using elliptic Fourier analysis of Procrustes aligned outlines.

The anatomical effects of artificial cranial deformation on the face and the base have been subject to various metric approaches, including standard linear as well as finite element techniques, and have produced controversial results (Antón [1989] Am. J. Phys. Anthropol. 79:253-267; Kohn et al. [1993] Am. J. Phys. Anthropol. 90:147-158). It can be argued that diverging observations partly result from methodological constraints. The present study compares samples of intentionally deformed and undeformed human crania, using elliptic Fourier analysis (EFA), a morphometric approach which has been shown to be particularly appropriate for characterizing the shape of two-dimensional outlines and associated shape changes. We improve the standard EFA approach by adding a preliminary orientation of the outlines following the rotation parameters of a Procrustes superimposition, using multiple homologous landmarks called control points. The results confirm that circumferentially deformed skulls exhibit modifications of the basioccipital region, together with increased anterior and inferior facial projection. However, the degree to which basioccipital flattening is modified in circumferentially deformed Peruvians was found to be less marked than changes observed in the face. Some of the modifications observed here can be related to morphological trends existing in the population from which our sample was taken. The observation of other modifications may be subject to methodological constraints of standard morphometric approaches.

Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional Procrustes analysis.

Heterochronic studies compare ontogenetic trajectories of an organ in different species: here, the skulls of common chimpanzees and modern humans. A growth trajectory requires three parameters: size, shape, and ontogenetic age. One of the great advantages of the Procrustes method is the precise definition of size and shape for whole organs such as the skull. The estimated ontogenetic age (dental stages) is added to the plot to give a graphical representation to compare growth trajectories. We used the skulls of 41 Homo sapiens and 50 Pan troglodytes at various stages of growth. The Procrustes superimposition of all specimens was completed by statistical procedures (principal component analysis, multivariate regression, and discriminant function) to calculate separately size-related shape changes (allometry common to chimpanzees and humans), and interspecific shape differences (discriminant function). The results confirm the neotenic theory of the human skull (sensu Gould [1977] Ontogeny and Phylogeny, Cambridge: Harvard University Press; Alberch et al. [1979] Paleobiology 5:296-317), but modify it slightly. Human growth is clearly retarded in terms of both the magnitude of changes (size-shape covariation) and shape alone (size-shape dissociation) with respect to the chimpanzees. At the end of growth, the adult skull in humans reaches an allometric shape (size-related shape) which is equivalent to that of juvenile chimpanzees with no permanent teeth, and a size which is equivalent to that of adult chimpanzees. Our results show that human neoteny involves not only shape retardation (paedomorphosis), but also changes in relative growth velocity. Before the eruption of the first molar, human growth is accelerated, and then strongly decelerated, relative to the growth of the chimpanzee as a reference. This entails a complex process, which explains why these species reach the same overall (i.e., brain + face) size in adult stage. The neotenic traits seem to concern primarily the function of encephalization, but less so other parts of the skull. Our results, based on the discriminant function, reveal that additional structural traits (corresponding to the nonallometric part of the shape which is specific to humans) are rather situated in the other part of the skull. They mainly concern the equilibrium of the head related to bipedalism, and the respiratory and masticatory functions. Thus, the reduced prognathism, the flexed cranial base (forward position of the foramen magnum which is brought closer to the palate), the reduced anterior portion of the face, the reduced glabella, and the prominent nose mainly correspond to functional innovations which have nothing to do with a neotenic process in human evolution. The statistical analysis used here gives us the possibility to point out that some traits, which have been classically described as paedomorphic because they superficially resemble juvenile traits, are in reality independent of growth.