RESUMEN

We performed whole-exome sequencing using a human exome capture kit to analyze the potential genetic factors related to patent ductus arteriosus in Japanese macaques. Compared with the reference sequences of other primates, we identified potential missense variants in five genes: ADAM15, AZGP1, CSPG4, TNFRSF13B, and EPOR.

Asunto(s)

RESUMEN

In this essay, I summarize my research career, with reference to the early days of the Laboratory of Physical Anthropology (LPA) at Kyoto University led by Kinji Imanishi and Junichiro Itani. When I started conducting research on the sexual behavior of Japanese macaques in 1975, I made some unexpected observations. High-ranking males did not obtain high mating success. Estrous females often rejected the courtships of high-ranking males and chose to mate with lower-ranking males. Some male-female dyads exhibited long-lasting affinitive relations, but they avoided mating. Females frequently showed 'excessive' sexuality. Clear explanations for some of these observations do not exist. After that, I changed my study subjects several times from chimpanzees, Yakushima macaques (a subspecies of Japanese macaque), and ringtailed lemurs. It is difficult to summarize my findings into a consistent story. Instead, I review my research and experiences. Throughout my career, I kept two things in mind. The first was established by Imanishi at the Laboratory of Physical Anthropology at Kyoto University: to explore the evolution of human society. Second, I tried to understand seemingly incomprehensible phenomena using evolutionary theory. Despite adhering to these foundational concepts, things did not always work out as planned.

Asunto(s)

RESUMEN

Animals often initiate social interactions by exchanging signals. Especially when initiating amicable interactions, signaling one's friendly stance toward others in advance may be important to avoid being misunderstood as having hostile intentions. We used data on dyadic play fighting in a group of Japanese macaques, Macaca fuscata, to examine the function of "play face" at the opening of a play session. We found no support for the previously proposed hypothesis that play face expression is likelier before entering risky situations (e.g., before gaining an undue advantage over the partner) to avoid being misunderstood. The results showed that play face expression was likelier in male juveniles before initiating play with other males than in females before initiating play with males or other females and that juveniles were likelier to express play face before initiating play with others closer in age. As male Japanese macaques play more frequently than females, and juveniles prefer to play with individuals closer in age, play face expression before play initiation may reflect the individual's motivation for subsequent play interactions. This interpretation is supported by our observation that play bouts lasted longer when initiated with bidirectional play face by both participants than when initiated without play face. We also argued that since there was no tendency that play face was likelier to be expressed toward individuals with low play propensity (e.g., females) or infrequent partners to play with (e.g., individuals more distant in age), Japanese macaques may not tactically deploy this signal to recruit reluctant partners.

Asunto(s)

RESUMEN

Non-human primates are important models for investigations of neural development and evolution, and the use of Japanese macaque monkeys has especially contributed to the advancement of neuroscience studies. However, these studies are restricted by the number of animals able to be evaluated and the invasiveness of the methodologies. Induced pluripotent stem cells (iPSCs) can provide an alternative strategy for investigating neural development in vitro. We have established direct neurosphere (dNS) formation cultures of primate iPSCs as an in vitro model of early neurodevelopment in primate species. Here, we used dNS formation and neuronal differentiation cultures established from Japanese macaque iPSCs (jm-iPSCs) to investigate the usefulness of these cells as an in vitro model of early neural development. Time-course analyses of developmental potency and gene expression kinetics were performed during dNS formation culture of jm-iPSCs. During a 1-week culture, jm-iPSC-derived dNSs became neurogenic by day 3 and underwent stepwise expression changes of key developmental regulators along early neural development in a similar manner to chimpanzee dNS formation previously reported. Meanwhile, a subset of genes, including CYP26A1 and NPTX1, showed differential expression propensity in Japanese macaque, chimpanzee, and human iPSC-derived dNSs. Spontaneous upregulation of NOTCH signaling-associated genes HES5 and DLL1 was also observed in neuronal differentiation cultures of Japanese macaque but not chimpanzee dNSs, possibly reflecting the earlier neurogenic competence in Japanese macaques. The use of jm-iPSCs provides an alternative approach to neurological studies of primate development. Furthermore, jm-iPSCs can be used to investigate species differences in early neural development that are key to primate evolution.

