Relationship between formation of the femoral bicondylar angle and trochlear shape: independence of diaphyseal and epiphyseal growth

During hominin evolution, an increase in the femoral bicondylar angle was the initial change that led to selection for protuberance of the lateral trochlear lip and the elliptical profile of the lateral condyle. No correlation is found during ontogeny between the degree of femoral obliquity and of the prominence of the lateral trochlear lip. Might there be a relationship with the elliptical profile of the lateral condyle? On intact femoral diaphyses of juvenile humans and great apes, we compared the anteroposterior length of the lateral and medial sides of the distal metaphysis. The two diaphyseal pillars remain equal during postnatal growth in great apes, while the growth of the lateral pillar far exceeds that of the medial pillar in humans. Increase in bicondylar angle is correlated with disproportionate anteroposterior lengthening of the lateral pillar. The increased anteroposterior length of the lateral side of the metaphysis would contribute to increasing the radius of the curvature of the lateral condyle, but not to the projection of the lateral trochlear lip. The similar neonatal and adult femoro‐patellar joint shape in humans prompted an assessment of the similarity during growth of the entire neonatal and adult epiphyses. We showed that the entire epiphysis undergoes drastic changes in proportions during postnatal growth. Finally, we emphasize the need to distinguish the cartilaginous phenotype and the ossified phenotype of the distal femoral epiphysis (and of any epiphysis) during postnatal growth. This crucial distinction applies to most postcranial bones, for they almost all develop following the process of endochondral ossification. Am J Phys Anthropol, 2006. © 2006 Wiley‐Liss, Inc.     

Effects of age and gender on the location and orientation of the foramen magnum in rhesus macaques (Macaca mulatta)

Endocasts from 378 rhesus macaque skulls from the Cayo Santiago skeletal collection were measured to determine the effects of age and gender on the position and orientation of the foramen magnum. The foramen magnum migrates from a rostral to a caudal position and its angle changes during postnatal development. The angles and relative positions of the foramen magnum are similar for both genders of infants and for both genders of adults. However, analyses of linear response and plateau (LRP) functions reveal significant differences between males and females in the timing of reorientation of the angle and migration of the foramen magnum. The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. A similar pattern is observed for the brainstem region of the basicranium. Mean adult lengths of the brainstem region are reached at 5.2 years in females and 7.1 years in males. The relationships between cranial capacity, the growth pattern of the brainstem, and the pattern of change for the angle and the relative position of the foramen magnum are examined. Quantification of the effects of age and gender on the location of the foramen magnum in a large sample of endocasts from one species of higher primate has potential implications for research on human development, and for interpretation of juvenile specimens in the hominid fossil record.     

Femoral/humeral strength in early African Homo erectus

Lower-to-upper limb-bone proportions give valuable clues to locomotor behavior in fossil taxa. However, to date only external linear dimensions have been included in such analyses of early hominins. In this study, cross-sectional measures of femoral and humeral diaphyseal strength are determined for the two most complete early Homo erectus (or ergaster) associated skeletons--the juvenile KNM-WT 15000 and the adult KNM-ER 1808. Modern comparative samples include an adult human skeletal sample representative of diverse body shapes, a human longitudinal growth series, and an adult chimpanzee sample. When compared to appropriately age-matched samples, both H. erectus specimens fall very close to modern human mean proportions and far from chimpanzee proportions (which do not overlap with those of humans). This implies very similar mechanical load-sharing between the lower and upper limbs, and by implication, similar locomotor behavior in early H. erectus and modern humans. Thus, by the earliest Pleistocene (1.7 Ma), completely modern patterns of bipedal behavior were fully established in at least one early hominin taxon.     

Articular and diaphyseal remodeling of the proximal femur with changes in body mass in adults.

Proximal femoral dimensions were measured from radiographs of 80 living subjects whose current body weight and body weight at initial skeletal maturity (18 years) could be ascertained. Results generally support the hypothesis that articular size does not change in response to changes in mechanical loading (body weight) in adults, while diaphyseal cross-sectional size does. This can be explained by considering the different bone remodeling constraints characteristic of largely trabecular bone regions (articulations) and largely compact cortical bone regions (diaphyses). The femoral neck shows a pattern apparently intermediate between the two, consistent with its structure. When the additional statistical "noise" created by an essentially static femoral head size is accounted for, the present study supports other studies that have demonstrated rather marked positive allometry in femoral articular and shaft cross-sectional dimensions to body mass among adult humans. Body weight prediction equations developed from these data give reasonable results for modern U.S. samples, with average percent prediction errors of about 10%-16% for individual weights and about 2% for sample mean weights using the shaft dimension equations. When predicting body weight from femoral head size in earlier human samples, a downward correction factor of about 10% is suggested to account for the increased adiposity of very recent U.S. adults.     

