The functional role of the gluteus medius differs between extant humans and other primates. In nonhuman primates, the muscle rotates the pelvis in the horizontal plane and assists forelimb reach. By contrast, in humans, it pulls the pelvis upward in the frontal plane and contributes to mediolateral stability during bipedal gait. In the earliest evolutionary stage of bipedalism, however, a functional flexibility would have been required to cope with both bipedalism and locomotion using all four limbs. This study conducted a moment arm analysis based on a model-kinematics matching approach in Japanese macaques (Macaca fuscata), which lack any morphological adaptations for bipedalism. We hypothesized that it was postural change itself that triggered the functional transition of the gluteus medius. The primary action of the gluteus medius was found to shift from medial rotation to abduction with a change from quadrupedal to bipedal walking. This is likely to have been caused by a change in the geometric relationship between the muscular force vector and femoral orientation. This indicates that the gluteus medius has the faculties to change its action regardless of iliac morphology while also suggesting that the behavioral changes preceded morphological adaptations in the evolutionary process of the hip abductor apparatus. In the earliest evolutionary stage, a versatile gluteus medius likely facilitated mediolaterally stable bipedal gaits while ensuring the kinematic demands of quadrupedal locomotion, which led to a seamless locomotor transition to bipedalism.

The vocal membrane, an extended part of the vocal fold, is present in a broad range of species including non-human primates. Its contribution to animal vocalizations has long been of interest. A theoretical study (Mergell P, Fitch T, Herzel H. 1999 Modeling the role of nonhuman vocal membranes in phonation. J. Acoust. Soc. Am. 105, 2020-2028. (https://doi.org/10.1121/1.424994)) predicted that vocal membranes enhance vocal efficiency by lowering the phonation threshold pressure. To test this, excised larynx experiments were conducted on rhesus macaques (Macaca mulatta). Comparisons before and after surgical removal of the vocal membranes showed that the phonation threshold pressure was indeed lower-and vocal efficiency higher-when the vocal membranes were present. Most experiments exhibited periodic oscillations of the vocal folds and/or membranes, while some showed irregular broadband oscillations potentially indicative of chaos. A computational model representing the vocal membrane as a dynamic, reed-like plate reproduced both periodic and irregular oscillations, depending on parameter settings such as the damping ratio. These simulations suggest that transitions between different regimes can arise from individual anatomical or physiological variation. Although this pilot study is based on two macaque larynges, the results support the idea that vocal membranes may contribute to vocal efficiency and dynamic variability, potentially enabling louder calls with less pulmonary effort.

We investigated the causal basis of abrupt frequency jumps in a unique database of New World monkey vocalizations. We used a combination of acoustic and electroglottographic recordings in vivo, excised larynx investigations of vocal fold dynamics, and computational modelling. We particularly attended to the contribution of the vocal membranes: thin upward extensions of the vocal folds found in most primates but absent in humans. In three of the six investigated species, we observed two distinct modes of vocal fold vibration. The first, involving vocal fold vibration alone, produced low-frequency oscillations, and is analogous to that underlying human phonation. The second, incorporating the vocal membranes, resulted in much higher-frequency oscillation. Abrupt fundamental frequency shifts were observed in all three datasets. While these data are reminiscent of the rapid transitions in frequency observed in certain human singing styles (e.g. yodelling), the frequency jumps are considerably larger in the nonhuman primates studied. Our data suggest that peripheral modifications of vocal anatomy provide an important source of variability and complexity in the vocal repertoires of nonhuman primates. We further propose that the call repertoire is crucially related to a species' ability to vocalize with different laryngeal mechanisms, analogous to human vocal registers. This article is part of the theme issue 'Nonlinear phenomena in vertebrate vocalizations: mechanisms and communicative functions'.

The vocal membrane, i.e., an extended part of the vocal fold, is present in non-human primates. To understand its function in animal vocalization, Mergell et al. (1999) constructed a mathematical model of the vocal membrane and predicted that the vocal membrane lowers the phonation threshold pressure required to initiate the vocal fold oscillations. The present study constructed a physical model of the vocal membrane based on a micro-computed tomography measurement of a rhesus macaque larynx. Our physical experiment confirmed that the phonation threshold pressure was indeed lowered and, consequently, the vocal efficiency was increased by the vocal membrane.

