Functional-adaptive anatomy of the axial skeleton of some extant marsupials and the paleobiology of the paleocene marsupials Mayulestes ferox and Pucadelphys andinus

In this study, the axial skeletons of two Early Paleocene marsupials, Mayulestes ferox and Pucadelphys andinus, were analyzed functionally and compared to that of six South American and three Australian species of extant marsupials. In the case of the South American opossums, myological data of the epaxial musculature were collected and analyzed and osteological-myological associations were related to locomotor behavior. Various features of the vertebral column that relate to diet or to locomotor or postural patterns were pointed out. These features include: the craniocaudal development of the neural process of the axis; the position of the anticlinal vertebra; the morphology of the neural processes of the thoracolumbar vertebrae (orientation, length, and craniocaudal width); the length, orientation, and curvature of the transverse processes of the lumbar vertebrae; and the length and robustness of the caudal vertebrae. In both fossil forms the vertebral column is mobile and allows a great range of flexion and extension of the spine, more so than in most of the living didelphids. It is emphasized here that the analysis of the axial skeleton complements and improves the conclusions provided by the forelimb and hindlimb analyses. It is proposed that Mayulestes and Pucadelphys represent an ancestral morphotype suggesting that the generalized type of locomotion of Paleocene marsupials was partly terrestrial with some climbing ability.     

Evaluation of "unique" aspects of human vertebral bodies and pedicles with a consideration of Australopithecus africanus

Recent functional studies of human vertebrae have revealed that loads borne by the axial skeleton during bipedal postures and locomotion pass through the pedicles and posterior elements as well as through the bodies and discs. Accordingly, particular morphological attributes of these vertebral elements have been linked exclusively with bipedalism. In order to test the validity of current form-function associations in human vertebral anatomy, this study considers the morphology of human thoracolumbar vertebral bodies and pedicles in the context of a wide comparative primate sample. The last lumbar vertebra of STS 14 (Australopithecus africanus) is also included in the analysis. Results indicate that certain features of human vertebrae previously thought to reflect bipedalism are characteristic of several nonhuman primates, including those whose posture is habitually pronograde. These features include the decrease in vertebral body surface area and the increase in cross-sectional area of the pedicle between the penultimate and last lumbar vertebra. In addition, although humans have relatively large and wide last lumbar pedicles, the enlargement and widening of the pedicle between the penultimate and last lumbar vertebra is not unique to humans. On the other hand, human vertebrae do exhibit several unique adaptations to bipedal posture and locomotion: (1) the vertebral body surface areas of the lower lumbar vertebrae and the cross-sectional areas of the last lumbar pedicles are large relative to body size, and (2) the last lumbar pedicles are wider relative to length and to body size than are those of nonhuman primates. The last lumbar vertebra of STS 14 does not exhibit any of these human-like vertebral features—its pedicles and body surface areas are relatively small, and its pedicles are not relatively wide, but relatively short.     

Placement of the diaphragmatic vertebra in catarrhines: implications for the evolution of dorsostability in hominoids and bipedalism in hominins

A fundamental adaptation to orthograde posture and locomotion amongst living hominoid primates is a numerically reduced lumbar column, which acts to stiffen the lower back and reduce injuries to the intervertebral discs. A related and functionally complementary strategy of spinal stability is a caudal position of the diaphragmatic vertebra relative to the primitive condition found in nonhominoid primates and most other mammals. The diaphragmatic vertebra marks the transition in vertebral articular facet (zygapophysis) orientation, which either resists (prediaphragmatic) or allows (postdiaphragmatic) trunk movement in the sagittal plane (i.e., flexion and extension). Unlike most mammals, which have dorsomobile spines (long lumbar columns and cranially placed diaphragmatic vertebrae) for running and leaping, hominoids possess dorsostable spines (short lumbar columns and caudally placed diaphragmatic vertebrae) adapted to orthogrady and antipronogrady. In contrast to humans and other extant hominoids, all known early hominin partial vertebral columns demonstrate cranial displacement of the diaphragmatic vertebra. To address this difference, variation in diaphragmatic placement is assessed in a large sample of catarrhine primates. I show that while hominoids are characterized by modal common placement of diaphragmatic and last rib-bearing vertebrae in general, interspecific differences in intraspecific patterns of variation exist. In particular, humans and chimpanzees show nearly identical patterns of diaphragmatic placement. A scenario of hominin evolution is proposed in which early hominins evolved cranial displacement from the ancestral hominid condition of common placement to achieve effective lumbar lordosis during the evolution of bipedal locomotion.     

Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus

An attempt to determine the locomotor activities of Mayulestes ferox (Borhyaenoidea) and Pucadelphys andinus (Didelphoidea) from the early Paleocene site of Tiupampa (Bolivia) is presented. The functional anatomy of the forelimbs of these South American marsupials is compared to that of some living didelphids: Caluromys philander, Micoureus demerarae, Marmosa murina, Didelphis marsupialis, Monodelphis brevicaudata and Metachirus nudicaudatus. Deductions from bone morphology to myology and locomotor behavior in the fossils are inferred from the comparisons with living forms. Some features of the postcranial skeleton, indicative of arboreal adaptations, are found in the extinct marsupials: anteriorly projected acromion, hemispherical head of the humerus, extended humeral lateral epicondylar ridge, medially protruding humeral entepicondyle, proximal ulnar posterior convexity, and deep flexor fossa on the medial side of the ulna. But other features are related to a more terrestrial pattern: the well-developed tubercles of the humeral head, the elongated olecranon process of the ulna, and the oval shape of the radial head. Mayulestes had clear arboreal abilities, but, as a predaceous mammal, probably hunted on the ground. Pucadelphys was less specialized, close to the living Monodelphis, a terrestrial insectivorous form with some skeletal features related to arboreal locomotion that are probably plesiomorphic for marsupials.     

Distal Humeral Morphology Indicates Locomotory Divergence in Extinct Giant Kangaroos

Previous studies of the morphology of the humerus in kangaroos showed that the shape of the proximal humerus could distinguish between arboreal and terrestrial taxa among living mammals, and that the extinct “giant” kangaroos (members of the extinct subfamily Sthenurinae and the extinct macropodine genus Protemnodon) had divergent humeral anatomies from extant kangaroos. Here, we use 2D geometric morphometrics to capture the shape of the distal humerus in a range of extant and extinct marsupials and obtain similar results: sthenurines have humeral morphologies more similar to arboreal mammals, while large Protemnodon species (P. brehus and P. anak) have humeral morphologies more similar to terrestrial quadrupedal mammals. Our results provide further evidence for prior hypotheses: that sthenurines did not employ a locomotor mode that involved loading the forelimbs (likely employing bipedal striding as an alternative to quadrupedal or pentapedal locomotion at slow gaits), and that large Protemnodon species were more reliant on quadrupedal locomotion than their extant relatives. This greater diversity of locomotor modes among large Pleistocene kangaroos echoes studies that show a greater diversity in other aspects of ecology, such as diet and habitat occupancy.

     

