Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading?

Human hip joint anatomy differs substantially from that in other primates. Humans modulate pelvic tilt during walking with a highly developed abductor apparatus, but other primates (such as chimpanzees) clearly lack such an apparatus (they exhibit a Trendelenburg gait during bipedal progression). Because the primate femoral neck is cantilevered whenever it supports body mass, it must be consistently subjected to substantial bending at the neck/shaft interface during stance phase in quadrupedal or bipedal locomotion. It has been argued, however, that the powerful abduction during the single support phase in humans results in almost entirely compressive stress on the human femoral neck. We examined collagen fiber orientation in human and chimpanzee femoral neck cortices using circularly polarized light, which has been shown to be a strong correlate of bone loading patterns. Chimpanzee superior femoral neck cortex was shown to be largely nonbirefringent (dark), but the inferior cortex was strongly birefringent. Human femoral necks showed strong birefringence both superiorly and inferiorly. These results are consistent with loading patterns suggested from anatomical structure, and provide corroborative evidence of bone's ability to preferentially orient collagen fibers during extracellular matrix deposition.

Bone mineral content and density in the humerus of adult myostatin-deficient mice.

Myostatin (GDF-8), a member of the transforming growth factor-b superfamily of secreted growth and differentiation factors, is a negative regulator of skeletal muscle growth. We investigated the effects of increased muscle mass on bone morphology by examining bone mineral content and density in the humeri of myostatin-deficient mice. We compared the humeri of 11 mixed-gender, adult mice homozygous for the disrupted myostatin sequence with those from 11 mixed-gender, adult wild-type mice. Body mass, deltoid mass, and triceps mass were recorded from each animal and densitometric and geometric parameters were collected from the humerus using peripheral quantitative computed tomography (pQCT). Cross-sectional slices were scanned at four different positions along the humerus corresponding to 15%, 40%, 60%, and 85% of total humerus length. Results show that the myostatin- deficient mice weigh more than controls and have significantly larger triceps and deltoid muscles. The myostatin-deficient animals also have significantly (P < 0.05) higher trabecular area and trabecular bone mineral content (BMC) in the proximal humerus (15% length) and significantly (P < 0.01) higher cortical BMC, cortical area, and periosteal circumference in the region of the deltoid crest (40% length). The myostatin knockouts otherwise do not differ from controls in cortical BMC. Moreover, experimental and control mice do not differ significantly from one another in cortical bone mineral density (BMD) at any of the sites examined. These results suggest that the effects of increased muscle mass on the mouse humerus are localized to regions where muscles attach; furthermore, these effects include increased mineral content of both trabecular and cortical bone.

Branching, segmentation and the metapterygial axis: pattern versus process in the vertebrate limb.

Explanations of the patterns of vertebrate fin and limb evolution are improving as specific hypotheses based on molecular and developmental data are proposed and tested. Comparative analyses of gene expression patterns and functions in developing limbs, and morphological patterns in embryonic, adult and fossil limbs point to digit specification as a key developmental innovation associated with the origin of tetrapods. Digit development during the fin-to-limb transition involved sustained proximodistal outgrowth and a new phase of Hox gene expression in the distal fin bud. These patterning changes in the distal limb have been explained by the linked concepts of the metapterygial axis and the digital arch. These have been proposed to account for the generation of limb pattern by sequential branching and segmentation of precartilagenous elements along the proximodistal axis of the limb. While these ideas have been very fruitful, they have become increasingly difficult to reconcile with experimental and comparative studies of fin and limb development. Here we argue that limb development does not involve a branching mechanism, and reassess the concept of a metapterygial axis in limb development and evolution.

Adaptationism and the anthropoid postcranium: selection does not govern the length of the radial neck.

The length of the radial neck has been assumed to vary in living and extinct primates in accordance with its role as a moment arm during flexion by the m. biceps brachii. We here use a simple developmental approach to investigate whether or not this trait does, in fact, vary in such a manner. We find, instead, that virtually all variation in radial neck length is explicable as a simple correlate of overall body size, and that there is no evidence to conclude that selection has separately modified radial neck length in response to differing locomotor patterns. Further implications for the interpretation of mammalian skeletal morphology are briefly discussed.

Femoral morphology and cross-sectional geometry of adult myostatin-deficient mice.

