Hip medial rotator action of gluteus medius in Japanese macaque (Macaca fuscata) and implications to adaptive significance for quadrupedal walking in primates.

The gluteus medius (GM) muscle in quadrupedal primates has long been thought to mainly act as a hip extensor. However, previous reports argue that it may be a prime hip medial rotator and functions to rotate the pelvis in the horizontal plane, suggesting the functional differentiation between the GM and other hip extensors as hamstrings. In this study, we aim to quantify the muscle actions of the GM and hamstrings using muscle moment arm lengths and discuss the functional differentiation among hip extensors. Muscle attachment sites of eight specimens of Japanese macaque (Macaca fuscata) were digitized, and musculoskeletal models were constructed. Flexor-extensor, abductor-adductor, and medial-lateral rotator moment arms were calculated as the models were moved following the experimentally acquired kinematic data during walking on a pole substrate. Using electromyography, we also recorded the pattern of muscle activation. The GM showed a larger medial rotator moment arm length than the extensor moment arm length when it was activated, suggesting this muscle acts mainly as a hip medial rotator rather than as a hip extensor. The medial rotator action of the GM in the early support phase may rotate the pelvis in the horizontal plane and function to help contralateral forelimb reaching as a previous study suggested and facilitate contralateral hindlimb swinging to place the foot near the ipsilateral forelimb's hand.

New femoral remains of Nacholapithecus kerioi: Implications for intraspecific variation and Miocene hominoid evolution.

The middle Miocene stem kenyapithecine Nacholapithecus kerioi (16-15 Ma; Nachola, Kenya) is represented by a large number of isolated fossil remains and one of the most complete skeletons in the hominoid fossil record (KNM-BG 35250). Multiple fieldwork seasons performed by Japanese-Kenyan teams during the last part of the 20th century resulted in the discovery of a large sample of Nacholapithecus fossils. Here, we describe the new femoral remains of Nacholapithecus. In well-preserved specimens, we evaluate sex differences and within-species variation using both qualitative and quantitative traits. We use these data to determine whether these specimens are morphologically similar to the species holotype KNM-BG 35250 (which shows some plastic deformation) and to compare Nacholapithecus with other Miocene hominoids and extant anthropoids to evaluate the distinctiveness of its femur. The new fossil evidence reaffirms previously reported descriptions of some distal femoral traits, namely the morphology of the patellar groove. However, results also show that relative femoral head size in Nacholapithecus is smaller, relative neck length is longer, and neck-shaft angle is lower than previously reported for KNM-BG 35250. These traits have a strong functional signal related to the hip joint kinematics, suggesting that the morphology of the proximal femur in Nacholapithecus might be functionally related to quadrupedal-like behaviors instead of more derived antipronograde locomotor modes. Results further demonstrate that other African Miocene apes (with the exception of Turkanapithecus kalakolensis) generally fall within the Nacholapithecus range of variation, whose overall femoral shape resembles that of Ekembo spp. and Equatorius africanus. Our results accord with the previously inferred locomotor repertoire of Nacholapithecus, indicating a combination of generalized arboreal quadrupedalism combined with other antipronograde behaviors (e.g., vertical climbing).

A comparison of axial trunk rotation during bipedal walking between humans and Japanese macaques.

OBJECTIVES: Human walking involves out-of-phase axial rotations of the thorax and pelvis. It has long been believed that this rotational capability is a distinctive feature of the genus Homo. However, Thompson et al. (2015) showed that chimpanzees also counter-rotate their thorax relative to the pelvis during bipedal walking, which raised questions regarding the origins and development of this characteristic. In this study, we measured the axial rotation of the trunk during bipedal walking in humans and macaques to investigate if intra-trunk axial rotations are observed in non-hominoid primate species. MATERIALS AND METHODS: We collected three-dimensional trunk kinematic data during bipedal walking in six humans and five Japanese macaques. The human subjects walked on a treadmill, and the animal subjects walked on a 5-m runway. During walking, the positions of cluster markers, which defined trunk segments, were recorded by multiple video cameras. Segmental xyz coordinates were digitized, and transverse rotations were calculated using motion analysis software. RESULTS: Although trunk rotations in the global coordinate system were greater in macaques than in humans, the intra-trunk rotation and range of motion showed a similar pattern in the two species. CONCLUSIONS: Thoracic rotation relative to the pelvis during bipedal walking is not unique to the hominid lineage but rather a characteristic generated by the mechanical requirements of bipedal walking. The fact that the range of motion of counter rotation is similar in these species infers that an optimal range of rotation exists for bipedal walking.