Locomotor variation and bending regimes of capuchin limb bones

Primates are very versatile in their modes of progression, yet laboratory studies typically capture only a small segment of this variation. In vivo bone strain studies in particular have been commonly constrained to linear locomotion on flat substrates, conveying the potentially biased impression of stereotypic long bone loading patterns. We here present substrate reaction forces (SRF) and limb postures for capuchin monkeys moving on a flat substrate (“terrestrial”), on an elevated pole (“arboreal”), and performing turns. The angle between the SRF vector and longitudinal axes of the forearm or leg is taken as a proxy for the bending moment experienced by these limb segments. In both frontal and sagittal planes, SRF vectors and distal limb segments are not aligned, but form discrepant angles; that is, forces act on lever arms and exert bending moments. The positions of the SRF vectors suggest bending around oblique axes of these limb segments. Overall, the leg is exposed to greater moments than the forearm. Simulated arboreal locomotion and turns introduce variation in the discrepancy angles, thus confirming that expanding the range of locomotor behaviors studied will reveal variation in long bone loading patterns that is likely characteristic of natural locomotor repertoires. “Arboreal” locomotion, even on a linear noncompliant branch, is characterized by greater variability of force directions and discrepancy angles than “terrestrial” locomotion (significant for the forearm only), partially confirming the notion that life in trees is associated with greater variation in long bone loading. Directional changes broaden the range of external bending moments even further. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Simulation of the behaviour of the L1 vertebra for different material properties and loading conditions

Three-dimensional finite element models of the thoracolumbar junction (T12–L2) and isolated L1 vertebra were developed to investigate the role of material properties and loading conditions on vertebral stresses and strains to predict fracture risk. The geometry of the vertebrae was obtained from computed tomography images. The isolated vertebra model included an L1 vertebra loaded through polymethylmethacrylate plates located at the top and bottom of the vertebra, and the segment model included T12 to L2 vertebrae and seven ligaments, fibrous intervertebral discs and facet joints. Each model was examined with both homogeneous and spatially varying bone tissue properties. Stresses and strains were compared for uniform compression and flexion. Including material heterogeneity remarkably reduced the stiffness of the isolated L1 vertebra and increased the magnitudes of the minimum principal strains and stresses in the mid-transverse section. The stress and strain distributions further changed when physiological loading was applied to the L1 vertebra. In the segment models, including heterogeneous material properties increased the magnitude of the minimum principal strain by 158% in the centre of the mid-transverse section. Overall, the inclusion of heterogeneity and physiological loading increased the magnitude of the strains up to 346% in flexion and 273% in compression.     

The angular distribution of vertebral trabeculae in modern humans,chimpanzees and the Kebara 2 Neanderthal

Bone is known to remodel to optimize its structure according to its mechanical environment. In particular trabecular arcades are thought to align with the orientations of components of principal strain. This paper presents the application of a novel method for quantifying trabecular orientation to test the hypothesis that hominoid posture and locomotion are reflected in trabecular architecture. Lateral radiographs were taken of vertebrae from the entire thoracolumbar spines of eight modern humans, seven Pan troglodytes and one Neanderthal. The radiographs were digitized and a square region of interest located at the centre of each vertebral body selected. Fourier transforms of the regions of interest were performed and the relative magnitude of the transform in each of 16 angular segments calculated. The simple indices of external vertebral body morphology, wedge angle and aspect ratio, were also calculated from the radiographs.All three species exhibit the same pattern, with the majority of trabeculae oriented either axially or dorsoventrally. This suggests that vertebral mechanical loading is similar in chimpanzees and humans, despite their apparent postural and locomotor differences. Significant differences between the magnitudes of the Fourier transform in the 78.75 degrees and 135 degrees orientations of chimpanzee and human vertebrae were observed in all but the upper thoracic spine. As the magnitudes at these orientations in the Neanderthal correspond more closely to that in the human and the orientational features were unrelated to the external vertebral morphology, the difference between the two magnitudes may well prove to be a useful parameter in future phylogenetic analysis. Modern human spines were found to show a greater variation in the proportions of axial and dorsoventral trabeculae with spinal level than chimpanzees, with the greatest differences observed in the upper thoracic spine and thoracolumbar junction, suggesting an association with postural spinal curves.     

