Ontogenetic changes to metacarpal trabecular bone structure in mountain and western lowland gorillas.

The trabecular bone morphology of adult extant primates has been shown to reflect mechanical loading related to locomotion. However, ontogenetic studies of humans and other mammals suggest an adaptive lag between trabecular bone response and current mechanical loading patterns that could result in adult trabecular bone morphology reflecting juvenile behaviours. This study investigates ontogenetic changes in the trabecular bone structure of the third metacarpal of mountain gorillas (Gorilla beringei beringei; n = 26) and western lowland gorillas (Gorilla gorilla gorilla; n = 26) and its relationship to expected changes in locomotor loading patterns. Results show that trabecular bone reflects predicted mechanical loading throughout ontogeny. Bone volume fraction, trabecular thickness and trabecular number are low at birth and increase with age, although degree of anisotropy remains relatively stable throughout ontogeny. A high concentration of bone volume fraction can be observed in the distopalmar region of the third metacarpal epiphysis in early ontogeny, consistent with the high frequency of climbing, suspensory and other grasping behaviours in young gorillas. High trabecular bone concentration increases dorsally in the epiphysis during the juvenile period as terrestrial knuckle-walking becomes the primary form of locomotion. However, fusion of the epiphysis does not take place until 10-11 years of age, and overall trabecular structure does not fully reflect the adult pattern until 12 years of age, indicating a lag between adult-like behaviours and adult-like trabecular morphology. We found minimal differences in trabecular ontogeny between mountain and western lowland gorillas, despite presumed variation in the frequencies of arboreal locomotor behaviours. Altogether, ontogenetic changes in Gorilla metacarpal trabecular structure reflect overall genus-level changes in locomotor behaviours throughout development, but with some ontogenetic lag that should be considered when drawing functional conclusions from bone structure in extant or fossil adolescent specimens.

Kinematics of the anthropoid os centrale and the functional consequences of scaphoid-centrale fusion in African apes and hominins.

In most primates, the os centrale is interposed between the scaphoid, trapezoid, trapezium, and head of the capitate, thus constituting a component of the wrist's midcarpal complex. Scaphoid-centrale fusion is among the clearest morphological synapomorphies of African apes and hominins. Although it might facilitate knuckle-walking by increasing the rigidity and stability of the radial side of the wrist, the exact functional significance of scaphoid-centrale fusion is unclear. If fusion acts to produce a more rigid radial wrist that stabilizes the hand and limits shearing stresses, then in taxa with a free centrale, it should anchor ligaments that check extension and radial deviation, but exhibit motion independent of the scaphoid. Moreover, because the centrale sits between the scaphoid and capitate (a major stabilizing articulation), scaphoid-centrale mobility should correlate with scaphocapitate mobility in extension and radial deviation. To test these hypotheses, the centrale's ligamentous binding was investigated via dissection in Pongo and Papio, and the kinematics of the centrale were quantified in a cadaveric sample of anthropoids (Pongo sp., Ateles geoffroyi, Colobus guereza, Macaca mulatta, and Papio anubis) using a computed-tomography-based method to track wrist-bone motion. Results indicate that the centrale rotates freely relative to the scaphoid in all taxa. However, centrale mobility is only correlated with scaphocapitate mobility during extension in Pongo-possibly due to differences in overall wrist configuration between apes and monkeys. If an extant ape-like wrist characterized early ancestors of African apes and hominins, then scaphoid-centrale fusion would have increased midcarpal rigidity in extension relative to the primitive condition. Although biomechanically consistent with a knuckle-walking hominin ancestor, this assumes that the trait evolved specifically for that biological role, which must be squared with contradictory interpretations of extant and fossil hominoid morphology. Regardless of its original adaptive significance, scaphoid-centrale fusion likely presented a constraint on early hominin midcarpal mobility.

Hand pressures during arboreal locomotion in captive bonobos (Pan paniscus).