Adult male proboscis monkeys, Nasalis larvatus, develop an enlarged external nose. Males often produce loud, long-distance calls filtered through the nasal passage. The enlarged nose probably functions as a visual badge of social status and a visual key representing the owner's physical and sexual quality, and thus is useful for females in selecting mates. In addition to such visual signalling, a larger external nose enhances the lower frequencies in calls, possibly exaggerating acoustic signals related to body size. Here, we used computational simulations with three-dimensional models of the nasal passage to show how the external nose modifies the acoustic property, indicating that the external nose develops to enhance lower frequencies in adults but varies in a specific formant position among adult males. This finding suggests that the external nose generates acoustic signals about physical-sexual maturity in adult males and individual identity among them. The unusual features of the social organization in this species, a patrilineality of a multilevel community consisting of one-male-multi-female units, may reinforce the functional importance of individual male recognition for males and females to monitor the location of both their own units and those of other males.

OBJECTIVES:An adequate understanding of the evolution of the larynx presumably clarify the physiology and functional histoanatomy of the present-day human organ. This study investigated the comparative histoanatomy of the epiglottis and preepiglottic space of the lemur larynx (a non-human primate without vocal tract). METHODS:Two normal adult ring-tailed lemur larynges obtained from natural death were investigated. The whole organ serial section technique was employed. RESULTS:The histologic structures of the lemur epiglottis and preepiglottic space differed considerably from that of human adults. The lemur epiglottis was proportionally thick and vertical. It was connected to the thyroid cartilage anteroinferiorly without an intervening thyroepiglottic ligament and to the hyoid bone anteriorly with intervening large bundles of collagen fibers, indicating that the lemur epiglottis does not play the role of retroflection. The lemur larynges did not have a preepiglottic space. These findings also reflect the fact that lemurs do not have a descended larynx and do not acquire the pharyngeal space of the vocal tract. The lemur epiglottis was composed of fibrocartilage, adipose tissue and a small amount of elastic cartilage covered with mucosa (lamina propria and pseudostratified ciliated columnar epithelium). The histologic findings also indicate that the lemur epiglottis is not flexible and does not play the role of retroflection. CONCLUSIONS:The results of this study are consistent with the hypothesis that, in the process of evolution, the histologic structures of epiglottis and preepiglottic space likely change to make the larynx descend and lengthen the pharyngeal space of the vocal tract for speech production in humans. Moreover, the distribution of the human preepiglottic space likely allows the epiglottis to more effectively play the role of retroflection during swallowing in order to prevent aspiration.

OBJECTIVES:Comparative histoanatomy regarding the evolution of epiglottis and preepiglottic space (PES) of primate larynx as the supralaryngeal vocal tract (SVT) is acquired was investigated. METHODS:Two lemur, one galago, two macaque, two gorilla, and two chimpanzee normal larynges were investigated and compared with human larynges using the whole-organ serial section technique. RESULTS:Nonhuman primates with the limited pharyngeal space of SVT (lemurs, galago, and macaques, phyletic distant relative of humans) did not have PES. Their epiglottis was composed of cartilage that is not very flexible. Nonhuman primates with the lengthened pharyngeal space of SVT (gorillas and chimpanzees, hominids, phyletic close relative of humans) had PES. Furthermore, the PES of chimpanzees (phyletic closest relative of humans) existed astride the epiglottis similar to the human PES. The hominid epiglottises were composed of elastic cartilage, which is flexible, and play the role of retroflection. These histoanatomical structures of the epiglottis and PES reflect the fact that those features evolved as the pharyngeal space of SVT was lengthened. CONCLUSIONS:The results of this study are consistent with the hypothesis that, in the process of evolution, the histoanatomical structures of epiglottis and PES changed and allowed the larynx to descend and the pharyngeal space of the SVT to be lengthened. This may facilitate speech production in humans. Moreover, the distribution of the human PES allows the epiglottis to more effectively play the role of retroflection during swallowing in order to prevent aspiration, which may have been derived from primate swallowing physiology.