Influences of passive intervertebral range of motion on cervical vertebral form.

OBJECTIVES: The cervical spine is the junction between the head and trunk, and it therefore facilitates head mobility and stability. The goal of this study is to test several predictions regarding cervical morphology and intervertebral ranges of motion. MATERIALS AND METHODS: Intervertebral ranges of motion for 12 primate species were collected via radiographs or taken from the literature. Morphometric data describing functionally relevant aspects of cervical vertebral morphology were obtained from museum specimens representing these species. We tested for correlations between intervertebral movement and vertebral form using phylogenetic generalized least-squares regression. RESULTS: Results demonstrate limited support for the hypothesis that range of motion (ROM) is influenced by cervical vertebral morphology. Few morphological variables correlate with ROM and no relationship is consistently significant across cervical joints. DISCUSSION: These results indicate that the relationship between vertebral morphology and joint ranges of motion is, at most, weak, providing little support the use of bony morphology to reconstruct axial mobility in fossil specimens. Future work should investigate the role of soft tissues in vertebral joint stability.

Sexual dimorphism of body size in an African fossil ape, Nacholapithecus kerioi.

Sexual size dimorphism in the African fossil ape Proconsul nyanzae (18 million years ago, 18 Ma) has been previously documented. However, additional evidence for sexual dimorphism in Miocene hominoids can provide great insight into the history of extant hominoid mating systems. The present study focused on body mass (BM) sexual dimorphism in Nacholapithecus kerioi from the Middle Miocene (16-15 Ma) in Africa. Bootstrap analysis revealed that P. nyanzae BM sexual dimorphism was lower than that in Pan troglodytes, which exhibits moderate sexual dimorphism, as reported previously. The same simulation revealed that BM sexual dimorphism of N. kerioi was comparable with that in Gorilla spp.; i.e., the males were approximately twice as large as the females. High sexual dimorphism in extant apes is usually indicative of a polygynous social structure (gorilla) or solitary/fission-fusion social system (orangutan). However, because of the high proportion of adult males in this fossil assemblage, the magnitude of dimorphism inferred here cannot be associated with a gorilla-like polygynous or oranguran-like solitary/fission-fusion social structure, and may reflect either taphonomic bias, or some other social structure. Extant hominoids have a long evolutionary history owing to their deep branching, comprising only a few existing members of the original highly successful group. Therefore, it is not surprising that the mating systems of extant hominoids fail to provide fossil apes with a perfect "model". The mating systems of extinct hominoids may have been more diverse than those of extant apes.

Topological analysis of DPY19L3, a human C-mannosyltransferase.

C-mannosylation is a rare type of protein glycosylation, the functions and mechanisms of which remain unclear. Recently, we identified DPY19L3 as a C-mannosyltransferase of R-spondin1 in human cells. DPY19L3 is predicted to be a multipass transmembrane protein that localizes to the endoplasmic reticulum (ER); however, its structure is undetermined. In this study, we propose a topological structure of DPY19L3 by in silico analysis and experimental methods such as redox-sensitive luciferase assay and introduction of N-glycosylation sites, suggesting that DPY19L3 comprises 11 transmembrane regions and two re-entrant loops with the N- and C-terminal ends facing the cytoplasm and ER lumen, respectively. Furthermore, DPY19L3 has four predicted N-glycosylation sites, and we have demonstrated that DPY19L3 is N-glycosylated at Asn118 and Asn704 but not Asn319 and Asn439 , supporting our topological model. By mass spectrometry, we measured the C-mannosyltransferase activity of N-glycosylation-defective mutants of DPY19L3 and isoform2, a splice variant, which lacks the C-terminal luminal region of DPY19L3. Isoform2 does not possess C-mannosyltransferase activity, indicating the importance of the C-terminal region; however, N-glycosylations of DPY19L3 do not have any roles for its enzymatic activity. These novel findings on DPY19L3 provide important insights into the mechanism of C-mannosylation.