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.     

Sex determination of prehistoric central California skeletal remains using discriminant analysis of the femur and humerus

A large sample (n = 370) of Central California prehistoric skeletal remains was analyzed for sexual dimorphism of long bones using nine femoral and nine humeral dimensions. Sex of all individuals was assessed using traits of the os pubis. Discriminant analysis was done separately for the robust Early Horizon sample and the Middle/Late Horizon sample. Use of multiple variables did not produce appreciably better results over the use of several of the best variables, analyzed singly. Attention is focused on measurements of maximum diameter femoral head, femoral bicondylar width, and diameter of the humeral head (transverse or vertical). These variables produce excellent separation of the sexes with about 90% accuracy for the Middle/Late Horizon sample. They have been overlooked in the recent literature in which the relative values of length versus midshaft dimensions are debated. The measurements found to be superior in this study are taken at the ends of the bones where durability of these regions is indicated by large sample sizes found in this study. We suggest workers redirect their focus from the midshaft to the ends of the long bones. The discriminant analyses presented here have greater accuracy than most claims for either long bone or cranial sex determination. These standards, based on two samples with differing robusticity, may have applicability for workers in other areas who lack large skeletal samples.     

Body size estimators in primate skeletal material

A series of twenty-three skeletal variables are tested for their utility as estimators of body size, measured as partial skeletal weight, over 286 Old World anthropoids. Several variables proved to be consistently accurate in this for the present sample: bizygomatic breadth, bicondylar femoral width, skull length, orbital width, basioninion, femoral circumference and vertebral area. The only reasonably acceptable mandibular measurement was mandibular breadth. Other variables that have been used as size estimators in previous studies proved to be less accurate.     

The place of Neandertals in the evolution of hominid patterns of growth and development

This study uses the two developmental fields of dental maturation and femoral growth to determine if the pattern of growth and development in Neandertals (archaic Homo sapiens) was intermediate between that of Homo erectus and recent modern humans. Specimens used in the analysis included Neandertals and Upper Palaeolithic early modern Homo sapiens from Europe and individuals from two recent modern human populations. Ontogenetic data for the H. erectus adolescent KNM-WT 15000 and for Gorilla gorilla were included for comparison. Previous reports have indicated that H. erectus demonstrates a pattern of ontogeny characterized by earlier and more rapid linear growth than in modern humans. Results reported here demonstrate that Upper Paleolithic early modern Homo sapiens display a growth trajectory indistinguishable from that of recent modern humans. The pattern of Neandertal ontogeny is not intermediate between the pattern displayed in H. erectus and the derived pattern seen in the modern reference samples and the early modern H. sapiens sample. The Neandertal growth trajectory is consistent with either slow linear growth or advanced dental development.     

Adaptive benefits of differential post-fledging development patterns in the Lesser Flamingo (Phoenicopterus minor)

Measurements of five morphological components (mass, skull length, culmen, flattened wing and tarsus) and blood samples were taken from 154 fledged wild Lesser Flamingos Phoenicopterus minor captured during 2001 and 2002 at Lake Bogoria, Kenya (0°11'–20'N, 036°06'E). The sample included adults (>3 years old), immature birds (2–3 years old) and first-year juvenile birds of both sexes. The sex of each bird was determined by PCR amplification of the CHD-Z and CHD-W genes, using DNA extracted from blood samples. Within each gender, there were significant differences in mass and tarsus length amongst the three age groups, indicating that the skeletal size and mass of Lesser Flamingos continue to increase between fledging and attainment of adult plumage at three to four years of age. The different morphological components increased in size at different rates, although the same components appeared to increase at similar rates in both males and females. Skull and culmen lengths had reached adult size in juvenile birds, while juvenile wing length, tarsus length and mass were approximately 95%, 85% and 75% of adult size, respectively. The adaptive significance of these findings is discussed.     