Asunto(s)

RESUMEN

The relationship between the lumbosacral plexus (LSP) origin and the 12th rib length was recently determined in humans; cranial and caudal deviations of the plexus origin are related to shortening and elongation of the 12th rib, respectively. However, it remains unclear whether such anatomical correlations are also observed in non-human mammals. To address this issue, in the present study, we evaluated the LSP origin and the 12th rib length in Japanese macaques (Macaca fuscata). In typical cases, the femoral and obturator nerves were derived from both the 4th and 5th lumbar nerves, and the lumbosacral trunk was from the 5th to 7th lumbar nerves. Some of the LSPs exhibited a caudal deviation of their origins; the femoral and obturator nerves were also derived from the 6th lumbar nerve, in addition to the 4th and 5th lumbar nerves; the lumbosacral trunk lost the 5th lumbar nerve origin and arose from the 6th and 7th lumbar nerves. Individuals with the caudal deviation of LSP origin exhibited significant elongation of the 12th ribs, in comparison with individuals with the typical plexus. The present findings indicate that the caudal deviation of LSP origin was correlated to the 12th rib elongation in Japanese macaques, similar to humans. As a future studies, we need to clarify which mammalian groups exhibit such correlation between the deviation of the LSP origin and the lowest rib length, and further to provide evolutionary implications of this correlation.

Asunto(s)

RESUMEN

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.

Asunto(s)

RESUMEN

In this paper, I describe my 62 years in primatology focusing on some of the key findings from fieldwork conducted in Japan, India, and Africa. My first study on nonhuman primates described in detail the division of a troop of Japanese macaques at Takasakiyama. After that, I had an opportunity to work on Hanuman langurs at Dharwar, India. These langurs lived in one-male, multi-female groups. This type of group structure was maintained through takeovers by all-male parties. The adult male and all juvenile males were chased out of the group. By this process, the one-male, multi-female group system was maintained. The incoming adult male bit and killed all infants in the group. Mothers who lost their infants went into estrus and mated with the newly arrived male. For many years, scientists ignored these events or ruled them out as abnormal behavior. My work on Japanese macaques suggested that concentrated resources created by artificial feeding exaggerated dominance rank hierarchies among individuals, whereas it is comparatively relaxed in the natural environment. I also investigated the population dynamics of a troop and the life histories of individuals. From these studies, I documented the frequency of twin births, the carrying of dead infants by mothers, and the occurrence of physical malformations. These observations were made possible through artificial feeding, revealing the merits and demerits of this approach. I pointed out that authors and journal editors must be careful to acknowledge important elements of the environment where studies are conducted, and these should be described when reporting results in scientific articles. My studies of chimpanzees were conducted at Bossou, Guinea. I suggested that there are males who lived outside of bisexual groups. Chimpanzees in this population made and used many kinds of tools. Some of them were observed only at Bossou, and a few were only discovered 20 years after the establishment of Bossou as a research site. After decades of research on tool use in this species, I also suggested that there are cultural zones throughout the geographic distribution of chimpanzees.

Asunto(s)

RESUMEN

Improving captive environments for primates has been an important tool to enhance animal welfare. One method has been to provide primates with naturalistic vegetated enclosures to promote species-specific behaviors, enhancing interactions with their social and natural environment, such as an increase in feeding, foraging, and positive social behaviors such as play. To investigate the benefits in which living in naturalistic environments promote general animal well-being, we observed immature and adult males living in two outdoor housed groups of Japanese macaques (Macaca fuscata) in the Kyoto University Primate Research Institute (KUPRI), Inuyama, Japan, from June of 2015 until June 2016. One enclosure was naturally vegetated and the other was not. We recorded male activity budgets, affiliative (groom, play) behaviors, and rates of agonistic interactions. To examine health status, we recorded and compared coat conditions for both groups. We found that males in the vegetated enclosure spent more time in social play than males in the non-vegetated enclosure, while males in the non-vegetated enclosure displayed more stereotypic behaviors and agonistic interactions. We recorded better coat conditions in the vegetated enclosure males while rates of social grooming or self-grooming were no different between males in the two enclosures. The males in the vegetated enclosure did not have activity budgets more similar to their wild counterparts; but they spent more time in feeding-related activities and less time resting, which was more similar to their wild counterparts than males in the non-vegetated enclosure. Our findings suggest that individuals housed in naturalistic environments have significantly greater behavioral and physical markers of wellbeing than those housed in unnatural, large outdoor enclosures. Although we found that males in both types of enclosures overall had similar time budgets to males in the wild, the detailed behavioral and health results suggest that the welfare benefits to males were greater in the vegetated enclosure, compared with non-vegetated enclosures. Efforts to mimic more natural environments should promote the well-being of primates.