Sacral vertebral remains of the Middle Miocene hominoid Nacholapithecus kerioi from northern Kenya.

This study describes two new sacral specimens of Nacholapithecus kerioi, KNM-BG 42753I and KNM-BG 47687A, from the Aka Aiteputh Formation in Nachola, northern Kenya, excavated in 2002. They are of roughly equal size and are considered to belong to males. When scaled by body mass, the lumbosacral articular surface area of the better preserved specimen, KNM-BG 42753I, is smaller than that in Old World monkeys but similar to that in extant great apes and New World monkeys, as well as Proconsul nyanzae. The relatively narrow dimensions of the first sacral vertebral body in the transverse and sagittal planes are characteristics of N. kerioi and P. nyanzae and similar to those of extant great apes. In N. kerioi, lumbosacral surface area relative to body mass is small. This may simply be an extension of a trend from the previously reported small thoracolumbar vertebrae to the sacrum. ​The first sacral vertebrae of N. kerioi and Epipliopithecus vindobonensis have a higher craniocaudal vertebral body reduction (CVR; a higher CVR indicates a wider cranial width relative to a narrower caudal width), similar to that in Old World monkeys. Old World monkeys have a higher CVR, and usually have three sacral vertebrae, fewer than seen in extant great apes, which have a lower CVR and four to six (sometimes as many as eight) sacral vertebrae. New World monkeys have a lower CVR than Old World monkeys, but generally possess only three sacral vertebrae, and have a large caudal articular surface, which may be related, at least in the Atelidae, to the grasping ability of their tails. The possibility that N. kerioi had only three sacral vertebrae cannot be ruled out, because E. vindobonensis and Old World monkeys, with higher CVRs, have sacra consisting of three sacral vertebrae.

Identification of a novel compound that inhibits osteoclastogenesis by suppressing nucleoside transporters.

We screened small-molecule compounds that inhibit osteoclast differentiation to find new anti-osteoporosis agents and found that a novel compound, SUKU-1, suppressed osteoclastogenesis. We also synthesized 38 derivatives of SUKU-1 and discovered that nine of them had inhibitory effects on osteoclastogenesis and that SUKU-33 was the most potent inhibitor. Next, we investigated the mechanisms by which SUKU-33 suppressed osteoclast differentiation. By measuring the uptake of [(3) H]-uridine in cells, we found that SUKU-33 suppressed both equilibrative nucleoside transporters and concentrative nucleoside transporters. These results suggest that SUKU-33 inhibits osteoclast differentiation by suppressing nucleoside transporters.

Carpal bones of Nacholapithecus kerioi, a Middle Miocene Hominoid From Northern Kenya.

OBJECTIVES: The carpal bones of the middle Miocene hominoid Nacholapithecus kerioi are described based on new materials. MATERIALS AND METHODS: The materials comprise a trapezoid, three capitates, two hamates, a centrale, a lunate, a triquetrum, and a pisiform, collected during the 2001 and 2002 field seasons from Nachola, Kenya. We also describe a pisiform recently assigned to the type specimen of N. kerioi, KNM-BG 35250. RESULTS: In the Nacholapithecus wrist, the ulnar styloid process articulates with both the triquetrum and pisiform, and the triquetrum facet on the hamate is relatively proximodistally oriented in dorsal view. The Nacholapithecus capitate possesses a moderate distopalmar hook-like process and separated radial articular facets for the trapezoid and the second metacarpal due to the carpometacarpal ligament attachment that is absent in the Proconsul capitate. DISCUSSION: The carpal anatomy of Nacholapithecus is similar to that of the early Miocene hominoid Proconsul. However, Nacholapithecus wrist anatomy appears to exhibit slightly more emphasized stability. Am J Phys Anthropol 160:469-482, 2016. © 2016 Wiley Periodicals, Inc.

Morphology of the thoracolumbar spine of the middle Miocene hominoid Nacholapithecus kerioi from northern Kenya.