Numerical variation of the presacral vertebral column in three population groups in North America

A total of 1,239 skeletons from among Mongoloid, Caucasoid and Negroid population groups in North America was examined for variations in the number of presacral vertebrae. The overall incidence of variation was 11%; 6% with 23 and 5% with 25 presacral vertebrae. Differences in total variation among the three groups were not significant, but differences in the incidence of 23 and 25 presacral vertebrae among the groups were highly significant. Numerical vertebral variation occurred in 11% of both sexes, but with males having a higher frequency of 25 presacral vertebrae and females having a higher frequency of 23 presacral vertebrae. The incidence of the specific variation of 23 or 25 presacral vertebrae was not significantly different among the males of the three groups studied, whereas 23 presacral vertebrae were found significantly more often in the Negroid females. Numerical variation of vertebrae was not associated with age. The data strongly support the conclusion that the total frequency of variation in the number of presacral vertebrae is a specific characteristic of any particular population group and that there is a tendency in all population groups toward an increase in number in males and a decrease in number in females.     

Vertebrae numbers of the early hominid lumbar spine

General doctrine holds that early hominids possessed a long lumbar spine with six segments. This is mainly based on Robinson's (1972) interpretation of a single partial Australopithecus africanus skeleton, Sts 14, from Sterkfontein, South Africa. As its sixth last presacral vertebra exhibits both thoracic and lumbar characteristics, current definitions of lumbar vertebrae and lumbar ribs are discussed in the present study. A re-analysis of its entire preserved vertebral column and comparison with Stw 431, another partial A. africanus skeleton from Sterkfontein, and the Homo erectus skeleton KNM-WT 15000 from Nariokotome, Kenya, did not provide strong evidence for the presence of six lumbar vertebrae in either of these early hominids. Thus, in Sts 14 the sixth last presacral vertebra has on one side a movable rib. In Stw 431, the corresponding vertebra shows indications for a rib facet. In KNM-WT, 15000 the same element is very fragmentary, but the neighbouring vertebrae do not support the view that it is L1. Although in all three fossils the transitional vertebra at which the articular facets change orientation seems to be at Th11, this is equal to a large percentage of modern humans. Indeed, a modal number of five lumbar vertebrae, as in modern humans, is more compatible with evolutionary principles. For example, six lumbar vertebrae would require repetitive shortening and lengthening not only of the lumbar, but also of the entire precaudal spine. Furthermore, six lumbar vertebrae are claimed to be biomechanically advantageous for early hominid bipedalism, yet an explanation is lacking as to why the lumbar region should have shortened in later humans. All this raises doubts about previous conclusions for the presence of six lumbar vertebrae in early hominids. The most parsimonious explanation is that they did not differ from modern humans in the segmentation of the vertebral column.     

A Bio-Inspired Hopping Kangaroo Robot with an Active Tail

Inspired by kangaroo＇s locomotion, we report on developing a kangaroo-style hopping robot. Unlike bipeds, quadrupeds, or hexapods which altemate the legs for forward locomotion, the kangaroo uses both legs synchronously and generates the forward locomotion by continuous hopping behavior, and the tail actively balances the unwanted angular momentum generated by the leg motion. In this work, we generate the Center of Mass （CoM） locomotion of the robot based on the reduced-order Rolling Spring Loaded Inverted Pendulum （R-SLIP） model, for matching the dynamic behavior of the empirical robot legs. In order to compensate the possible body pitch variation, the robot is equipped with an active tail for pitch variation compensation, emulating the balance mechanism of a kangaroo. The robot is empirically built, and various design issues and strategies are addressed. Finally, the experimental evaluation is executed to validate the performance of the kangaroo-style robot with hopping locomotion.     

Locomotion in some small to medium-sized mammals: a geometric morphometric analysis of the penultimate lumbar vertebra,pelvis and hindlimbs