Asunto(s)

RESUMEN

A 7.5-year-old intact male Japanese macaque was presented for evaluation of vision loss. After a complete ophthalmic examination, the patient was diagnosed with hypermature cataract in both eyes. After the cataract surgery, it was able to locate food and walk in a straight line.

RESUMEN

Primates are popular species in wildlife tourism contexts and provide economic benefits to habitat countries where primate-based tourism activities are a part of the country's tourism economy. Primate tourism runs a broad gamut from safari-like expeditions within remote primate habitats to designated monkey parks and incidental primate tourism. In most forms of primate tourism, primate ecology and behaviour are directly influenced by humans, making these interfaces particularly relevant for examination using the lens of ethnoprimatology. While several studies have assessed the impact of tourism on primates, little is known about people's motivations for observing monkeys for recreational purposes. Here we present two case studies-the Jigokudani Monkey Park, Japan, and the Telaga Warna Nature Recreational Park, Indonesia-where we provide quantitative assessments of people's motivations for visiting managed (monkey parks) and unmanaged (incidental) monkey tourism sites. We further show that management regimes, socio-demographic attributes, previous experience of interactions with macaques, and feeding them play a role in people's desire to visit macaque tourism sites. In Japan, those who had interacted with macaques before were more likely to visit the park to observe macaques clearly and at close quarters. In contrast, respondents in Indonesia were more interested in the recreational opportunities offered by the nature reserve rather than in macaques. However, here too, people who had interacted with macaques earlier were more likely to visit incidental macaque tourist sites for the sole purpose of viewing or interacting with macaques. Almost 50% of the Japanese respondents visited the monkey park due to personal inclinations, while less than 14% of people in Indonesia visited the park of their own volition. Also, over 57% of the Japanese respondents said that visiting monkey parks helped them gain a better understanding of macaque behaviour, whereas only about 26% respondents said likewise in Indonesia. Unlike the Japanese respondents, most of the Indonesian respondents engaged in feeding macaques. These findings suggest that management regimes as well as socio-demographic attributes may influence people's motivations to visit macaque tourism sites.

Asunto(s)

RESUMEN

Translational research often requires the testing of experimental therapies in primates, but research in non-human primates is now stringently controlled by law around the world. Tissues fixed in formaldehyde without glutaraldehyde have been thought to be inappropriate for use in electron microscopic analysis, particularly those of the brain. Here we report the immunoelectron microscopic characterization of arginine vasopressin (AVP)-producing neurons in macaque hypothalamo-pituitary axis tissues fixed by perfusion with 4% formaldehyde and stored at -25 °C for several years (4-6 years). The size difference of dense-cored vesicles between magnocellular and parvocellular AVP neurons was detectable in their cell bodies and perivascular nerve endings located, respectively, in the posterior pituitary and median eminence. Furthermore, glutamate and the vesicular glutamate transporter 2 could be colocalized with AVP in perivascular nerve endings of both the posterior pituitary and the external layer of the median eminence, suggesting that both magnocellular and parvocellular AVP neurons are glutamatergic in primates. Both ultrastructure and immunoreactivity can therefore be sufficiently preserved in macaque brain tissues stored long-term, initially for light microscopy. Taken together, these results suggest that this methodology could be applied to the human post-mortem brain and be very useful in translational research.

Asunto(s)

RESUMEN

Mammalian faeces can be collected noninvasively during field research and provide valuable information on the ecology and evolution of the source individuals. Undigested food remains, genome/metagenome, steroid hormones, and stable isotopes obtained from faecal samples provide evidence on diet, host/symbiont genetics, and physiological status of the individuals. However, proteins in mammalian faeces have hardly been studied, which hinders the molecular investigations into the behaviour and physiology of the source individuals. Here, we apply mass spectrometry-based proteomics to faecal samples (n = 10), collected from infant, juvenile, and adult captive Japanese macaques (Macaca fuscata), to describe the proteomes of the source individual, of the food it consumed, and its intestinal microbes. The results show that faecal proteomics is a useful method to: (i) investigate dietary changes along with breastfeeding and weaning, (ii) reveal the taxonomic and histological origin of the food items consumed, and (iii) estimate physiological status inside intestinal tracts. These types of insights are difficult or impossible to obtain through other molecular approaches. Most mammalian species are facing extinction risk and there is an urgent need to obtain knowledge on their ecology and evolution for better conservation strategy. The faecal proteomics framework we present here is easily applicable to wild settings and other mammalian species, and provides direct evidence of their behaviour and physiology.