A new caudal thoracic and a new lumbar vertebra of Nacholapithecus kerioi, a middle Miocene hominoid from northern Kenya, are reported. The caudal thoracic vertebral body of N. kerioi has a rounded median ventral keel and its lateral sides are moderately concave. The lumbar vertebral body has an obvious median ventral keel. Based on a comparison of vertebral body cranial articular surface size between the caudal thoracic vertebrae in the present study and one discussed in a previous study (KNM-BG 35250BO, a diaphragmatic vertebra), N. kerioi has at least two post-diaphragmatic vertebrae (rib-bearing lumbar-type thoracic vertebrae), unlike extant hominoids. It also has thick, rounded, and moderately long metapophyses on the lumbar vertebra that project dorsolaterally. The spinous process bases of its caudal thoracic and lumbar vertebrae originate caudally between the postzygapophyses, as described previously in the KNM-BG 35250 holotype specimen. In other words, the postzygapophyses of N. kerioi do not project below the caudal border of the spinous processes, similar to those of extant great apes, and unlike small apes and monkeys, which have more caudally projecting postzygapophyses. Nacholapithecus kerioi has a craniocaudally expanded spinous process in relation to vertebral body length, also similar to extant great apes. Both these spinous process features of N. kerioi differ from those of Proconsul nyanzae. The caudal thoracic vertebra of N. kerioi has a caudally-directed spinous process, whose tip is tear-drop shaped. These features resemble those of extant apes. The morphology of the spinous process tips presumably helps vertebral stability by closely stacking adjacent spinous process tips as seen in extant hominoids. The morphology of the spinous process and postzygapophyses limits the intervertebral space and contributes to the stability of the functional lumbar region as seen in extant great apes, suggesting that antipronograde activity was included in the positional behavior of N. kerioi.

Functional morphology and anatomy of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene hominoid from Kenya.

This paper describes the morphology of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene primate species excavated from Nachola, Kenya in 1999-2002. The cervical vertebrae in Nacholapithecus are larger than those of Papio cynocephalus. They are more robust relative to more caudal vertebral bones. Since Nacholapithecus had large forelimbs, it is assumed that strong cervical vertebrae would have been required to resist muscle reaction forces during locomotion. On the other hand, the vertebral foramen of the lower cervical vertebrae in Nacholapithecus is almost the same size as or smaller than that of P. cynocephalus. Atlas specimens of Nacholapithecus resemble those of extant great apes with regard to the superior articular facet, and they have an anterior tubercle trait intermediate between that of extant apes and other primate species. Nacholapithecus has a relatively short and thick dens on the axis, similar to those of extant great apes and the axis body shape is intermediate between that of extant apes and other primates. Moreover, an intermediate trait between extant great apes and other primate species has been indicated with regard to the angle between the prezygapophyseal articular facets of the axis in Nacholapithecus. Although the atlas of Nacholapithecus is inferred as having a primitive morphology (i.e., possessing a lateral bridge), the shape of the atlas and axis leads to speculation that locomotion or posture in Nacholapithecus involved more orthograde behavior similar to that of extant apes, and, in so far as cervical vertebral morphology is concerned, it is thought that Nacholapithecus was incipiently specialized toward the characteristics of extant hominoids.

Brief communication: Three-dimensional motion analysis of hindlimb during brachiation in a white-handed gibbon (Hylobates lar).

In brachiating gibbons, it is thought that there is little movement in the hindlimb joints and that lateral body movement is quite limited. These hypotheses are based on naked-eye observations, and no quantitative motion analyses of the hindlimbs have been reported. This study quantitatively describes the three-dimensional movements of the lower trunk and distal thigh during continuous-contact brachiation in a white-handed gibbon (Hylobates lar) to evaluate the roles of the trunk and hindlimb. The results revealed that the lower trunk moved both laterally and vertically. The lateral movement of the lower trunk resulted from the lateral inclination of the trunk by gravity. The vertical movement of the trunk was converted into forward velocity, indicating an exchange between potential and kinetic energy. We also observed flexion and extension of the hip, although the excursion was within a small range. In addition, the lateral movement of the hindlimb in thedirection opposite to that of trunk movement helped to reduce the lateral sway of the body. These results suggest that during continuous-contact brachiation a gibbon uses hip flexion and extension motions to increase the kinetic energy in the swing. In addition, fine motions of the hip may restrict the lateral sway of the center of body mass.