We assessed the influence of a variety of aspects of locomotion and ecology including gait and locomotor types, maximal running speed, home range, and body size on postcranial shape variation in small to medium-sized mammals, employing geometric morphometric analysis and phylogenetic comparative methods. The four views analyzed, i.e., dorsal view of the penultimate lumbar vertebra, lateral view of the pelvis, posterior view of the proximal femur and proximal view of the tibia, showed clear phylogenetic signal and interesting patterns of association with movement. Variation in home range size was related to some tibia shape changes, while speed was associated with lumbar vertebra, pelvis and tibia shape changes. Femur shape was not related to any locomotor variables. In both locomotor type and high-speed gait analyses, locomotor groups were distinguished in both pelvis and tibia shape analyses. These results suggest that adaptations to both typical and high-speed gaits could explain a considerable portion of the shape of those elements. In addition, lumbar vertebra and tibia showed non-significant relationships with body mass, which suggests that they might be used in morpho-functional analyses and locomotor inferences on fossil taxa, with little or no bias for body size. Lastly, we observed morpho-functional convergences among several mammalian taxa and detected some taxa that achieve similar locomotor features following different morphological paths.     

Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico

Conspecific populations inhabiting different environments may exhibit morphological differences, potentially reflecting differential local adaptation. In anuran amphibians, morphology of the pelvis and hindlimbs may often experience strong selection due to effects on locomotion. In this study, we used the cane toad Rhinella marina to test the hypothesis that populations experiencing a higher abundance of predators should suffer higher mortality rates and exhibit morphological traits associated with enhanced locomotor performance (narrower pelvis and head, longer pelvis and hindlimbs, shorter presacral vertebral column). We investigated inter-population variation in survival rate, abundance of predators, and body shape across five populations in rivers in western Mexico. We conducted (1) mark-recapture experiments to calculate survival rates, (2) linear transects with point counts to estimate abundance of predatory spiders, snakes, and birds, and (3) geometric morphometric analyses to investigate body shape variation. We found significant differences among populations in survival rates, abundance of predators, and body shape. However, these three variables were not necessarily inter-related. Increased predator abundance did not result in decreased survival rates, suggesting other causes of mortality affect these populations. While some morphological differences supported our predictions (trend for longer pelvis, shorter presacral vertebral column, and narrower head in sites with increased abundance of spiders and snakes), other aspects of morphology did not. We discuss alternative explanations for the lack of clear associations between predation, survival, and morphology.     

Head‐turning morphologies: Evolution of shape diversity in the mammalian atlas–axis complex

Mammals flex, extend, and rotate their spines as they perform behaviors critical for survival, such as foraging, consuming prey, locomoting, and interacting with conspecifics or predators. The atlas–axis complex is a mammalian innovation that allows precise head movements during these behaviors. Although morphological variation in other vertebral regions has been linked to ecological differences in mammals, less is known about morphological specialization in the cervical vertebrae, which are developmentally constrained in number but highly variable in size and shape. Here, we present the first phylogenetic comparative study of the atlas–axis complex across mammals. We used spherical harmonics to quantify 3D shape variation of the atlas and axis across a diverse sample of species, and performed phylogenetic analyses to investigate if vertebral shape is associated with body size, locomotion, and diet. We found that differences in atlas and axis shape are partly explained by phylogeny, and that mammalian subclades differ in morphological disparity. Atlas and axis shape diversity is associated with differences in body size and locomotion; large terrestrial mammals have craniocaudally elongated vertebrae, whereas smaller mammals and aquatic mammals have more compressed vertebrae. These results provide a foundation for investigating functional hypotheses underlying the evolution of neck morphologies across mammals.     

Evidence of Spondyloarthropathy in the Spine of a Phytosaur (Reptilia: Archosauriformes) from the Late Triassic of Halberstadt,Germany