Asunto(s)

RESUMEN

Tumors of urinary origin are infrequently reported in non-human primates. Urothelial carcinoma involving the urinary bladder was diagnosed in an adult female Japanese macaque that extended transmurally to the uterus and cervix. To our knowledge, this is the first report of a primary cystic urothelial carcinoma in a Japanese macaque.

Asunto(s)

RESUMEN

Objective.Advances in brain-machine interfaces (BMIs) are expected to support patients with movement disorders. Electrocorticogram (ECoG) measures electrophysiological activities over a large area using a low-invasive flexible sheet placed on the cortex. ECoG has been considered as a feasible signal source of the clinical BMI device. To capture neural activities more precisely, the feasibility of higher-density arrays has been investigated. However, currently, the number of electrodes is limited to approximately 300 due to wiring difficulties, device size, and system costs.Approach.We developed a high-density recording system with a large coverage (14 × 7 mm2) and using 1152 electrodes by directly integrating dedicated flexible arrays with the neural-recording application-specific integrated circuits and their interposers.Main results.Comparative experiments with a 128-channel array demonstrated that the proposed device could delineate the entire digit representation of a nonhuman primate. Subsampling analysis revealed that higher-amplitude signals can be measured using higher-density arrays.Significance.We expect that the proposed system that simultaneously establishes large-scale sampling, high temporal-precision of electrophysiology, and high spatial resolution comparable to optical imaging will be suitable for next-generation brain-sensing technology.

Asunto(s)

RESUMEN

Fecal particle size provides important information on the feeding and digestion of herbivores. Understanding the effects of the potential proximate determinants on fecal particle size helps us interpret this widely used measurement. In folivores, previous studies found that diet composition, dietary toughness, and age-sex-related factors, such as body size and tooth wear, influenced fecal particle size. However, the role of these factors remains unknown in frugivorous and omnivorous primates. This study aims to clarify how age-sex class and diet influence fecal particle size in omnivorous Japanese macaques in Yakushima. We expected that their variable diet and differences among age-sex classes would cause variations in fecal particle size. We simultaneously documented Japanese macaques' diet, dietary toughness, and fecal particle size in the lowland area of Yakushima in the period from March 2018 to April 2019. Unexpectedly, fecal particle size showed limited differences across months and no difference among age-sex classes. Dietary toughness showed no effects on fecal particle size, while the consumption of fruits showed only a marginally significant negative effect. Our data indicate that the results of chewing were not affected by dietary toughness in our study subjects, while age-sex classes showed no difference in food comminution. This lack of variation might derive from a diet with low dietary toughness. We also found that the physical structure of preferred foods played an important role in fecal particle size variations. These results suggest that food comminution is less variable in frugivorous and omnivorous primates compared to highly specialized species (e.g., geladas). Factors other than what we examined in this study, such as food physical structure and chewing behavior, should also be taken into consideration.

Asunto(s)

RESUMEN

The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

Asunto(s)

RESUMEN

Animals show various forms of behavioral thermoregulation to minimize cold stress. Given that higher dominance rank is often associated with increased fitness in group-living animals, higher-ranking individuals may also benefit from better access to thermally optimal spatial positions within huddles. This study examined the association between dominance rank and the potential thermoregulatory benefits of huddling behavior in Japanese macaques (Macaca fuscata) inhabiting Shodoshima Island, which form exceptionally large huddles. I photographed monkey huddles, and analyzed the number of individuals that males were in contact with and males' spatial positons in huddles. Higher-ranking males were significantly more likely to be in contact with larger numbers of individuals in huddles. Higher-ranking males occupied non-peripheral positions in huddles more often than lower-ranking males, which put them in contact with larger numbers of individuals. These results suggest that high dominance rank may confer potential thermal advantages on male Japanese macaques. The mechanism for this is likely that the highest-ranking male often intrude in already-formed huddles, although such behaviors of males were not quantitatively assessed. This study contributes to a better understanding of the mechanisms of cold adaptation in relation to dominance rank in group-living animals.