Primates have varied vocal repertoires to communicate with conspecifics and sometimes other species. The larynx has a central role in vocal source generation, where a pair of vocal folds vibrates to modify the air flow. Here, we show that Madagascan lemurs have a unique additional pair of folds in the vestibular region, parallel to the vocal folds. The additional fold has a rigid body of a vocal muscle branch and it is covered by a stratified squamous epithelium, equal to those of the vocal fold. Such anatomical features support the hypothesis that it also vibrates in a manner like the vibrations that occur in the vocal folds. To examine the acoustic function of the two pairs of folds, we made a silicone compound model to demonstrate that they can simultaneously vibrate to lower the fundamental frequency and increase vocal efficiency. Similar acoustic effects are achieved using different features of the larynx for the other primates, e.g., by vibrating multiple sets of ventricular folds in several species and further by an evolutionary modification of enlarged larynx in howler monkeys. Our multidisciplinary approaches found that these functions were acquired through a unique evolutionary adaptation of the twin vocal folds in Madagascan lemurs.

The tongue plays a major role in speech production. Comparisons of the tongue muscle fiber architecture between humans and nonhuman primates are required to understand the evolutionary acquisition of tongue deformability in human speech. In this study, we performed diffusion-weighted imaging of flash-frozen tongue specimens from macaques, a representative animal model, to visualize the three-dimensional architecture of the intrinsic muscles. The procedures and scanning methods used in this study can also be applied to non-model animals, and are expected to provide quantified data for their tongue architecture to understand the evolutionarily derived features of human tongue deformability.

The genus Macaca includes medium-to large-bodied monkeys and represents one of the most diverse primate genera, also having a very large geographic range. Nowadays, wild macaque populations are found in Asia and Africa, inhabiting a wide array of habitats. Fossil macaques were also present in Europe from the Late Miocene until the Late Pleistocene. Macaques are considered ecologically flexible monkeys that exhibit highly opportunistic dietary strategies, which may have been critical to their evolutionary success. Nevertheless, available ecological information regarding fossil European species is very sparse, limiting our knowledge of their evolutionary history in this geographic area. To further our understanding of fossil European macaque ecology, we investigated the dietary ecology of Macaca majori, an insular endemic species from Sardinia. In particular, we characterized the dental capabilities and potential dietary adaptations of M. majori through dental topographic and enamel thickness analyses of two M(2)s from the Early Pleistocene site of Capo Figari (1.8 Ma). We also assessed its diet through dental microwear texture analysis, while the microwear texture of M. majori was also compared with microwear textures from other European fossil macaques from mainland Europe. The dental topographic and enamel thickness analyses suggest that M. majori frequently consumes hard/mechanically challenging and/or abrasive foods. The results of the dental microwear analysis are consistent with this interpretation and further suggest that M. majori probably exhibited more durophagous dietary habits than mainland Plio-Pleistocene macaques. Overall, our results indicate that M. majori probably occupied a different dietary niche compared to its mainland fossil relatives, which suggests that they may have inhabited different paleoenvironments.

OBJECTIVES:Understanding of the evolution of the larynx clarifies the physiology and functional histoanatomy of the present-day human organ. Comparative histoanatomy of the epiglottis and pre-epiglottic space of the chimpanzee larynx (a hominid, phyletic closest relative of humans) was investigated. METHODS:Two normal adult chimpanzee larynges obtained from natural deaths were investigated. The whole organ serial section technique was employed. RESULTS:The histoanatomical structures of the chimpanzees' epiglottis and pre-epiglottic space were considerably similar to those of human adults. The chimpanzees' epiglottic cartilage was relatively thin and composed of elastic cartilage. These histologic findings of epiglottis indicate that the chimpanzee's epiglottis is flexible and plays the role of retroflection. The chimpanzees' larynges had a pre-epiglottic space composed of adipose tissue and loose connective tissue. Epiglottic cartilage was connected to the thyroid cartilage anteroinferiorly with an intervening thyroepiglottic ligament and to the hyoid bone anteriorly with an intervening hyoepiglottic ligament. These histoanatomical structures of the epiglottis and pre-epiglottic space reflect the fact that chimpanzees have a descended larynx and acquire the pharyngeal space of the vocal tract. CONCLUSION:The results of this study are consistent with the hypothesis that, in the process of evolution, the histoanatomical structures of the epiglottis and pre-epiglottic space change and allow the larynx to descend and lengthen the pharyngeal space of the vocal tract which facilitates speech production in humans. Moreover, the distribution of the human pre-epiglottic space likely allows the epiglottis to more effectively play the role of retroflection during swallowing in order to prevent aspiration.

