David J. Green

Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa. DOI: http://dx.doi.org/10.7554/eLife.09560.001

Australopithecus afarensis scapular ontogeny, function, and the role of climbing in human evolution.

Climbing Like an Ape Recently, studies of several early human leg and foot fossils have implied that in some early species—even after humans became bipedal—climbing may have still been important. Shoulder bones, which would provide i mportant complementary information, are scarce, however. One of the few examples is from Australopithecus afarensis skeleton (DIK-1-1), which includes both scapula. Green and Alemseged (p. 514; see the Perspective of Larson) provide an analysis of the fossils shoulders and show that, unlike modern humans, they retain several traits that are common in climbing apes, which may indicate that A. afarensis was an active climber. The shoulder of Australopithecus afarensis implies that, although bipedal, this early human was an active climber. Scapular morphology is predictive of locomotor adaptations among primates, but this skeletal element is scarce in the hominin fossil record. Notably, both scapulae of the juvenile Australopithecus afarensis skeleton from Dikika, Ethiopia, have been recovered. These scapulae display several traits characteristic of suspensory apes, as do the few known fragmentary adult australopith representatives. Many of these traits change significantly throughout modern human ontogeny, but remain stable in apes. Thus, the similarity of juvenile and adult fossil morphologies implies that A. afarensis development was apelike. Additionally, changes in other scapular traits throughout African ape development are associated with shifts in locomotor behavior. This affirms the functional relevance of those characteristics, and their presence in australopith fossils supports the hypothesis that their locomotor repertoire included a substantial amount of climbing.

Metacarpal proportions in Australopithecus africanus

Recent work has shown that, despite being craniodentally more derived, Australopithecus africanus had more apelike limb-size proportions than A. afarensis. Here, we test whether the A. africanus hand, as judged by metacarpal shaft and articular proportions, was similarly apelike. More specifically, did A. africanus have a short and narrow first metacarpal (MC1) relative to the other metacarpals? Proportions of both MC breadth and length were considered: the geometric mean (GM) of articular and midshaft measurements of MC1 breadth was compared to those of MC2-4, and MC1 length was compared to MC3 length individually and also to the GM of MC2 and 3 lengths. To compare the extant hominoid sample with an incomplete A. africanus fossil record (11 attributed metacarpals), a resampling procedure imposed sampling constraints on the comparative groups that produced composite intrahand ratios. Resampled ratios in the extant sample are not significantly different from actual ratios based on associated elements, demonstrating the methodological appropriateness of this technique. Australopithecus africanus metacarpals do not differ significantly from the great apes in the comparison of breadth ratios but are significantly greater than chimpanzees and orangutans in both measures of relative length. Conversely, A. africanus has a significantly smaller breadth ratio than modern humans, but does not significantly differ from this group in either measure of relative length. We conclude that the first metacarpals of A. africanus are more apelike in relative breadth while also being more humanlike in relative length, a finding consistent with previous work on A. afarensis hand proportions. This configuration would have likely promoted a high degree of manipulative dexterity, but the relatively slender, apelike first metacarpal suggests that A. africanus did not place the same mechanical demands on the thumb as more recent, stone-tool-producing hominins.

Locomotor activity influences muscle architecture and bone growth but not muscle attachment site morphology

The ability to make behavioural inferences from skeletal remains is critical to understanding the lifestyles and activities of past human populations and extinct animals. Muscle attachment site (enthesis) morphology has long been assumed to reflect muscle strength and activity during life, but little experimental evidence exists to directly link activity patterns with muscle development and the morphology of their attachments to the skeleton. We used a mouse model to experimentally test how the level and type of activity influences forelimb muscle architecture of spinodeltoideus, acromiodeltoideus, and superficial pectoralis, bone growth rate and gross morphology of their insertion sites. Over an 11-week period, we collected data on activity levels in one control group and two experimental activity groups (running, climbing) of female wild-type mice. Our results show that both activity type and level increased bone growth rates influenced muscle architecture, including differences in potential muscular excursion (fibre length) and potential force production (physiological cross-sectional area). However, despite significant influences on muscle architecture and bone development, activity had no observable effect on enthesis morphology. These results suggest that the gross morphology of entheses is less reliable than internal bone structure for making inferences about an individuals past behaviour.