GDF-8, also known as myostatin, is a member of the transforming growth factor-beta (TGF-beta) superfamily of secreted growth and differentiation factors that is expressed in vertebrate skeletal muscle. Myostatin functions as a negative regulator of skeletal muscle growth and myostatin null mice show a doubling of muscle mass compared with normal mice. We examined femoral morphology of adult myostatin-deficient mice to assess the effects of muscle fiber hypertrophy and hyperplasia on bone shape and cross-sectional geometry. Femora of age- and weight-matched adult mice homozygous for the disrupted myostatin sequence were compared with those of wild-type controls (n = 8 per group). Results show that, as was the case in previous studies, myostatin null mice have hindlimb muscle masses that are approximately double those of controls. Myostatin-deficient mice exhibit third trochanters that are significantly larger than those of controls, whereas the femoral midshafts of the control and experimental mice do not differ significantly from one another in cortical area, bending moment of inertia, and polar moment of inertia. Our findings indicate that the increased muscle mass of myostatin-deficient mice primarily affects sites of muscle insertion, but does not induce additional cortical bone deposition in the diaphysis relative to controls. We therefore conclude that the expanded third trochanters of myostatin-deficient subjects result from tendon and Sharpey fiber expansion associated with muscle growth rather than cortical bone deposition in response to increased levels of mechanical stress.

Morphological analysis of the mammalian postcranium: a developmental perspective.

The past two decades have greatly improved our knowledge of vertebrate skeletal morphogenesis. It is now clear that bony morphology lacks individual descriptive specification and instead results from an interplay between positional information assigned during early limb bud deployment and its "execution" by highly conserved cellular response programs of derived connective tissue cells (e.g., chondroblasts and osteoblasts). Selection must therefore act on positional information and its apportionment, rather than on more individuated aspects of presumptive adult morphology. We suggest a trait classification system that can help integrate these findings in both functional and phylogenetic examinations of fossil mammals and provide examples from the human fossil record.

AL 288-1--Lucy or Lucifer: gender confusion in the Pliocene.

Häusler & Schmid (1995) challenged the long held opinion that AL 288-1 (Australopithecus afarensis), popularly known as "Lucy", was female. They concluded that AL 288-1 was most probably male ("Lucifer") and, by extension, the hypodigm for A. afarensis consists of two species which differ from one another in body size; in their opinion, AL 288-1 was most probably a male of the smaller of the two species. Häusler & Schmid based their conclusion on an obstetric analysis of AL 288-1 and Sts 14 (A. africanus) and on a comparison of the two australopithecine pelves with those of modern humans. This study evaluates the pelvic anatomy and probable sex of AL 288-1 by both assessing the obstetric adequacy of its pelvis and critically reviewing Häusler & Schmid's (1995, 1997) analyses of australopithecine pelvic dimorphism and relative body size of AL 288-1. Three results are shown. First, using Häusler & Schmid's own data, AL-288-1's and Sts 14's pelves are seen not to be dimorphic with respect to each other, as are human males and females, but they are in fact comparable in both size and shape. Second, AL 288-1's pelvis would have been obstetrically adequate, even with an inferred newborn brain size (as suggested by Häusler & Schmid) for A. afarensis that is likely overestimated. Third, AL 288-1 is shown to be one of the smallest adult individuals in A. afarensis. We conclude that AL 288-1 and Sts 14 were the same sex, and that the name "Lucy" correctly identifies AL 288-1's gender as female.

Cortical bone distribution in the femoral neck of hominoids: implications for the locomotion of Australopithecus afarensis.

Contiguous high resolution computed tomography images were obtained at a 1.5 mm slice thickness perpendicular to the neck axis from the base of the femoral head to the trochanteric line in a sample of 10 specimens each of Homo sapiens, Pan troglodytes, and Gorilla gorilla, plus five specimens of Pan paniscus. Superior, inferior, anterior, and posterior cortical thicknesses were automatically measured directly from these digital images. Throughout the femoral neck H. sapiens displays thin superior cortical bone and inferior cortical bone that thickens distally. In marked contrast, cortical bone in the femoral neck of African apes is more uniformly thick in all directions, with even greater thickening of the superior cortical bone distally. Because the femoral neck acts as a cantilevered beam, its anchorage at the neck-shaft junction is subjected to the highest bending stresses and is the most biomechanically relevant region to inspect for response to strain. As evinced by A.L. 128-1, A.L. 211-1 and MAK-VP-1/1, Australopithecus afarensis is indistinguishable from H. sapiens, but markedly different from African apes in cortical bone distribution at the femoral neck-shaft junction. Cortical distribution in the African ape indicates much greater variation in loading conditions consistent with their more varied locomotor repertoire. Cortical distribution in hominids is a response to the more stereotypic loading pattern imposed by habitual bipedality, and thin superior cortex in A. afarensis confirms the absence of a significant arboreal component in its locomotor repertoire.