We carried out ex vivo and in vivo experiments to explore the functional role of the ventricular folds in sound production in macaques. In the ex vivo experiments, 29 recordings out of 67 showed that the ventricular folds co-oscillated with the vocal folds. Transitions from normal vocal fold oscillations to vocal-ventricular fold co-oscillations as well as chaotic irregular oscillations were also observed. The in vivo experiments indicated that the vocal-ventricular fold co-oscillations were also observed in two macaque individuals. In both ex vivo and in vivo experiments, the vocal-ventricular fold co-oscillations significantly lowered the fundamental frequency. A mathematical model revealed that the lowering of the fundamental frequency was caused by a low oscillation frequency inherent in the ventricular folds, which entrained the vocal folds to their low-frequency oscillations. From a physiological standpoint, the macaques may utilize the ventricular fold oscillations more frequently than humans. The advantages as well as disadvantages of using the ventricular folds as an additional vocal repertory are discussed.

音声言語の起源と進化は，人類進化のなかでも未解明な部分が多く残されたラストフロンティアである．ヒトは，多様な音素を一息の中で連続的に連ねて言語コミュニケーションをするが，サル類は，声の大きさや高さ，長さなどを手掛かりに音声コミュニケーションする．音声は，声帯振動により作られる音源により，声道空間が共鳴して，発せられる．ヒトは，長い咽頭腔と短い口腔からなる声道をもち，声道形状の変化を高度に制御して，意図した音素を繰り出す．また，声帯膜を喪失した単純な声帯により，安定した声帯振動を長く維持することができるので，その音素の変化を正しく伝える．サル類は，静的な声道形状で，声帯膜により発声の経済性が上がるものの，音源の安定性を欠く．ヒトの音声言語は，原初から，対面で届く範囲の相手に，音素の連なりを安定して届けるコミュニケーション形態として起源したのだろう．

Pelvic morphology exhibits a particular sexual dimorphism in humans, which reflects obstetrical constraints due to the tight fit between neonates and mothers. Huseynov et al. [Proc. Natl. Acad. Sci. U.S.A. 113, 5227-5232 (2016)] showed that in humans, pelvic sexual dimorphism is greatest around the age of highest fertility, and it becomes less marked in association with menopause in females. They proposed that this reflects changes of obstetrical versus locomotor functional demands in females. It remains unknown whether such developmental adjustment of the pelvic morphology is unique to humans. Macaques exhibit human-like cephalopelvic proportions, but they lack menopause and usually maintain fertility throughout adulthood. Here, we track pelvic development in Japanese macaques from neonate to advanced ages using computed tomography-based data. We show that female pelvic morphology changes throughout adult life, reaching the obstetrically most favorable shape at advanced ages rather than around primiparity. We hypothesize that pelvic morphology in Japanese macaques is developmentally adjusted to childbirth at advanced ages, where obstetrical risks are potentially higher than at younger ages. Our data contribute to the growing evidence that the female primate pelvis changes its morphology during the whole lifespan, possibly adjusting for changing functional demands during adulthood.

Mandibular morphology is determined not only by dietary habits, but also by sexual selection and allometry in primates. It is well-known that African papionins show intra- and interspecific variations through varied extensions of a common ontogenetic allometric trajectory in the face. Here, we used geometric morphometrics to compare the ontogenetic trajectories of large-bodied Japanese macaques and small-bodied long-tailed macaques in the sister clade of African papionins. The two species showed a major common allometric trend that was comparable to that of African papionins, but the allometric trajectory was transposed parallel to each other with few interspecies differences in mandibular shape. A minor allometric trend occurred before the eruption of the first molar. During extensino of this allometric trend in Japanese macaques, mandibular shape becomes mechanically suitable for processing tough food items in their dietary repertoire in winter. The decoupling of size and shape in the major allometric trend can allow for adaptive modifications in mandibular shape, which in turn may play a central role in speciation in macaques. Compared to other African papionins, macaques are widely distributed in temperate areas and have survived in fluctuating climates and habitats. Thus, evolutionary modifications that occur in different ontogenetic bases can result in variations in size and shape that are uniquely adaptive for a given clade.