Ontogeny of the hominoid scapula: The influence of locomotion on morphology

Primate shoulder morphology has been linked with locomotor habits, oftentimes irrespective of phylogenetic heritage. Among hominoids, juvenile African apes are known to climb more frequently than adults, while orangutans and gibbons maintain an arboreal lifestyle throughout ontogeny. This study examined if these ontogenetic locomotor differences carry a morphological signal, which should be evident in the scapulae of chimpanzees and gorillas but absent in taxa that do not display ontogenetic behavioral shifts. The scapular morphology of five hominoid primates and one catarrhine outgroup was examined throughout ontogeny to evaluate if scapular traits linked with arboreal activities are modified in response to ontogenetic behavioral shifts away from climbing. Specifically, the following questions were addressed: 1) which scapular characteristics distinguish taxa with different locomotor habits; and 2) do these traits show associated changes during development in taxa known to modify their behavioral patterns? Several traits characterized suspensory taxa from nonsuspensory forms, such as cranially oriented glenohumeral joints, obliquely oriented scapular spines, relatively narrow infraspinous fossae, and inferolaterally expanded subscapularis fossae. The relative shape of the dorsal scapular fossae changed in Pan, Gorilla, and also Macaca in line with predictions based on reported ontogenetic changes in locomotor behavior. These morphological changes were mostly distinct from those seen in Pongo, Hylobates, and Homo and imply a unique developmental pattern, possibly related to ontogenetic locomotor shifts. Accordingly, features that sorted taxa by locomotor habits and changed in concert with ontogenetic behavioral patterns should be particularly useful for reconstructing the locomotor habits of fossil forms.

Footprints reveal direct evidence of group behavior and locomotion in Homo erectus

Bipedalism is a defining feature of the human lineage. Despite evidence that walking on two feet dates back 6–7 Ma, reconstructing hominin gait evolution is complicated by a sparse fossil record and challenges in inferring biomechanical patterns from isolated and fragmentary bones. Similarly, patterns of social behavior that distinguish modern humans from other living primates likely played significant roles in our evolution, but it is exceedingly difficult to understand the social behaviors of fossil hominins directly from fossil data. Footprints preserve direct records of gait biomechanics and behavior but they have been rare in the early human fossil record. Here we present analyses of an unprecedented discovery of 1.5-million-year-old footprint assemblages, produced by 20+ Homo erectus individuals. These footprints provide the oldest direct evidence for modern human-like weight transfer and confirm the presence of an energy-saving longitudinally arched foot in H. erectus. Further, print size analyses suggest that these H. erectus individuals lived and moved in cooperative multi-male groups, offering direct evidence consistent with human-like social behaviors in H. erectus.

Mouse shoulder morphology responds to locomotor activity and the kinematic differences of climbing and running.

Mechanical loads play a significant role in determining long bone shape and strength, but less work has explored how these loads influence flat bones like the scapula, which has been shown to vary with locomotor preference among primate taxa. Here, we tested the effects of voluntary running and climbing exercise in mice to examine how the mechanical loads borne from different locomotor patterns influence shoulder morphological development. Ninety-nine female wild-type mice were distributed equally among sedentary control, activity-wheel running, and vertical climbing experimental conditions. Running mice had the lowest body masses, larger intrinsic shoulder muscles, and the most pronounced differences in scapular size and shape relative to the other groups. Climbing mouse scapular morphology also differed significantly from the control individuals, but these differences were not as marked as those between the running and control mice. This might be attributable in part to greater levels of activity in the wheel-runners relative to the climbers. Additionally, climbing mice held their bodies closer to the substrate and maintained more flexed limbs and posterior hand positions compared with the kinematics of running. As a result, climbers differed significantly from both the running and control mice in developing a relatively broader infraspinous region, which is likely related to preferential recruitment of the infraspinatus and teres minor muscles to maintain flexed shoulder postures. The results of this study demonstrate that variation in activity level and type of locomotor regime over a significant portion of the life history influences muscle and bone development in the shoulder.

The effects of hypermuscularity on shoulder morphology in myostatin-deficient mice.