Evolution of the human hand has undergone a transition from use during locomotion to use primarily for manipulation. Previous comparative morphological and biomechanical studies have focused on potential changes in manipulative abilities during human hand evolution, but few have focused on functional signals for arboreal locomotion. Here, we provide this comparative context though the first analysis of hand loading in captive bonobos during arboreal locomotion. We quantify pressure experienced by the fingers, palm and thumb in bonobos during vertical locomotion, suspension and arboreal knuckle-walking. The results show that pressure experienced by the fingers is significantly higher during knuckle-walking compared with similar pressures experienced by the fingers and palm during suspensory and vertical locomotion. Peak pressure is most often experienced at or around the third digit in all locomotor modes. Pressure quantified for the thumb is either very low or absent, despite the thumb making contact with the substrate during all suspensory and vertical locomotor trials. Unlike chimpanzees, bonobos do not show a rolling pattern of digit contact with the substrate during arboreal knuckle-walking - instead, we found that digits 3 and 4 typically touch down first and digit 5 almost always made contact with the substrate. These results have implications for interpreting extant and fossilized hand morphology; we expect bonobo (and chimpanzee) bony morphology to primarily reflect the biomechanical loading of knuckle-walking, while functional signals for arboreal locomotion in fossil hominins are most likely to appear in the fingers, particularly digit 3, and least likely to appear in the morphology of the thumb.

Unexpected terrestrial hand posture diversity in wild mountain gorillas.

OBJECTIVES: Gorillas, along with chimpanzees and bonobos, are ubiquitously described as 'knuckle-walkers.' Consequently, knuckle-walking (KW) has been featured pre-eminently in hypotheses of the pre-bipedal locomotor behavior of hominins and in the evolution of locomotor behavior in apes. However, anecdotal and behavioral accounts suggest that mountain gorillas may utilize a more complex repertoire of hand postures, which could alter current interpretations of African ape locomotion and its role in the emergence of human bipedalism. Here we documented hand postures during terrestrial locomotion in wild mountain gorillas to investigate the frequency with which KW and other hand postures are utilized in the wild. MATERIALS AND METHODS: Multiple high-speed cameras were used to record bouts of terrestrial locomotion of 77 habituated mountain gorillas at Bwindi Impenetrable National Park (Uganda) and Volcanoes National Park (Rwanda). RESULTS: We captured high-speed video of hand contacts in 8% of the world's population of mountain gorillas. Our results reveal that nearly 40% of these gorillas used "non-KW" hand postures, and these hand postures constituted 15% of all hand contacts. Some of these "non-KW" hand postures have never been documented in gorillas, yet match hand postures previously identified in orangutans. DISCUSSION: These results highlight a previously unrecognized level of hand postural diversity in gorillas, and perhaps great apes generally. Although present at lower frequencies than KW, we suggest that the possession of multiple, versatile hand postures present in wild mountain gorillas may represent a shared feature of the African ape and human clade (or even great ape clade) rather than KW per se.

Ontogeny and variability of trabecular bone in the chimpanzee humerus, femur and tibia.

OBJECTIVES: Trabecular bone structure is known to be influenced by joint loading during life. However, many additional variables have the potential to contribute to trabecular bone structure of an adult individual, including age, sex, body size, genetics, and overall activity level. There is little research into intraspecific variability in trabecular bone and ontogeny of trabecular bone structure, especially in nonhuman primates. MATERIALS AND METHODS: This study investigates trabecular structure in adult and immature chimpanzees from a single population using high-resolution microcomputed tomographic scans of the proximal humerus, proximal femur, and distal tibia. Trabecular bone volume fraction (BV/TV), trabecular thickness (Tb.Th), trabecular number (Tb.N), trabecular spacing (Tb.Sp), and degree of anisotropy (DA) were quantified in specific regions of adult and immature chimpanzees, and color maps were generated to visualize the distribution of BV/TV throughout the joint in the metaphysis of immature specimens. RESULTS: The results demonstrate that variability in adult trabecular structure cannot be explained by sex or body size. During ontogeny, there is a general increase in trabecular BV/TV and Tb.Th with age, and ratios of trabecular parameters between the fore- and hindlimb may be consistent with locomotor transitions during ontogeny. DISCUSSION: Variation in trabecular morphology among adult individuals is not related to sex or body size, and the factors contributing to intraspecific variability, such as overall activity levels and genetic differences, require further investigation. Trabecular ontogeny in chimpanzees differs from humans in some respects, most notably the absence of a high BV/TV at birth.

