Timothy M. Ryan

The primate semicircular canal system and locomotion.

The semicircular canal system of vertebrates helps coordinate body movements, including stabilization of gaze during locomotion. Quantitative phylogenetically informed analysis of the radius of curvature of the three semicircular canals in 91 extant and recently extinct primate species and 119 other mammalian taxa provide support for the hypothesis that canal size varies in relation to the jerkiness of head motion during locomotion. Primate and other mammalian species studied here that are agile and have fast, jerky locomotion have significantly larger canals relative to body mass than those that move more cautiously.

Oligocene mammals from Ethiopia and faunal exchange between Afro-Arabia and Eurasia

Afro-Arabian mammalian communities underwent a marked transition near the Oligocene/Miocene boundary at approximately 24 million years (Myr) ago. Although it is well documented that the endemic paenungulate taxa were replaced by migrants from the Northern Hemisphere, the timing and evolutionary dynamics of this transition have long been a mystery because faunas from about 32 to 24 Myr ago are largely unknown. Here we report a late Oligocene fossil assemblage from Ethiopia, which constrains the migration to postdate 27 Myr ago, and yields new insight into the indigenous faunal dynamics that preceded this event. The fauna is composed of large paenungulate herbivores and reveals not only which earlier taxa persisted into the late Oligocene epoch but also demonstrates that one group, the Proboscidea, underwent a marked diversification. When Eurasian immigrants entered Afro-Arabia, a pattern of winners and losers among the endemics emerged: less diverse taxa such as arsinoitheres became extinct, moderately species-rich groups such as hyracoids continued into the Miocene with reduced diversity, whereas the proboscideans successfully carried their adaptive radiation out of Afro-Arabia and across the world.

Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading

Significance Compared with other primates and earlier human species, contemporary humans possess relatively lightly built skeletons. Previous studies suggest that skeletal gracility results from a lack of physical activity because of increased reliance on culture, is a biomechanical consequence of bipedal locomotion, or reflects systemic physiological differences between modern humans and other primates. We found that bone strength in the hip joint of human foragers is comparable to similarly sized nonhuman primates, and is significantly more robust than sedentary agriculturalists. These results conclusively demonstrate the utility of trabecular bone structure for differentiating activity and mobility patterns among prehistoric hominins and reveal that low levels of physical activity contribute to reduced bone strength, and consequently increased fracture risk, in contemporary human populations. The postcranial skeleton of modern Homo sapiens is relatively gracile compared with other hominoids and earlier hominins. This gracility predisposes contemporary humans to osteoporosis and increased fracture risk. Explanations for this gracility include reduced levels of physical activity, the dissipation of load through enlarged joint surfaces, and selection for systemic physiological characteristics that differentiate modern humans from other primates. This study considered the skeletal remains of four behaviorally diverse recent human populations and a large sample of extant primates to assess variation in trabecular bone structure in the human hip joint. Proximal femur trabecular bone structure was quantified from microCT data for 229 individuals from 31 extant primate taxa and 59 individuals from four distinct archaeological human populations representing sedentary agriculturalists and mobile foragers. Analyses of mass-corrected trabecular bone variables reveal that the forager populations had significantly higher bone volume fraction, thicker trabeculae, and consequently lower relative bone surface area compared with the two agriculturalist groups. There were no significant differences between the agriculturalist and forager populations for trabecular spacing, number, or degree of anisotropy. These results reveal a correspondence between human behavior and bone structure in the proximal femur, indicating that more highly mobile human populations have trabecular bone structure similar to what would be expected for wild nonhuman primates of the same body mass. These results strongly emphasize the importance of physical activity and exercise for bone health and the attenuation of age-related bone loss.