Comparison of diaphyseal growth between the Libben Population and the Hamann-Todd chimpanzee sample.

The differences in limb lengths and proportions between humans and chimpanzees are widely known. Humans have relatively shorter forelimbs and longer hind limbs than chimpanzees. Humans have a longer period of long bone formation than chimpanzees. Recent advances in estimating age-at-death in chimpanzees from their dentition have allowed us to reexamine long bone growth in chimpanzees using their skeletal remains and compare it with similar data for humans. A chronological normalization procedure allowing direct interspecific comparison of long bone growth is presented. The preadult chimpanzee sample (n = 43) is from the Hamann-Todd Osteological Collection from the Cleveland Museum of Natural History. All human specimens (n = 202) are from the late Woodland Libben Population currently housed at Kent State University. Relying on these cross-sectional data, we conclude that both species elongate their femora at similar absolute (length per unit time) but different relative (length relative to normalized dental age) rates. The species differ in the absolute growth rate of the humerus but share a common normalized rate of growth. Forelimb segment proportion differences between species are due to differential elongation rates of the segments. Hind limb diaphyseal proportions are the same in both species, which suggests that changes in segment length are proportional. Therefore, alternative developmental mechanisms exist in these closely related species which can produce changes in limb length.

Independent test of the fourth rib aging technique.

The sternal surface of the 4th rib has been suggested as a useful predictor of adult age-at-death (Iscan et al.: Journal of Forensic Sciences 29:1094-1104, 1984; American Journal of Physical Anthropology 65:147-156, 1984). We tested its ability to do so in two tests. In the first, we developed a method of seriation and target age assignment for the 4th rib so that inaccuracy and bias of the method could be assessed by decade. We found that the 4th rib shows characteristic changes in morphology with age and can be included in multifactorial age estimates. In the second test, we applied the phase method developed by Iscan et al. (Journal of Forensic Sciences 29:1094-1104, 1984). The results of our three judges were generally similar to those reported by Iscan and Loth (Journal of Forensic Sciences 31:122-132, 1986). Measures of race differences in 4th rib morphology were included in both tests. Americans of African descent (black) showed a non-significant trend for the rib changes to be delayed compared to Americans of European descent (white). This is in contrast to the work of Iscan et al., which predicted that blacks would show a tendency toward accelerated rib changes compared to whites, especially after the early 30s (phases 5-7) (Iscan et al.: Journal of Forensic Sciences 32(2):452-466, 1987).

Test of the multifactorial aging method using skeletons with known ages-at-death from the Grant Collection.

The multifactorial aging method has been shown to be a highly reliable method of skeletal aging because it incorporates age information from as many age indicators as are available for each skeleton (Lovejoy et al.; Am. J. Phys. Anthropol. 68:1-14, 1985). The present study was a blind test to assess its accuracy on a skeletal sample composed of 55 individuals with verified death certificates (Grant Collection, University of Toronto). Three authors (C.O.L., M.E.B., and K.F.R.), with no access to the death certificate ages, independently seriated and aged the sample using three to four criteria: auricular surface, pubic symphysis, and radiographs of the proximal femur and clavicle. Summary ages were then calculated for each individual in the sample. The authors' independent summary age estimates showed strong correlations with one another (r = 0.84-0.89). Multifactorial age estimates correlated better with real age than did those from any single indicator used. The mean error (averaging 8.7 years) for summary age was at least 1 year less than that for any single indicator. Average bias ranged from -0.7 (underage) to 1.4 (overage) years. These results indicate that utilization of several age indicators, weighted according to their reliability, helps control for variation in the changes that occur with age in any single morphological indicator. This method may therefore be considered one of the most accurate available for the determination of skeletal age-at-death, particularly for paleodemographic analysis.

Further evidence on relative dental maturation and somatic developmental rate in hominoids.

