Christine Tardieu

Short Adolescence in Early Hominids: Infantile and Adolescent Growth of the Human Femur

Did the first hominids have a short developmental period similar to that of the great apes or a longer period closer to that of modern humans? Evidence from studies on dental and facial growth favors the first point of view. Additional evidence presented in this report is provided by a morphogenetic analysis of the lower limb. Some morphological modifications undergone by the human femur during infantile and adolescent growth are shown to be excellent markers of different developmental stages. The angular remodelling of the femoral diaphysis, which results in femoral bicondylar angle, is a marker of infancy, while the reshaping of the distal femoral epiphysis is a marker of adolescence. This reshaping of the bony epiphysis consists of the strong projection of the external lip of the femoral trochlea, the increase of the radius of curvature of the external condyle, and the anteroposterior lengthening of the whole epiphysis. The growth spurt in linear dimensions of the femur, characteristic of human adolescence, is shown to be associated with qualitative changes of the distal femoral epiphysis engendered by the late closure of the distal epiphysis. The femur of the first hominids (Australopithecus afarensis) shows only features of infantile growth, whereas characters of both precocious and later growth are typical of later hominids (Homo). The absence of the derived epiphyseal features in Australopithecus would be linked to their early epiphyseal closure and short adolescent growth period; their presence in Homo would have been promoted by their delayed epiphyseal closure and prolonged adolescent growth period. The transition from Australopithecus to Homo appears to have involved a heterochronic process of time hypermorphosis (Gould, [1977], Ontogeny and Phylogeny [Cambridge: Harvard University Press]) in which the size of the femur increases, the epiphysis is modified, and the period of peripubertal growth is prolonged. The shape of the distal epiphyses of KNM-WT 15000, an immature Homo erectus (Brown et al. [1985] Nature 316:788-792), lies clearly within the range of modern human adolescents. In contradiction to Smiths ([1993] in A. Walker and R. Leakey [eds.]: The Nariokotome Homo erectus Skeleton [Cambridge: Harvard University Press], pp. 195-220) hypothetical reconstruction of life span of Homo erectus, we infer that a growth spurt had begun with Homo erectus but was probably less pronounced and of shorter duration than in modern humans. Our findings on the femur are consistent with studies of the growth on the hominid pelvis (Berge [1996] in LF Marcus, M Corti, A Loy, G Naylor, and DE Slice [eds.]: Advances in Morphometrics [Chicago: Plenum Publishing Corp.], pp. 441-448). It is suggested that the lengthening of the adolescent growth period, from Australopithecus to Homo, would have been also associated with the shape changes of the pelvis and with the lengthening of the lower limbs.

Ontogeny and phylogeny of femoro-tibial characters in humans and hominid fossils: Functional influence and genetic determinism

Three different human femoro-tibial characters are selected as functionally relevant and derived hominid characters: femoral bicondylar angle, shape of the femoral distal epiphysis, and the tibial insertion of the lateral meniscus. The timing and mode of formation of these characters are investigated during human ontogeny and are shown to differ considerably. The available hominid fossils (Australopithecus afarensis and early Homo) are interpreted in the light of this ontogenetic analysis with the conclusion that, during hominid evolution, different modes of selection of these features must have occurred. In modern humans, the femoral bicondylar angle proves to be an epigenetic functional feature, which develops during early childhood growth. It is present in all australopithecines and we suggest that it developed following a change in their locomotor behavior and not upon a genomic change: the early practice of bipedal walking, with adducted knee joints, in the locomotor repertoire of infant australopithecines, was sufficient to promote this angle. Later in hominid evolution, the knee joint evolved from having a single insertion of the lateral meniscus on the tibia to a double one. While Australopithecus afarensis exhibits a single insertion, early Homo clearly exhibits a double insertion of the lateral meniscus on the tibia. The double insertion restricts the mobility of the meniscus on the tibial plateau, indicating a habitual practice of full extension movements of the knee joint. Among modern humans, the posterior insertion of the lateral meniscus appears early in fetal life. Consequently in early Homo, this new selected feature developed directly as a result of a genomic change. The derived shape of human distal femoral epiphysis includes a prominence of the lateral lip of the femoral trochlea, an elliptical profile of the lateral condyle, and an anteroposterior lengthening of the epiphysis. Analysis of human fetal and neonatal distal epiphyses shows that the prominence of the lateral lip of the trochlea arises before any use, and thus appears to be genetically determined. However, the postnatal development of this joint shows that this feature is also modified epigenetically by use. It is argued that the hominid femoro-patellar joint would have been reshaped following the process of genetic assimilation (Waddington [1942] Nature 3811:563-565). The prominence of the lateral lip of the femoral trochlea was probably selected following a two-staged process-first epigenetic, then genetic. Far from being a Lamarckian explanation, this concept applies precisely to adaptive characters that are induced by an external stimulus during a single lifetime and are replaced through natural selection by genetically based equivalent characters. The nature of the structures involved in the studied features is shown to be an important parameter determining their mode of development and selection.