Vertebral morphology of Nacholapithecus kerioi based on KNM-BG 35250.

This paper describes the morphology of the vertebral remains of the KNM-BG 35250 Nacholapithecus kerioi individual from the Middle Miocene of Kenya. Cervical vertebrae are generally large relative to presumed body mass, suggesting a heavy head with large jaws and well-developed neck muscles. The atlas retains the lateral and posterior bridges over the vertebral artery. The axis has a robust dens and a large angle formed by superior articular surfaces. The thoracic vertebral specimens include the diaphragmatic vertebra and one post-diaphragmatic vertebra. The thoracic vertebral bodies are much smaller that those of male Papio cynocephalus, whereas many of the dorsal elements are large and robust, exceeding those of male P. cynocephalus. Lumbar vertebral bodies are small relative to body mass, craniocaudally moderately long, and have a median ventral keel. The transverse process is craniocaudally long and arises from the widest part of the body cranially and the pedicle above the inferior vertebral notch caudally. Anapophyses are present in one of the preserved lumbar vertebrae. The postzygapophyses are thick dorsoventrally. These lumbar features are broadly shared with Proconsul. However, the base of the spinous process is longer and more caudally positioned in N. kerioi compared to Proconsul, and is more similar to the condition in Pongo. They are not dorsally (or moderately caudally) directed as is seen in P. nyanzae, Pan, and most other extant primates. A caudally directed spinous process does not permit a broad range of spinal dorsiflexion. The presumed stiff back in N. kerioi suggests a different locomotor repertoire than in Proconsul. Morotopithecus bishopi, although not possessing the same features, exhibits another morphological suite of characters for lumbar stiffness. Diverse functional adaptations of the lumbar spine were present in African hominoids during the Early to Middle Miocene.

Computerized restoration of nonhomogeneous deformation of a fossil cranium based on bilateral symmetry.

We developed a computerized method of correcting plastic deformation of a fossil skull, based on bilateral symmetry with respect to the midsagittal plane, and applied this method to reconstruction of a fossilized Proconsul heseloni cranium (KNM-RU-7290A). A three-dimensional (3D) model of the fossil was generated using consecutive cross-sectional images retrieved from computed tomography. 3D coordinates of anatomical landmarks that should be located on the midsagittal plane and pairs of landmarks that should be symmetrical with respect to this plane were acquired. These landmarks were then repositioned so that geometrical constraints were satisfied, while translated distances of landmarks were minimized. We adopted a thin-plate spline function to mathematically describe the 3D nonlinear volumetric transformation between acquired and repositioned landmarks. Using this function, the entire fossil shape was transformed, and the effect of reversing the deformation could be visualized. The results indicated that the proposed method was effective in eliminating nonhomogeneous deformation of the fossil skull. The antemortem appearance of the skull cannot be completely restored by this method alone, due to methodological limitations. However, the presented method has a role as an adjunct in complementing conventional restoration techniques on account of its objective nature.

Maxillae and associated gnathodental specimens of Nacholapithecus kerioi, a large-bodied hominoid from Nachola, northern Kenya.

The middle Miocene large-bodied hominoid from Nachola, initially attributed to Kenyapithecus, was recently transferred to a new genus and species Nacholapithecus kerioi. The hypodigm of N. kerioi consists of numerous maxillae, mandibles, and isolated teeth, as well as a number of postcranial bones. A detailed description of the previously discovered postcranial material has already been presented. This article aims to give a detailed description of maxillary specimens (including some mandibular fragments associated with them) of N. kerioi collected by the Japan-Kenya Joint Project team during the field seasons of 1982, 1984, and 1986. The maxillary specimens of N. kerioi retain a set of primitive catarrhine features, such as a relatively shallow palate, low position of the anterior zygomatic root, and the lack of enlarged premolars. Yet, compared to the Early Miocene Proconsul, N. kerioi is derived in having a moderately elongated subnasal clivus that appears to have overlapped the hard palate.