Great ape walking kinematics: Implications for hominoid evolution.

OBJECTIVES: Great apes provide a point of reference for understanding the evolution of locomotion in hominoids and early hominins. We assessed (1) the extent to which great apes use diagonal sequence, diagonal couplet gaits, like other primates, (2) the extent to which gait and posture vary across great apes, and (3) the role of body mass and limb proportions on ape quadrupedal kinematics. METHODS: High-speed digital video of zoo-housed bonobos (Pan paniscus, N = 8), chimpanzees (Pan troglodytes, N = 13), lowland gorillas (Gorilla gorilla, N = 13), and orangutans (Pongo spp. N = 6) walking over-ground at self-selected speeds were used to determine the timing of limb touch-down, take-off, and to measure joint and segment angles at touch-down, midstance, and take-off. RESULTS: The great apes in our study showed broad kinematic and spatiotemporal similarity in quadrupedal walking. Size-adjusted walking speed was the strongest predictor of gait variables. Body mass had a negligible effect on variation in joint and segment angles, but stride frequency did trend higher among larger apes in analyses including size-adjusted speed. In contrast to most other primates, great apes did not favor diagonal sequence footfall patterns, but exhibited variable gait patterns that frequently shifted between diagonal and lateral sequences. CONCLUSION: Similarities in the terrestrial walking kinematics of extant great apes likely reflect their similar post-cranial anatomy and proportions. Our results suggest that the walking kinematics of orthograde, suspensory Miocene ape species were likely similar to living great apes, and highlight the utility of videographic and behavioral data in interpreting primate skeletal morphology.

Manual pressure distribution patterns of knuckle-walking apes.

Differences in how the hands of gorillas and chimpanzees contact the ground while knuckle walking have been noted but generally not quantified. It is widely believed that gorillas maintain a pronated arm and contact the ground with digits 2-5 consistently, while chimpanzees have variable arm position and digit contact. To further test these generalizations, distribution of pressure across the manus, peak digital pressures, and hand position were quantified using a pressure mat in eight captive chimpanzees (Pan troglodytes) and seven gorillas (Gorilla gorilla). Chimpanzees and gorillas make initial ground contact with the ulnar aspect of the hand and pressure moves radially. They differ in which digit usually makes final contact and receives maximum pressure, and hand position during contact. Gorillas regularly use a palm-back hand position and touch-off with digit 2. They show less variation in pressure application across the digits. Chimpanzees are more variable in hand position and pressure application. In both, hand position plays a key role in determining which digit acts as the final touch-off element.

Carpal allometry of African apes among mammals.

OBJECTIVES: Morphological variation in African ape carpals has been used to support the idea that Pan and Gorilla evolved knuckle-walking independently. Little work, however, has focused on the effect of body mass on carpal morphology. Here, we compare carpal allometry in Pan and Gorilla to that of other quadrupedal mammals with similar body mass differences. If allometric trends in Pan and Gorilla carpals mirror those of other mammals with similar body mass variation, then body mass differences may provide a more parsimonious explanation for African ape carpal variation than the independent evolution of knuckle-walking. MATERIALS AND METHODS: Three linear measurements were collected on the capitate, hamate, lunate, and scaphoid (or scapholunate) of 39 quadrupedal species from six mammalian families/subfamilies. Relationships between linear measurements and estimated body mass were analyzed using reduced major axis regression. Slopes were compared to 0.33 for isometry. RESULTS: Within Hominidae, higher body mass taxa (Gorilla) have relatively anteroposteriorly wider, mediolaterally wider, and/or proximodistally shorter capitates, hamates, and scaphoids than low body mass taxa (Pan). These allometric relationships are mirrored in most, but not all, mammalian families/subfamilies included in the analysis. CONCLUSIONS: Within most mammalian families/subfamilies, carpals of high body mass taxa are proximodistally shorter, anteroposteriorly wider, and mediolaterally wider than those of low body mass taxa. These distinctions may be caused by the need to accommodate relatively higher forelimb loading associated with greater body mass. Because these trends occur within multiple mammalian families/subfamilies, some carpal variation in Pan and Gorilla is consistent with body mass differences.