Age differences in craniofacial dimensions among adults from Indian Knoll,Kentucky

Adult craniofacial expansion with aging has recently been documented in a living US white population sample (Israel, '73a, '77). The present study extends these findings to a prehistoric Amerindian skeletal sample from the Indian Knoll, Kentucky site. Sixteen craniofacial dimensions available for 136 adult males were compared in younger (20–34 years) and older (35–50 years) age groups. Of these, six dimensions showed a significant difference between age groups; all significantly different dimensions were larger in the older adult age group. The multivariate (T²) difference between age groups was highly significant. Comparison of results before and after a size standardization indicated that the majority of differences between age groups were associated with an overall size increase, or expansion with aging, and did not represent merely remodeling, or “shape” changes. The pattern of craniofacial change with age appeared generally similar to that observed in the modern US white sample; however, some differences were noted. It is shown that the age trends observed at Indian Knoll are most likely to reflect true craniofacial growth in size among the adult male inhabitants of the site, rather than secular trends or other artifacts of the sampling procedure. The causes for continuing adult craniofacial expansion are unknown, and probably involve a complex interaction of many factors. However, this pattern of change with age among adults does appear to be characteristic of population samples of widely differing genetic and environmental backgrounds.     

The ontogeny of Holocene and Late Pleistocene human postcranial strength

While a wide variety of studies have focused on population variation in adult cross‐sectional properties, relatively little is known about population variation in postcranial robusticity in immature individuals. Furthermore, the age at which the population differences readily detected in adults manifest during growth is also unknown. This research addresses these gaps in our current understanding through the analysis of immature humeral and femoral long bone strength. Cross‐sectional geometry was used to compare the developmental trajectories of diaphyseal strength in Late Pleistocene Neandertal and modern human subadults to a sample of immature humans from seven geographically diverse Holocene populations. Population differences in size‐standardized cross‐sectional properties appear to be systemic and develop very early in ontogeny in the Holocene sample. In many cases, these differences are present before one year of age. In general, the Late Pleistocene fossil samples fit within the range of recent human variation in long bone strength. Population differences detected here are likely related to a combination of factors including activity patterns, genetic propensities, and nutritional status. These results highlight the complex mosaic of processes that result in adult postcranial robusticity, and suggest that further exploration of the developmental interplay between intrinsic and extrinsic influences on skeletal robusticity will likely enhance our understanding of adult postcranial morphology. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Trabecular bone ontogeny in the human proximal femur

Ontogenetic changes in the human femur associated with the acquisition of bipedal locomotion, especially the development of the bicondylar angle, have been well documented. The purpose of this study is to quantify changes in the three-dimensional structure of trabecular bone in the human proximal femur in relation to changing functional and external loading patterns with age. High-resolution X-ray computed tomography scan data were collected for 15 juvenile femoral specimens ranging in age from prenatal to approximately nine years of age. Serial slices were collected for the entire proximal femur of each individual with voxel resolutions ranging from 0.017 to 0.046 mm depending on the size of the specimen. Spherical volumes of interest were defined within the proximal femur, and the bone volume fraction, trabecular thickness, trabecular number, and fabric anisotropy were calculated in three dimensions. Bone volume fraction, trabecular number, and degree of anisotropy decrease between the age of 6 months and 12 months, with the lowest values for these parameters occurring in individuals near 12 months of age. By age 2-3 years, the bone volume, thickness, and degree of anisotropy increase slightly, and regions in the femoral neck become more anisotropic corresponding to the thickening of the inferior cortical bone of the neck. These results suggest that trabecular structure in the proximal femur reflects the shift in external loading patterns associated with the initiation of unassisted walking in infants.     

Human body mass estimation: a comparison of "morphometric" and "mechanical" methods

In the past, body mass was reconstructed from hominin skeletal remains using both "mechanical" methods which rely on the support of body mass by weight-bearing skeletal elements, and "morphometric" methods which reconstruct body mass through direct assessment of body size and shape. A previous comparison of two such techniques, using femoral head breadth (mechanical) and stature and bi-iliac breadth (morphometric), indicated a good general correspondence between them (Ruff et al. [1997] Nature 387:173-176). However, the two techniques were never systematically compared across a large group of modern humans of diverse body form. This study incorporates skeletal measures taken from 1,173 Holocene adult individuals, representing diverse geographic origins, body sizes, and body shapes. Femoral head breadth, bi-iliac breadth (after pelvic rearticulation), and long bone lengths were measured on each individual. Statures were estimated from long bone lengths using appropriate reference samples. Body masses were calculated using three available femoral head breadth (FH) formulae and the stature/bi-iliac breadth (STBIB) formula, and compared. All methods yielded similar results. Correlations between FH estimates and STBIB estimates are 0.74-0.81. Slight differences in results between the three FH estimates can be attributed to sampling differences in the original reference samples, and in particular, the body-size ranges included in those samples. There is no evidence for systematic differences in results due to differences in body proportions. Since the STBIB method was validated on other samples, and the FH methods produced similar estimates, this argues that either may be applied to skeletal remains with some confidence.     