In humans, obstetrical difficulties arise from the large head and broad shoulders of the neonate relative to the maternal birth canal. Various characteristics of human cranial development, such as the relatively small head of neonates compared with adults and the delayed fusion of the metopic suture, have been suggested to reflect developmental adaptations to obstetrical constraints. On the other hand, it remains unknown whether the shoulders of humans also exhibit developmental features reflecting obstetrical adaptation. Here we address this question by tracking the development of shoulder width from fetal to adult stages in humans, chimpanzees, and Japanese macaques. Compared with nonhuman primates, shoulder development in humans follows a different trajectory, exhibiting reduced growth relative to trunk length before birth and enhanced growth after birth. This indicates that the perinatal developmental characteristics of the shoulders likely evolved to ease obstetrical difficulties such as shoulder dystocia in humans.

Human speech production obeys the same acoustic principles as vocal production in other animals but has distinctive features: A stable vocal source is filtered by rapidly changing formant frequencies. To understand speech evolution, we examined a wide range of primates, combining observations of phonation with mathematical modeling. We found that source stability relies upon simplifications in laryngeal anatomy, specifically the loss of air sacs and vocal membranes. We conclude that the evolutionary loss of vocal membranes allows human speech to mostly avoid the spontaneous nonlinear phenomena and acoustic chaos common in other primate vocalizations. This loss allows our larynx to produce stable, harmonic-rich phonation, ideally highlighting formant changes that convey most phonetic information. Paradoxically, the increased complexity of human spoken language thus followed simplification of our laryngeal anatomy.

Objectives Morphometrics has played essential roles in the comprehension of biological variation and the evolution of morphological phenotypes. This approach usually imposes strict requirements on data, such as rigid alignment of subjects, and the collection and manual preprocessing of data meeting these requirements are often time consuming. Artificial intelligence (AI) technology is developing and it potentially reduces this load, but they usually presuppose the availability of "big data" for successful learning, beyond the empirically plausible amount in biological studies. Here, we propose a deep learning-based analysis of three-dimensional data. Materials and Methods We built a deep learning-based analysis of three-dimensional morphological data that does not require strict alignment or an implausible sample size. We benchmarked the proposed method by case studying sex classification of macaques, referring to computed tomography scans of their mandible. Results The model learned from just 139 mandible specimens of Japanese macaques and successfully generalized the learned classification to previously unseen specimens of the same species and even other species of macaques. Moreover, we visualized those characteristic regions in the data that the model used during sex classification and showed that they were consistent with the criteria used by human experts. Discussion Our analysis does not require rigidly aligned data, so can effectively use data collected in previous studies with different focus/aims. This proposed AI method can potentially help researchers to discover new morphological features of different species and other biological groups. Implementation of this proposed AI system will be available to other researchers for further investigation.

The vocal membrane, i.e., an extended part of the vocal fold, is observed in a wide range of species including bats and primates. A theoretical study [Mergell, Fitch, and Herzel (1999). J. Acoust. Soc. Am. 105(3), 2020–2028] predicted that the vocal membranes can make the animal vocalizations more efficient by lowering the phonation threshold pressure. To examine this prediction, a synthetic model of the vocal membrane was developed, and its oscillation properties were examined. The experiments revealed that the phonation threshold pressure was lower in the vocal membrane model compared to that in a model with no vocal membrane. Chaotic oscillations were observed as well.

Up to the mid-1990's, only a few remains of Cercopithecoidea were known from the Lukeino Formation (Tugen Hills, Kenya). Surveys from 1998 onwards by the Kenya Palaeontology Expedition led to the discovery of new material at Aragai, a site situated in the lower levels of the Lukeino Formation dated at c. 6-5.8 Ma. Most of the collection consists of craniodental specimens generally well-preserved in a hard matrix but there are three postcranial bones. A new taxon of fossil colobine monkey is described: Sawecolobus lukeinoensis n. gen., n. sp. It is a small to medium-sized, short-faced colobine. Sawecolobus n. gen. shares many features with Cercopithecoides Mollett, 1947, especially in the face and the calvarium, but differs from it by the less pronounced supraorbital tori. The two genera differ greatly in mandibular morphology. In Sawecolobus n. gen. the mandibular corpus is slender and not robust as in Cercopithecoides Mollett, 1947, and the anterior surface of its symphysis is inclined posteriorly and not vertical. The numerous new specimens from the Lukeino Formation contribute to our understanding of the local diversity of Miocene Cercopithecoidea and fill out the distribution of the superfamily in the continent for the same period.