Trabecular Bone Structure in the Humeral and Femoral Heads of Anthropoid Primates

The functional significance of three‐dimensional trabecular bone architecture in the primate postcranial skeleton has received significant interest over the last decade. Some previous work has produced promising results, finding significant relationships between femoral head trabecular bone structure and hypothesized locomotor loading in leaping and nonleaping strepsirrhines. Conversely, most studies of anthropoid femoral head bone structure have found broad similarity across taxonomic and locomotor groups. The goal of this study is to expand on past analyses of anthropoid trabecular bone structure by assessing the effects of differential limb usage on the trabecular bone architecture of the forelimb and hindlimb across taxa characterized by diverse locomotor behaviors, including brachiation, quadrupedalism, and climbing. High‐resolution x‐ray computed tomography scans were collected from the proximal humerus and proximal femur of 55 individuals from five anthropoid primate species, including Symphalangus syndactylus, Papio sp., Presbytis rubicunda, Alouatta caraya, and Pan troglodytes. Trabecular bone structural features including bone volume fraction, anisotropy, trabecular thickness, and trabecular number were quantified in large volumes positioned in the center of the humeral or femoral head. Femoral head trabecular bone volume is consistently and significantly higher than trabecular bone volume in the humerus in all taxa independent of locomotor behavior. Humeral trabecular bone is more isotropic than femoral trabecular bone in all species sampled, possibly reflecting the emphasis on a mobile shoulder joint and manipulative forelimb. The results indicate broad similarity in trabecular bone structure in these bones across anthropoids. Anat Rec, 293:719–729, 2010.

Beyond the closed suture in Apert syndrome mouse models: evidence of primary effects of FGFR2 signaling on facial shape at birth

Apert syndrome is a congenital disorder caused mainly by two neighboring mutations on fibroblast growth factor receptor 2 (FGFR2). Premature closure of the coronal suture is commonly considered the identifying and primary defect triggering or preceding the additional cranial malformations of Apert phenotype. Here we use two transgenic mouse models of Apert syndrome, Fgfr2+/S252W and Fgfr2+/P253R, to explore variation in cranial phenotypes in newborn (P0) mice. Results show that the facial skeleton is the most affected region of the cranium. Coronal suture patency shows marked variation that is not strongly correlated with skull dysmorphology. The craniofacial effects of the FGFR2 mutations are similar, but Fgfr2+/S252W mutant mice display significantly more severe dysmorphology localized to the posterior palate. Our results demonstrate that coronal suture closure is neither the primary nor the sole locus of skull dysmorphology in these mouse models for Apert syndrome, but that the face is also primarily affected. Developmental Dynamics 239:3058–3071, 2010.

Unique Suites of Trabecular Bone Features Characterize Locomotor Behavior in Human and Non-Human Anthropoid Primates

Understanding the mechanically-mediated response of trabecular bone to locomotion-specific loading patterns would be of great benefit to comparative mammalian evolutionary morphology. Unfortunately, assessments of the correspondence between individual trabecular bone features and inferred behavior patterns have failed to reveal a strong locomotion-specific signal. This study assesses the relationship between inferred locomotor activity and a suite of trabecular bone structural features that characterize bone architecture. High-resolution computed tomography images were collected from the humeral and femoral heads of 115 individuals from eight anthropoid primate genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, Symphalangus). Discriminant function analyses reveal that subarticular trabecular bone in the femoral and humeral heads is significantly different among most locomotor groups. The results indicate that when a suite of femoral head trabecular features is considered, trabecular number and connectivity density, together with fabric anisotropy and the relative proportion of rods and plates, differentiate locomotor groups reasonably well. A similar, yet weaker, relationship is also evident in the trabecular architecture of the humeral head. The application of this multivariate approach to analyses of trabecular bone morphology in recent and fossil primates may enhance our ability to reconstruct locomotor behavior in the fossil record.

Comparative forefoot trabecular bone architecture in extant hominids

The appearance of a forefoot push-off mechanism in the hominin lineage has been difficult to identify, partially because researchers disagree over the use of the external skeletal morphology to differentiate metatarsophalangeal joint functional differences in extant great apes and humans. In this study, we approach the problem by quantifying properties of internal bone architecture that may reflect different loading patterns in metatarsophalangeal joints in humans and great apes. High-resolution x-ray computed tomography data were collected for first and second metatarsal heads of Homo sapiens (n = 26), Pan paniscus (n = 17), Pan troglodytes (n = 19), Gorilla gorilla (n = 16), and Pongo pygmaeus (n = 20). Trabecular bone fabric structure was analyzed in three regions of each metatarsal head. While bone volume fraction did not significantly differentiate human and great ape trabecular bone structure, human metatarsal heads generally show significantly more anisotropic trabecular bone architectures, especially in the dorsal regions compared to the corresponding areas of the great ape metatarsal heads. The differences in anisotropy between humans and great apes support the hypothesis that trabecular architecture in the dorsal regions of the human metatarsals are indicative of a forefoot habitually used for propulsion during gait. This study provides a potential route for predicting forefoot function and gait in fossil hominins from metatarsal head trabecular bone architecture.