Ticks, Hair Loss, and Non-Clinging Babies: A Novel Tick-Based Hypothesis for the Evolutionary Divergence of Humans and Chimpanzees.

Human straight-legged bipedalism represents one of the earliest events in the evolutionary split between humans (Homo spp.) and chimpanzees (Pan spp.), although its selective basis is a mystery. A carrying-related hypothesis has recently been proposed in which hair loss within the hominin lineage resulted in the inability of babies to cling to their mothers, requiring mothers to walk upright to carry their babies. However, a question remains for this model: what drove the hair loss that resulted in upright walking? Observers since Darwin have suggested that hair loss in humans may represent an evolutionary strategy for defence against ticks. The aim of this review is to propose and evaluate a novel tick-based evolutionary hypothesis wherein forest fragmentation in hominin paleoenvironments created conditions that were favourable for tick proliferation, selecting for hair loss in hominins and grooming behaviour in chimpanzees as divergent anti-tick strategies. It is argued that these divergent anti-tick strategies resulted in different methods for carrying babies, driving the locomotor divergence of humans and chimpanzees.

A Geometric Morphometric Examination of Hominoid Third Metacarpal Shape and Its Implications for Inferring the Precursor to Terrestrial Bipedalism.

The third metacarpal has been a focus of study when examining questions surrounding early hominin locomotion since this bone is adapted to the diverse range of positional behaviors performed by extant hominoids. The shape of this bone is potentially under strong selective pressure related to the biomechanical demands of terrestrial knuckle-walking, arboreal clambering, and brachiation performed by extant hominoids since the hand directly interacts with the substrate during the performance of these movements. The objective of the present study was to explore shape variation of the third metacarpal and examine how different parts of the bone discriminated between hominoid genera that perform these different locomotor behaviors. In addition to examining general interspecies variation, shape analysis was applied to testing the knuckle-walking hypothesis for human evolution. Fourteen 3D landmark coordinates were collected on hominoid third metacarpals, and principal component analysis and Procrustes distances were used to examine metacarpal shape. Comparable measurements were collected on fossilized third metacarpals of Australopithecus afarensis as an early hominin test case for examining the knuckle-walking hypothesis. Analyses that included landmarks collected on both ends of the bone distinguished humans from great apes and presented a strong functional signal related to suspensory locomotion among nonhuman hominoids, whereas the distal articular surface provided the strongest knuckle-walking signal. The shapes of Australopithecus afarensis metacarpals examined in the current study did not provide evidence for a trajectory of shape change in early hominin evolution that started from a metacarpal adapted for terrestrial knuckle-walking. Anat Rec, 302:983-998, 2019. © 2018 Wiley Periodicals, Inc.

Why Do Knuckle-Walking African Apes Knuckle-Walk?

Among living mammals, only the African apes and some anteaters adopt knuckle-walking as their primary locomotor behavior. That Pan and Gorilla both knuckle-walk has been cited as evidence of their common ancestry and a primitive condition for a combined Homo, Pan, and Gorilla clade. Recent research on forelimb ontogeny and anatomy, in addition to recently described hominin fossils, indicate that knuckle-walking was independently acquired after divergence of the Pan and Gorilla lineages. Although the large-bodied, largely suspensory orangutan shares some aspects of the African ape bauplan, it does not regularly knuckle-walk when terrestrial. While many anatomical correlates of knuckle-walking have been identified, a functional explanation of this unusual locomotor pattern has yet to be proposed. Here, we argue that it was adopted by African apes as a means of ameliorating the consequences of repetitive impact loadings on the soft and hard tissues of the forelimb by employing isometric and/or eccentric contraction of antebrachial musculature during terrestrial locomotion. Evidence of this adaptation can be found in the differential size and fiber geometry of the forearm musculature, and differences in torso shape between the knuckle-walking and non-knuckle-walking apes (including humans). We also argue that some osteological features of the carpus and metacarpus that have been identified as adaptations to knuckle-walking are consequences of cartilage remodeling during ontogeny rather than traits limiting motion in the hand and wrist. An understanding of the functional basis of knuckle-walking provides an explanation of the locomotor parallelisms in modern Pan and Gorilla. Anat Rec, 301:496-514, 2018. © 2018 Wiley Periodicals, Inc.