Evaluating developmental shape changes in Homo antecessor subadult facial morphology

The fossil ATD6-69 from Atapuerca, Spain, dated to ca. 900 ka (thousands of years ago) has been suggested to mark the earliest appearance of modern human facial features. However, this specimen is a subadult and the interpretation of its morphology remains controversial, because it is unclear how developmental shape changes would affect the features that link ATD6-69 to modern humans. Here we analyze ATD6-69 in an evolutionary and developmental context. Our modern human sample comprises cross-sectional growth series from four populations. The fossil sample covers human specimens from the Pleistocene to the Upper Paleolithic, and includes several subadult Early Pleistocene humans and Neanderthals. We digitized landmarks and semilandmarks on surface and CT scans and analyzed the Procrustes shape coordinates using multivariate statistics. Ontogenetic allometric trajectories and developmental simulations were employed in order to identify growth patterns and to visualize potential adult shapes of ATD6-69. We show that facial differences between modern and archaic humans are not exclusively allometric. We find that while postnatal growth further accentuates the differences in facial features between Neanderthals and modern humans, those features that have been suggested to link ATD6-69's morphology to modern humans would not have been significantly altered in the course of subsequent development. In particular, the infraorbital depression on this specimen would have persisted into adulthood. However, many of the facial features that ATD6-69 shares with modern humans can be considered to be part of a generalized pattern of facial architecture. Our results present a complex picture regarding the polarity of facial features and demonstrate that some modern human-like facial morphology is intermittently present in Middle Pleistocene humans. We suggest that some of the facial features that characterize recent modern humans may have developed multiple times in human evolution.     

Sex determination in the Lesser Flamingo (Phoenicopterus minor) using morphological measurements

Morphological measurements and blood samples were taken from 154 Lesser Flamingos Phoenicopterus minor, including adults (>3 years old), immature sub-adults (2–3 years old) and first-year juvenile birds of both sexes, captured at Lake Bogoria, Kenya (0°11'–20' N, 036°06' E) during 2001 and 2002. PCR amplification of the CHD-Z and CHD-W genes using DNA extracted from the blood samples was used to determine the sex of each bird. There were significant differences in mass and tarsus length among the three age groups, indicating that Lesser Flamingos continue to grow in skeletal size and mass between fledging and the attainment of adult plumage at 3–4 years of age. On average, males were significantly larger than females in all age groups, although there was substantial overlap between the sexes in all morphological measurements. The element with the least amount of overlap was head-and-bill length. Discriminant functions utilising head-and-bill length that correctly predict the sex of juvenile and immature birds with approximately 93% accuracy are presented. By adding total tarsus length, the sex of wild adult Lesser Flamingos is correctly predicted with approximately 98% accuracy. The same discriminant function developed for wild adult birds predicted the sex of 19 captive adult Lesser Flamingos of known sex with 100% accuracy.     

Ontogeny of robusticity of craniofacial traits in modern humans: A study of South American populations

To date, differences in craniofacial robusticity among modern and fossil humans have been primarily addressed by analyzing adult individuals; thus, the developmental basis of such differentiation remains poorly understood. This article aims to analyze the ontogenetic development of craniofacial robusticity in human populations from South America. Geometric morphometric methods were used to describe cranial traits in lateral view by using landmarks and semilandmarks. We compare the patterns of variation among populations obtained with subadults and adults to determine whether population‐specific differences are evident at early postnatal ontogeny, compare ontogenetic allometric trajectories to ascertain whether changes in the ontogeny of shape contribute to the differentiation of adult morphologies, and estimate the amount of size change that occurs during growth along each population‐specific trajectory. The results obtained indicate that the pattern of interpopulation variation in shape and size is already established at the age of 5 years, meaning that processes acting early during ontogeny contribute to the adult variation. The ontogenetic allometric trajectories are not parallel among all samples, suggesting the divergence in the size‐related shape changes. Finally, the extension of ontogenetic trajectories also seems to contribute to shape variation observed among adults. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Myogenin regulates a distinct genetic program in adult muscle stem cells