Preliminary analysis of Nacholapithecus scapula and clavicle from Nachola, Kenya.

The Miocene ape Nacholapithecus is known from rather complete skeletons; some of them preserve the shoulder joint, identified by three scapulae and one clavicle. Comparisons made with other Miocene and living apes ( Proconsul, Equatorius, Ugandapithecus) suggest that the mobility of the scapulohumeral joint was important, and scapular features such as the morphology and position of the spine and the morphology of the acromion and axillary border resemble those of climbing arboreal primates except for chimpanzees, gorillas, or orang-utans. From the size of the scapula (male Nasalis size), it is clear that the animal is smaller than an adult chimpanzee, but the clavicle is almost as relatively long as those of chimpanzees. Some features closer to colobine morphology reinforce the hypothesis that Nacholapithecus was probably a good climber and was definitely adapted for an arboreal life.

Nacholapithecus skeleton from the Middle Miocene of Kenya.

An almost entire skeleton of a male individual of Nacholapithecus kerioi (KNM-BG 35250) was discovered from Middle Miocene (approximately 15 Ma) sediments at Nachola, northern Kenya. N. kerioi exhibits a shared derived subnasal morphology with living apes. In many postcranial features, such as articular shape, as well as the number of the lumbar vertebrae, N. kerioi resembles Proconsul heseloni and/or P. nyanzae, and lacks suspensory specializations characteristic of living apes. Similarly, N. kerioi shares some postcranial characters with Kenyapithecus spp. However, despite the resemblance, N. kerioi and Proconsul spp. are quite different in their body proportions and some joint morphologies. N. kerioi has proportionally large forelimb bones and long pedal digits compared to its hindlimb bones and lumbar vertebrae. Its distinctive body proportions suggest that N. kerioi was more derived for forelimb dominated arboreal activities than P. nyanzae and P. heseloni. On the other hand, it exhibits a mixture of derived and primitive cranio-dental and postcranial features relative to the contemporaneous Kenyapithecus and Early MioceneMorotopithecus. While the phylogenetic position of N. kerioi is unsettled, it seems necessary to posit parallel evolution of cranio-dental and/or postcranial features in fossil and living apes.

Comparative and functional anatomy of phalanges in Nacholapithecus kerioi, a Middle Miocene hominoid from northern Kenya.

We describe phalanges of the KNM-BG 35250 Nacholapithecus kerioi skeleton from the Middle Miocene of Kenya. Phalanges of N. kerioi display similarities to those of Proconsul heseloni despite their enhanced robusticity. They do not show highly specialized features as in living suspensory primates. However, N. kerioi manifests several distinctive features that are observed in neither living arboreal quadrupeds nor P. heseloni or P. nyanzae. The most remarkable of them is its phalangeal elongation. N. kerioi phalanges (particularly pedal) are as long as those of Pan despite its much smaller body size. While lengthened digits enable a secure grip of supports and are especially adaptive for grasping large vertical trunks, the skeletal and soft tissues are subjected to greater stress. Probably, strong selective pressures favored powerful hallucal/pollical assisted grips. Although this functional adaptation does not exclude the possible use of the terrestrial environment, arboreal behavioral modes must have been crucial in its positional repertoire. N. kerioi is distinguished from P. heseloni in the greater size of its manual phalanges over its pedal phalanges. These derived features of N. kerioi suggest positional modes supporting more weight on the forelimb, and which occur more frequently on vertical supports. If Proconsul is referred to as an "above-branch arboreal quadruped" with a deliberate and effective climbing capability, N. kerioi may be thought of as an "orthograde climber". While living apes are powerful orthograde climbers, they are also more or less suspensory specialists. Suspensory behavior (plus climbing) and pronograde quadrupedalism (plus climbing) are the two main arboreal behavioral adaptations in living anthropoids. Thus, N. kerioi is an unusual fossil primate in that it cannot be incorporated into this dichotomy. It is plausible that a N. kerioi-like orthograde climber with large forelimbs and cheiridia was a precursor of suspensory living apes, and N. kerioi may demonstrate what an initial hominoid of this grade might have looked like.