New data on hominoid dental development are presented. Individual bivariate pairings of all mandibular teeth were made for African apes and humans. Data were analyzed with a full linear regression model. No statistically significant differences were found among apes, although a consistent pattern of earlier incisal development was observed in Pan relative to Gorilla. This is concordant with an earlier fusion of the premaxillary:maxillary suture in Pan. Only one tooth pair differed significantly by sex among apes. Two biologically distinct human samples (Libben and Hamann-Todd), although assessed differently (extraction and radiography) yielded virtually identical results. Humans differ from apes only by earlier relative calcification of their anterior teeth. This can be viewed as a consequence of reduced facial prognathism and a shift in hominid canine function.

Reliability of age at death in the Hamann-Todd collection: validity of subselection procedures used in blind tests of the summary age technique.

The blind test procedures used by Lovejoy et al., (Am. J. Phys. Anthropol. 68:1-14, 1985a) have been criticized because they used the Hamann-Todd collection as their known-age population. It has been suggested that variation within this sample was reduced by selection procedures designed to ensure accuracy of age at death. Powerful statistical tests for differences in dispersion of ages for pubic symphyseal stages were applied to comparisons between their core sample (N = 238) and those of a large autopsy-room collection used to develop the Suchey-Brooks System (N = 530). The variances in ages of the selected Hamann-Todd Sample are not reduced. The careful subselection of specimens has resulted in a valid statistical core sample for use in the development of aging methodologies.

Metatarsophalangeal joints of Australopithecus afarensis.

Metatarsophalangeal joints from African pongids, modern humans, and Australopithecus afarensis are compared to investigate the anatomical and mechanical changes that accompanied the transition to terrestrial bipedality. Features analyzed include the shape and orientation of the metatarsal heads, excursion of the metatarsophalangeal joints, and orientation of the basal articular surface of the proximal phalanges. These features unequivocally segregate quadrupedal pongids and bipedal hominids and demonstrate a clear adaptation to terrestrial bipedality in the Hadar pedal skeleton.

Hallucal tarsometatarsal joint in Australopithecus afarensis.

Hallucal tarsometatarsal joints from African pongids, modern humans, and Australopithecus afarensis are compared to investigate the anatomical and mechanical changes that accompanied the transition to terrestrial bipedality. Features analyzed include the articular orientation of the medial cuneiform, curvature of the distal articular surface of the medial cuneiform, and the articular configuration of the hallucal metatarsal proximal joint surface. Morphological characteristics of the hallucal tarsometatarsal joint unequivocally segregate quadrupedal pongids and bipedal hominids.

The radiographic preauricular groove: its non-relationship to past parity.

Deep preauricular sulci were identified on abdominal radiographs in 29 of 190 (15%) adult females and in none of 110 adult males. To assess the value of the deep preauricular sulcus as an index of past pregnancy, we examined gravidity and parity records of 190 women, using standard films that included the sacroiliac region. Deep, radiographic preauricular grooves were identified in 4 of 41 (10%) nulliparous women and in 25 of 149 (17%) women with positive pregnancy histories. We also examined radiographs obtained before and after pregnancy in six primigravidas. No evidence of radiographic changes in the preauricular grooves was seen in any of the six women. We conclude that the presence of a deep, radiographic preauricular sulcus is not necessarily an indication of past pregnancy.

The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality.

Calcanei from African apes, modern humans, and Australopithecus afarensis are compared to investigate the anatomical and mechanical changes that occurred in this bone as a result of the transition to terrestrial bipedality. Features analyzed include the cross-sectional area and volume of the calcaneal tuber, the geometry and orientation of the articular surfaces, and the surface topography of the calcaneal corpus. Calcaneal morphology is unequivocal in its partitioning of quadrupedal pongids and bipedal hominids.

Talocrural joint in African hominoids: implications for Australopithecus afarensis.

Talocrural joints of the African apes, modern humans, and A.L.288-1 are compared in order to investigate ankle function in the Hadar hominids. Comparisons between the hominids and African pongids clearly illustrate the anatomical and mechanical changes that occurred in this joint as a consequence of the evolutionary transition to habitual bipedality. Features which are considered include the obliquity of the distal tibial articular surface, the shape of the talar trochlea, and the location and functional implications of the talocrural axis. In every functionally significant feature examined the A.L.288-1 talocrural joint is fully bipedal. Moreover, the Hadar ankle complex also shows the functional constraints which are necessarily imposed by the adaptation to habitual bipedalism.