New species from Ethiopia further expands Middle Pliocene hominin diversity

Middle Pliocene hominin species diversity has been a subject of debate over the past two decades, particularly after the naming of Australopithecus bahrelghazali and Kenyanthropus platyops in addition to the well-known species Australopithecus afarensis. Further analyses continue to support the proposal that several hominin species co-existed during this time period. Here we recognize a new hominin species (Australopithecus deyiremeda sp. nov.) from 3.3–3.5-million-year-old deposits in the Woranso–Mille study area, central Afar, Ethiopia. The new species from Woranso–Mille shows that there were at least two contemporaneous hominin species living in the Afar region of Ethiopia between 3.3 and 3.5 million years ago, and further confirms early hominin taxonomic diversity in eastern Africa during the Middle Pliocene epoch. The morphology of Au. deyiremeda also reinforces concerns related to dentognathic (that is, jaws and teeth) homoplasy in Plio–Pleistocene hominins, and shows that some dentognathic features traditionally associated with Paranthropus and Homo appeared in the fossil record earlier than previously thought.

Trabecular bone microstructure scales allometrically in the primate humerus and femur

Most analyses of trabecular microarchitecture in mammals have focused on the functional significance of interspecific variation, but they have not effectively considered the influence of body size or phylogeny on bone architecture. The goals of this study were to determine the relationship between trabecular bone and body size in the humeral and femoral heads of extant primates, and to assess the influence of phylogeny on bone microstructure. Using a sample of 235 individuals from 34 primate species, ranging in body size from 0.06 to 130 kg, the relationships between trabecular bone structure and body size were assessed by using conventional and phylogenetic regression analyses. Bone volume fraction, trabecular thickness and trabecular spacing increase with body size, whereas bone surface-area-to-volume ratio decreases. Shape variables such as trabecular number, connectivity density and degree of anisotropy scale inversely with size. Most of these variables scale with significant negative allometry, except bone surface-area-to-volume ratio, which scales with slight positive allometry. Phylogenetic regressions indicate a relatively weak phylogenetic signal in some trabecular bone variables. These data demonstrate that, relative to body size, large primates have thinner and more tightly packed trabeculae than small primates. The relatively thin trabeculae in large primates and other mammals, coupled with constraints on trabecular thickness related to osteocyte function, suggest that increased skeletal loads in the postcranial joints of large mammals are probably mitigated not only through alterations in trabecular microarchitecture, but also through other mechanisms such as changes in cortical bone distribution, limb posture and gait speed.

A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae)

The most complete and best-preserved cranium of a Paleogene anthropoid ever found, that of a small female of the early Oligocene (≈29–30 Ma) stem catarrhine species Aegyptopithecus zeuxis, was recovered from the Jebel Qatrani Formation (Fayum Depression, Egypt) in 2004. The specimen is that of a subadult and, in craniodental dimensions, is the smallest Aegyptopithecus individual known. High-resolution computed tomographic (microCT) scanning of the specimens well preserved cranial vault confirms that Aegyptopithecus had relatively unexpanded frontal lobes and a brain-to-body mass ratio lower than those of living anthropoids. MicroCT scans of a male cranium recovered in 1966 [Egyptian Geological Museum, Cairo (CGM) 40237] reveal that previous estimates of its endocranial volume were too large. Thus, some amount of encephalization evolved independently in platyrrhine and catarrhine anthropoids, and the relative brain size of the last common ancestor of crown Anthropoidea was probably strepsirrhine-like or smaller. A. zeuxis shows extreme sexual dimorphism in craniodental morphology (apparently to a degree otherwise seen only in some highly dimorphic Miocene catarrhines), and the crania of female Aegyptopithecus lack a number of morphological features seen in larger males that have been accorded phylogenetic significance in catarrhine systematics (e.g., a well developed rostrum, elongate sagittal crest, and frontal trigon). Although a unique pattern of craniofacial sexual dimorphism may have characterized advanced stem and basal crown catarrhines, expression of various allegedly “discrete” craniofacial features may have been intraspecifically variable in early catarrhine species due to high levels of dimorphism and so should be treated with caution in phylogenetic analyses.