Locomotor Hand Postures, Carpal Kinematics During Wrist Extension, and Associated Morphology in Anthropoid Primates.

The biomechanics of wrist extension (or dorsiflexion) are important for understanding functional adaptation of the primate hand because extension mobility varies with habitual locomotor hand posture and facilitates certain manipulative tasks. Here, intercarpal kinematics are employed to investigate mechanisms underlying wrist extension in a sample of anthropoids representing various arboreal and terrestrial locomotor modes. Carpal kinematics are studied using computed-tomography of cadaveric forelimbs, and these data are combined with a morphometric analysis of biomechanically-informative anatomical features. The results indicate that stiff-wristed knuckle-walking chimpanzees and digitigrade baboons are characterized by low ranges of motion (ROMs) at the radiocarpal and midcarpal complexes. Palmigrade-capable monkeys have high extension ROMs at both the radiocarpus and midcarpus, while palmigrade-capable orangutans achieve wrist extension through moderate radiocarpal ROMs and high midcarpal ROMs. Morphometrics demonstrate that a more projecting dorsal ridge of the distal radius corresponds with low-to-moderate radioscaphoid mobility in the apes, but that baboons resemble palmigrade-capable monkeys in this metric. Thus, the dorsal ridge of the radius alone is not a good indicator of wrist mobility and hand posture. However, the extent of the lunate's articular arc on the dorsum of the capitate head is correlated with midcarpal mobility across taxa. These findings suggest that although a precise relationship between wrist extension ROM and morphology is difficult to define, the presence of a pronounced dorsal ridge combined with an abbreviated dorsal capitate articular arc reflects limited overall dorsiflexion with attendant constraints on the adoption of palmigrade hand postures. Anat Rec, 300:382-401, 2017. © 2016 Wiley Periodicals, Inc.

The Functional Anatomy of the Carpometacarpal Complex in Anthropoids and Its Implications for the Evolution of the Hominoid Hand.

Previously, we described several features of the carpometacarpal joints in extant large-bodied apes that are likely adaptations to the functional demands of vertical climbing and suspension. We observed that all hominids, including modern humans and the 4.4-million-year-old hominid Ardipithecus ramidus, lacked these features. Here, we assess the uniqueness of these features in a large sample of monkey, ape, and human hands. These new data provide additional insights into the functional adaptations and evolution of the anthropoid hand. Our survey highlights a series of anatomical adaptations that restrict motion between the second and third metacarpals (MC2 and MC3) and their associated carpals in extant apes, achieved via joint reorganization and novel energy dissipation mechanisms. Their hamate-MC4 and -MC5 joint surface morphologies suggest limited mobility, at least in Pan. Gibbons and spider monkeys have several characters (angled MC3, complex capitate-MC3 joint topography, variably present capitate-MC3 ligaments) that suggest functional convergence in response to suspensory locomotion. Baboons have carpometacarpal morphology suggesting flexion/extension at these joints beyond that observed in most other Old World monkeys, probably as an energy dissipating mechanism minimizing collision forces during terrestrial locomotion. All hominids lack these specializations of the extant great apes, suggesting that vertical climbing was never a central feature of our ancestral locomotor repertoire. Furthermore, the reinforced carpometacarpus of vertically climbing African apes was likely appropriated for knuckle-walking in concert with other novel potential energy dissipating mechanisms. The most parsimonious explanation of the structural similarity of these carpometacarpal specializations in great apes is that they evolved independently.