Mechanical loads, particularly those generated by skeletal muscle, play a significant role in determining long‐bone shape and strength, but it is less clear how these loads influence the morphology of flat bones like the scapula. While scapular morphology has been shown to vary with locomotor mode in mammals, this study seeks to better understand whether genetically modified muscle size can influence scapular shape in the absence of significant locomotor differences. The soft‐ and hard‐tissue morphological characteristics were examined in 11 hypermuscular, mutant (myostatin‐deficient), 20 heterozygote, and 15 wild‐type mouse shoulders. Body mass did not significantly differ among the genotype groups, but homozygous mutant and heterozygote mice had significantly larger shoulder muscles than wild‐type mice. Mutant mice also differed significantly from the wild‐type controls in several aspects of scapular size and shape, including glenohumeral joint orientation, total scapular length, superior border length, and supraspinous and infraspinous fossa length. Conversely, several traits describing superoinferior scapular breadth measures (e.g. total breadth and dorsal scapular fossa breadth) did not significantly differ between mutant and wild‐type mice. Since the intrinsic musculature of the scapula is oriented in a mediolateral fashion, it follows that mediolaterally configured hard‐tissue features like scapular length were most distinct among genotype groups. As had been noted previously with long bones, this study demonstrates that genetically enhanced muscle size has marked effects on the morphological characteristics of the shoulder.

Geometric Morphometrics of Hominoid Infraspinous Fossa Shape

Recent discoveries of early hominin scapulae from Ethiopia (Dikika, Woranso‐Mille) and South Africa (Malapa) have motivated new examinations of the relationship between scapular morphology and locomotor function. In particular, infraspinous fossa shape has been shown to significantly differ among hominoids. However, this region presents relatively few homologous landmarks, such that traditional distance and angle‐based methods may oversimplify this three‐dimensional structure. To more thoroughly assess infraspinous fossa shape variation as it relates to function among adult hominoid representatives, we considered two geometric morphometric (GM) approaches—one employing five homologous landmarks (“wireframe”) and another with 83 sliding semilandmarks along the border of the infraspinous fossa. We identified several differences in infraspinous fossa shape with traditional approaches, particularly in superoinferior fossa breadth and scapular spine orientation. The wireframe analysis reliably captured the range of shape variation in the sample, which reflects the relatively straightforward geometry of the infraspinous fossa. Building on the traditional approach, the GM results highlighted how the orientation of the medial portion of the infraspinous fossa differed relative to both the axillary border and spine. These features distinguished Pan from Gorilla in a way that traditional analyses had not been able to discern. Relative to the wireframe method, the semilandmark approach further distinguished Pongo from Homo, highlighting aspects of infraspinous fossa morphology that may be associated with climbing behaviors in hominoid taxa. These results highlight the ways that GM methods can enhance our ability to evaluate complex aspects of shape for refining and testing hypotheses about functional morphology. Anat Rec, 298:180–194, 2015.

Reconciling the convergence of supraspinous fossa shape among hominoids in light of locomotor differences

Differences in scapular morphology between modern humans and the African and lesser apes are associated with the distinct locomotor habits of these groups. However, several traits, particularly aspects of the supraspinous fossa, are convergent between Homo and Pongo-an unexpected result given their divergent locomotor habits. Many morphological assessments of the scapula rely on the limited number of static landmarks available, and traditional approaches like these tend to oversimplify scapular shape. Here, we present the results of two geometric morphometric (GM) analyses of hominoid supraspinous fossa shape-one employing five homologous landmarks and another with 83 sliding semilandmarks-alongside those of traditional methods to evaluate if three-dimensional considerations of fossa shape afford more comprehensive insights into scapular shape and functional morphology. Traditional measures aligned Pongo and Homo with narrow and transversely oriented supraspinous fossae, whereas African ape and Hylobates fossae are broader and more obliquely situated. However, our GM results highlight that much of the convergence between Homo and Pongo is reflective of their more medially positioned superior angles. These approaches offered a more complete assessment of supraspinous shape and revealed that the Homo fossa, with an intermediate superior angle position and moderate superoinferior expansion, is actually reminiscent of the African ape shape. Additionally, both Pongo and Hylobates were shown to have more compressed fossae, something that has not previously been identified through traditional analyses. Thus, the total morphological pattern of the Pongo supraspinous fossa is unique among hominoids, and possibly indicative of its distinctive locomotor habits.