Three-dimensional study of pelvic asymmetry on anatomical specimens and its clinical perspectives

The aim of this study was to assess pelvic asymmetry (i.e. to determine whether the right iliac bone and the right part of the sacrum are mirror images of the left), both quantitatively and qualitatively, using three‐dimensional measurements. Pelvic symmetry was described osteologically using a common reference coordinate system for a large sample of pelvises. Landmarks were established on 12 anatomical specimens with an electromagnetic Fastrak system. Seventy‐one paired variables were tested with a paired t‐test and a non‐parametric test (Wilcoxon). A Pearson correlation matrix between the right and left values of the same variable was applied exclusively to values that were significantly asymmetric in order to calculate a dimensionless asymmetry index, ABGi, for each variable. Fifteen variables were significantly asymmetric and correlated with the right vs. left sides for the following anatomical regions: sacrum, iliac blades, iliac width, acetabulum and the superior lunate surface of the acetabulum. ABGi values above a threshold of ± 4.8% were considered significantly asymmetric in seven variables of the pelvic area. Total asymmetry involving the right and the left pelvis seems to follow a spiral path in the pelvis; in the upper part, the iliac blades rotate clockwise, and in the lower part, the pubic symphysis rotates anticlockwise. Thus, pelvic asymmetry may be evaluated in clinical examinations by measuring iliac crest orientation.

Ontogeny of the Knee Joint in Humans, Great Apes and Fossil Hominids: Pelvi-Femoral Relationships during Postnatal Growth in Humans

Results of a study of the femoral bicondylar angle in adult and juvenile humans and great apes are presented. These results raise the question of whether or not the measurement reference of this angle is valid. This is because humans and great apes have a very different growth process of the distal epiphyseal suture of the femur during the period between birth and adulthood. The approximately 3 million years old juvenile femoral diaphyses attributed to Australopithecus afarensis (AL 333-110 and AL 333-111) were also studied. These specimens show an insertion of the diaphysis into the epiphysis of the simplified type typical of modern humans. This region is more convoluted in nonhuman anthropoids. Pelvifemoral interrelations are investigated through both longitudinal and cross-sectional radiographic studies of 23 human children. Growth changes in bicondylar and collo-diaphyseal angles, total femoral and femoral neck lengths, and interacetabular distance are correlated with age and to each other. These results are used to demonstrate the distinctive features of the Australopithecus afarensis fossil, AL 288-1.

How is sagittal balance acquired during bipedal gait acquisition? Comparison of neonatal and adult pelves in three dimensions. Evolutionary implications

We compare adult and intact neonatal pelves, using a pelvic sagittal variable, the angle of sacral incidence, which presents significant correlations with vertebral curvature in adults and plays an important role in sagittal balance of the trunk on the lower limbs. Since the lumbar curvature develops in the child in association with gait acquisition, we expect a change in this angle during growth which could contribute to the acquisition of sagittal balance. To understand the mechanisms underlying the sagittal balance in the evolution of human bipedalism, we also measure the angle of incidence of hominid fossils. Fourty-seven landmarks were digitized on 50 adult and 19 intact neonatal pelves. We used a three-dimensional model of the pelvis (DE-VISU program) which calculates the angle of sacral incidence and related functional variables. Cross-sectional data from newborns and adults show that the angle of sacral incidence increases and becomes negatively correlated with the sacro-acetabular distance. During ontogeny the sacrum becomes curved, tends to sink down between the iliac blades as a wedge and moves backward in the sagittal plane relative to the acetabula, thus contributing to the backwards displacement of the center of gravity of the trunk. A chain of correlations links the degree of the sacral slope and of the angle of incidence, which is tightly linked with the lumbar lordosis. We sketch a model showing the coordinated changes occurring in the pelvis and vertebral column during the acquisition of bipedalism in infancy. In the australopithecine pelves, Sts 14 and AL 288-1, and in the Homo erectus Gona pelvis the angle of sacral incidence reaches the mean values of humans. Discussing the incomplete pelves of Ardipithecus ramidus, Australopithecus sediba and the Nariokotome Boy, we suggest how the functional linkage between pelvis and spine, observed in humans, could have emerged during hominid evolution.