Pathologies in the skeleton of phytosaurs, extinct archosauriform reptiles restricted to the Late Triassic, have only been rarely described. The only known postcranial pathologies of a phytosaur are two pairs of fused vertebrae of “Angistorhinopsis ruetimeyeri” from Halberstadt, Germany, as initially described by the paleontologist Friedrich von Huene. These pathologic vertebrae are redescribed in more detail in this study in the light of modern paleopathologic methods. Four different pathologic observations can be made in the vertebral column of this individual: 1) fusion of two thoracic vertebral bodies by new bone formation within the synovial membrane and articular capsule of the intervertebral joint; 2) fusion and conspicuous antero-posterior shortening of last presacral and first sacral vertebral bodies; 3) destruction and erosion of the anterior articular surface of the last presacral vertebra; and 4) a smooth depression on the ventral surface of the fused last presacral and first sacral vertebral bodies. Observations 1–3 can most plausibly and parsimoniously be attributed to one disease: spondyloarthropathy, an aseptic inflammatory process in which affected vertebrae show typical types of reactive new bone formation and erosion of subchondral bone. The kind of vertebral shortening present in the fused lumbosacral vertebrae suggests that the phytosaur acquired this disease in its early life. Observation 4, the smooth ventral depression in the fused lumbosacral vertebrae, is most probably not connected to the spondyloarthropathy, and can be regarded as a separate abnormality. It remains of uncertain origin, but may be the result of pressure, perhaps caused by a benign mass such as an aneurysm or cyst of unknown type. Reports of spondyloarthropathy in Paleozoic and Mesozoic reptiles are still exceptional, and our report of spondyloarthropathy in fossil material from Halberstadt is the first unequivocal occurrence of this disease in a Triassic tetrapod and in a phytosaur.     

Prezygapophyseal articular facet shape in the catarrhine thoracolumbar vertebral column

Two contrasting patterns of lumbar vertebral morphology generally characterize anthropoids. “Long‐backed” monkeys are distinguished from “short‐backed” apes [Benton: The baboon in medical research, Vol. 2 (1967:201)] with respect to several vertebral features thought to afford greater spinal flexibility in the former and spinal rigidity in the latter. Yet, discussions of spinal mobility are lacking important functional insight that can be gained by analysis of the zygapophyses, the spine's synovial joints responsible for allowing and resisting intervertebral movements. Here, prezygapophyseal articular facet (PAF) shape in the thoracolumbar spine of Papio, Hylobates, Pongo, Gorilla, and Pan is evaluated in the context of the “long‐backed” versus “short‐backed” model. A three‐dimensional geometric morphometric approach is used to examine how PAF shape changes along the thoracolumbar vertebral column of each taxon and how PAF shape varies across taxa at corresponding vertebral levels. The thoracolumbar transition in PAF shape differs between Papio and the hominoids, between Hylobates and the great apes, and to a lesser extent, among great apes. At the level of the first lumbar vertebra, the PAF shape of Papio is distinguished from that of hominoids. At the level of the second lumbar vertebra, there is variation to some extent among all taxa. These findings suggest that morphological and functional distinctions in primate vertebral anatomy may be more complex than suggested by a “long‐backed” versus “short‐backed” dichotomy. Am J Phys Anthropol 142:600–612, 2010. © 2010 Wiley‐Liss, Inc.     

Phenotypic integration of the cervical vertebrae in the Hominoidea (Primates)

Phenotypic integration and modularity represent important factors influencing evolutionary change. The mammalian cervical vertebral column is particularly interesting in regards to integration and modularity because it is highly constrained to seven elements, despite widely variable morphology. Previous research has found a common pattern of integration among quadrupedal mammals, but integration patterns also evolve in response to locomotor selective pressures like those associated with hominin bipedalism. Here, I test patterns of covariation in the cervical vertebrae of three hominoid primates (Hylobates, Pan, Homo) who engage in upright postures and locomotion. Patterns of integration in the hominoid cervical vertebrae correspond generally to those previously found in other mammals, suggesting that integration in this region is highly conserved, even among taxa that engage in novel positional behaviors. These integration patterns reflect underlying developmental as well as functional modules. The strong integration between vertebrae suggests that the functional morphology of the cervical vertebral column should be considered as a whole, rather than in individual vertebrae. Taxa that display highly derived morphologies in the cervical vertebrae are likely exploiting these integration patterns, rather than reorganizing them. Future work on vertebrates without cervical vertebral number constraints will further clarify the evolution of integration in this region.