Asunto(s)

RESUMEN

Non-human primates are our closest relatives and therefore offer valuable comparative models for human evolutionary studies and biomedical research. As such, Japanese macaques (Macaca fuscata) have contributed to the advancement of primatology in both field and laboratory settings. Specifically, Japanese macaques serve as an excellent model for investigating postnatal development and seasonal breeding in primates because of their relatively prolonged juvenile period and distinct seasonal breeding activity in adulthood. Pioneering histological studies have examined the developmental associations between their reproductive states and spermatogenesis by morphological observation. However, a molecular histological atlas of Japanese macaque spermatogenesis is only in its infancy, limiting our understanding of spermatogenesis ontogeny related to their reproductive changes. Here, we performed immunofluorescence analyses of spermatogenesis in Japanese macaque testes to determine the expression of a subset of marker proteins. The present molecular histological analyses readily specified major spermatogonial subtypes as SALL4+ A spermatogonia and Ki67+/C-KIT+ B spermatogonia. The expression of DAZL, SCP1, γH2AX, VASA, and calmegin further showed sequential changes regarding the protein expression profile and chromosomal structures during spermatogenesis in a differentiation stage-specific manner. Accordingly, comparative analyses between subadults and adults identified spermatogenic deficits in differentiation and synchronization in subadult testes. Our findings provide a new diagnostic platform for dissecting spermatogenic status and reproduction in the Japanese macaques.

Asunto(s)

RESUMEN

We investigated individual variation in diet in relation to age-sex class and kin relationship in 28 of 40 members of a small group of wild Japanese macaques (Macaca fuscata). We used stable isotope ratios from hair as an index of individual dietary profiles, genetic relatedness as an index of kin relationship, and mitochondrial DNA (mtDNA) haplotype as a marker of being an immigrant or native member of the group. The range of carbon and nitrogen stable isotope ratios from hair of individual macaques (δ13C: -24.1‰ to -22.6‰, δ15N:3.8-5.5‰), which reflected their diet over a period of ~ 6 months, implied small individual variation in diet. The results of PERMANOVA implied that there were no significant effects of age class, sex, or mtDNA haplotype on hair stable isotope ratios between individuals, or on the variation in individual diet. However, the isotope values of males with mtDNA haplotypes that differed from those of the native females appeared to differ from those of other group members, which implies that immigrant males might have had a different diet profile from that of native group members. Furthermore, there was a weak correlation trend between genetic relatedness and differences in stable isotope ratios between pairs of individuals. Differences in stable isotope values were more marked in pairs with a more distant genetic relationship. This implies that within the group, closely related kin tended to forage together to avoid competing for food. However, this effect might have been weak because the size of the group was small relative to the size of the food patches, thereby reducing competition.

Asunto(s)

RESUMEN

Arginine vasopressin (AVP), when released into portal capillaries with corticotrophin-releasing factor (CRF) from terminals of parvocellular neurones of the hypothalamic paraventricular nucleus (PVH), facilitates the secretion of adrenocorticotrophic hormone (ACTH) in stressed rodents. The AVP gene encodes a propeptide precursor containing AVP, AVP-associated neurophysin II (NPII), and a glycopeptide copeptin, although it is currently unclear whether copeptin is always cleaved from the neurophysin and whether the NPII and/or copeptin have any functional role in the pituitary. Furthermore, for primates, it is unknown whether CRF, AVP, NPII and copeptin are all colocalised in neurosecretory vesicles in the terminal region of the paraventricular CRF neurone axons. Therefore, we investigated, by fluorescence and immunogold immunocytochemistry, the cellular and subcellular relationships of these peptides in the CRF- and AVP-producing cells in unstressed Japanese macaque monkeys (Macaca fuscata). Reverse transcription-polymerase chain reaction analysis showed the expression of both CRF and AVP mRNAs in the monkey PVH. As expected, in the magnocellular neurones of the PVH and supraoptic nucleus, essentially no CRF immunoreactivity could be detected in NPII-immunoreactive (AVP-producing) neurones. Immunofluorescence showed that, in the parvocellular part of the PVH, NPII was detectable in a subpopulation (approximately 39%) of the numerous CRF-immunoreactive neuronal perikarya, whereas, in the outer median eminence, NPII was more prominent (approximately 52%) in the CRF varicosities. Triple immunoelectron microscopy in the median eminence demonstrated the presence of both NPII and copeptin immunoreactivity in dense-cored vesicles of CRF-containing axons. The results are consistent with an idea that the AVP propeptide is processed and NPII and copeptin are colocalised in hypothalamic-pituitary CRF axons in the median eminence of a primate. The CRF, AVP and copeptin are all co-packaged in neurosecretory vesicles in monkeys and are thus likely to be co-released into the portal capillary blood to amplify ACTH release from the primate anterior pituitary.

Asunto(s)