Biomechanical Reasons for the Divergent Morphology of the Knee Joint and the Distal Epiphyseal Suture in Hominoids

The obliquity of the femoral diaphysis accounts for the valgus position of the human knee joint and reduces bending moments in the frontal plane. A high angle of obliquity is considered a hallmark of hominid bipedality, but its functional importance has rarely been identified correctly. A biostatic investigation of the knee joint in various realistic positions unveils resultant joint forces which do not deviate greatly from the long axis of the femoral shaft. This is due to the length of the femur and to the shortness of the human foot. The flat epiphyseal suture is more or less perpendicular to these joint forces, and the equal size of the femoral condyles reflects the even distribution of forces between them. In great apes the resultant forces acting in the knee joint vary considerably in dependence on the degree of flexion and rotation of the knee joint. The resultant joint force may be line with the femur shaft or diverge. The epiphyseal surfaces offer facets to all joint forces found in the course of the study. Due to the pronounced varus position of the knee joint, the joint itself and the adjacent part of the femur are under medially concave bending moments, which lead to higher compressive forces at the medial than at the lateral condyle. The enlarged medial condyle allows the distribution of medially displaced joint forces over a relatively large area, and the elliptic cross-section yields high bending resistance in the frontal plane. A human-like angle of obliquity is present in the early australopithecines, the values being mostly within the range of variation of children. The valgus position of the australopithecine knee joint is considered to be a functional, and epigenetic consequence of habitual bipedality. It is particularly pronounced because of the short length of the femur and the great bitrochanteric width.

Anatomical study of the proximal femur in the fetus

Two angles effectively describe the upper femur geometry: The neck shaft angle (NSA) and anteversion (AV). AV and NSA decrease from birth until they reach their adult values, but little work has focused on in-utero life. Our aim was to determine if and how AV and NSA change through the fetal life. Eighty-seven femurs from 44 formalin preserved fetuses were sampled to achieve a biometry. Correlation tests and linear regression showed that AV was highly correlated with age: AV increases during the second half of gestation. No conclusion can be given concerning NSA. It is speculated that these changes may be caused by mechanical stresses.

An anatomical and biometrical study of the femoral trochlear groove in the human fetus

We performed a biometric analysis of the femoral trochlear groove in the fetus and compared our findings with those observed in adults. We studied 44 formalin‐preserved fetuses (13–38 weeks) and used digitized images to obtain measurements (α angle of the groove, trochlear slopes θL and θM). A comparison of means between our series and adults was achieved. For each angle of the distal epiphysis (α, θL, θM) there was no significant difference between our fetal series and adults. This is the first biometric study of fetal trochlea. The morphology of the lower femur appears to be the same in the fetus and the adult.

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.

Morphogénèse de la diaphyse fémorale chez l’homme: signification fonctionnelle et évolutive

The obliquity of the femoral diaphysis, measured by the bicondylar angle, permits the adducted position of the knee in humans. The presence of a high femoral bicondylar angle has been a hallmark of hominid bipedality, but its pattern of development has not been documented. We have observed radiographic and skeletal data on the development of this angle. The two samples exhibit a pattern of a bicondylar angle of 0 degrees at birth and then a steady average increase in the angle through infancy and into the juvenile years. These data establish a high degree of potential for plasticity in the development of this angle and the direct association of a bipedal locomotion with the developmental emergence of a human femoral bicondylar angle. We show that the obliquity angle, which occasionally appears in some non-human primates, is not homologous to the human condition. As this angle is an epigenetic functional feature in modern humans, we suggest that it developed following a change in infantile locomotor behaviour of the early australopithecines and was not the result of a genomic change.