In contrast to the detailed understanding we have for the regulation of skeletal muscle gene expression in embryos, similar insights into postnatal muscle growth and regeneration are largely inferential or do not directly address gene regulatory mechanisms. Muscle stem cells (satellite cells) are chiefly responsible for providing new muscle during postnatal and adult life. The purpose of this study was to determine the role that the myogenic basic helix-loop-helix regulatory factor myogenin has in postnatal muscle growth and adult muscle stem cell gene expression. We found that myogenin is absolutely required for skeletal muscle development and survival until birth, but it is dispensable for postnatal life. However, Myog deletion after birth led to reduced body size implying a role for myogenin in regulating body homeostasis. Despite a lack of skeletal muscle defects in Myog-deleted mice during postnatal life and the efficient differentiation of cultured Myog-deleted adult muscle stem cells, the loss of myogenin profoundly altered the pattern of gene expression in cultured muscle stem cells and adult skeletal muscle. Remarkably, these changes in gene expression were distinct from those found in Myog-null embryonic skeletal muscle, indicating that myogenin has separate functions during postnatal life.     

Femoral neck structure and function in early hominins

All early (Pliocene–Early Pleistocene) hominins exhibit some differences in proximal femoral morphology from modern humans, including a long femoral neck and a low neck‐shaft angle. In addition, australopiths (Au. afarensis, Au. africanus, Au. boisei, Paranthropus boisei), but not early Homo, have an “anteroposteriorly compressed” femoral neck and a small femoral head relative to femoral shaft breadth. Superoinferior asymmetry of cortical bone in the femoral neck has been claimed to be human‐like in australopiths. In this study, we measured superior and inferior cortical thicknesses at the middle and base of the femoral neck using computed tomography in six Au. africanus and two P. robustus specimens. Cortical asymmetry in the fossils is closer overall to that of modern humans than to apes, although many values are intermediate between humans and apes, or even more ape‐like in the midneck. Comparisons of external femoral neck and head dimensions were carried out for a more comprehensive sample of South and East African australopiths (n = 17) and two early Homo specimens. These show that compared with modern humans, femoral neck superoinferior, but not anteroposterior breadth, is larger relative to femoral head breadth in australopiths, but not in early Homo. Both internal and external characteristics of the australopith femoral neck indicate adaptation to relatively increased superoinferior bending loads, compared with both modern humans and early Homo. These observations, and a relatively small femoral head, are consistent with a slightly altered gait pattern in australopiths, involving more lateral deviation of the body center of mass over the stance limb. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Intrapopulational body size variation and cranial capacity variation in middle pleistocene humans: The Sima de los Huesos sample (Sierra de Atapuerca,Spain)

A sexual dimorphism more marked than in living humans has been claimed for European Middle Pleistocene humans, Neandertals and prehistoric modern humans. In this paper, body size and cranial capacity variation are studied in the Sima de los Huesos Middle Pleistocene sample. This is the largest sample of non-modern humans found to date from one single site, and with all skeletal elements represented. Since the techniques available to estimate the degree of sexual dimorphism in small palaeontological samples are all unsatisfactory, we have used the bootstraping method to asses the magnitude of the variation in the Sima de los Huesos sample compared to modern human intrapopulational variation. We analyze size variation without attempting to sex the specimens a priori. Anatomical regions investigated are scapular glenoid fossa; acetabulum; humeral proximal and distal epiphyses; ulnar proximal epiphysis; radial neck; proximal femur; humeral, femoral, ulnar and tibial shaft; lumbosacral joint; patella; calcaneum; and talar trochlea. In the Sima de los Huesos sample only the humeral midshaft perimeter shows an unusual high variation (only when it is expressed by the maximum ratio, not by the coefficient of variation). In spite of that the cranial capacity range at Sima de los Huesos almost spans the rest of the European and African Middle Pleistocene range. The maximum ratio is in the central part of the distribution of modern human samples. Thus, the hypothesis of a greater sexual dimorphism in Middle Pleistocene populations than in modern populations is not supported by either cranial or postcranial evidence from Sima de los Huesos. Am J Phys Anthropol 106:19–33, 1998. © 1998 Wiley-Liss, Inc.     

Variations in the anterior patellar groove of the human femur

An analysis of the anterior patellar groove of the human femur shows considerable variation in its medial and lateral spects. The groove itself, measured by the angle it encloses, shows considerably less variation than its individual components. The suggested functional relationship between bicondylar angle and lateral elevation of the patellar groove does not obtain for this sample.