Genomic Evidence for the Complex Evolutionary History of Macaques (Genus Macaca).

The genus Macaca is widely distributed, occupies a variety of habitats, shows diverse phenotypic characteristics, and is one of the best-studied genera of nonhuman primates. Here, we reported five re-sequencing Macaca genomes, including one M. cyclopis, one M. fuscata, one M. thibetana, one M. silenus, and one M. sylvanus. Together with published genomes of other macaque species, we combined 20 genome sequences of 10 macaque species to investigate the gene introgression and genetic differences among the species. The network analysis of the SNV-fragment trees indicates a reticular phylogeny of macaque species. Combining the results from various analytical methods, we identified extensive ancient introgression events among macaque species. The multiple introgression signals between different species groups were also observed, such as between fascicularis group species and silenus group species. However, gene flow signals between fascicularis and sinica group were not as strong as those between fascicularis group and silenus group. On the other hand, the unidirect gene flow in M. arctoides probably occurred between the progenitor of M. arctoides and the common ancestor of fascicularis group. Our study also shows that the genetic backgrounds and genetic diversity of different macaques vary dramatically among species, even among populations of the same species. In conclusion, using whole genome sequences and multiple methods, we have studied the evolutionary history of the genus Macaca and provided evidence for extensive introgression among the species.

Influence of COVID-19 on the emergence of stone-tool use behavior in a population of common long-tailed macaques (Macaca fascicularis fascicularis) in Thailand.

Stone tool use is a rare behavior across nonhuman primates. Here we report the first population of common long-tailed macaques (Macaca fascicularis fascicularis) who customarily used stone tools to open rock oysters (Saccostrea forskali) on a small island along the Thai Gulf in Koh Ped (KPE), eastern Thailand. We observed this population several times during the past 10 years, but no stone-tool use behavior was observed until our survey during the coronavirus disease 2019 (COVID-19) pandemic in July 2022. KPE is located in Pattaya City, a hotspot for tourism in Thailand. Tourists in this area frequently provided large amounts of food for the monkeys on KPE. During the COVID-19 curfew, however, tourists were not allowed to access the island, and monkeys began to face food scarcity. During this time, we observed stone-tool use behavior for the first time on KPE. Based on our observations, the first tool manipulation was similar to stone throwing (a known precursor of stone tool use). From our observations in March 2023, we found 17 subadult/adult animals performing the behavior, 15 of 17 were males and mostly solitary while performing the behavior. The M. f. fascicularis subspecies was confirmed by distribution, morphological characteristics, and mtDNA and SRY gene sequences. Taken together, we proposed that the stone tool use behavior in the KPE common long-tailed macaques emerged due to the COVID-19 food scarcity. Since traveling is no longer restricted many tourists have started coming back to the island, and there is a high risk for this stone tool-use behavior to disappear within this population of long-tailed macaques.

The Japan Monkey Centre Primates Brain Imaging Repository of high-resolution postmortem magnetic resonance imaging: The second phase of the archive of digital records.

A comparison of neuroanatomical features of the brain between humans and our evolutionary relatives, nonhuman primates, is key to understanding the human brain system and the neural basis of mental and neurological disorders. Although most comparative MRI studies of human and nonhuman primate brains have been based on brains of primates that had been used as subjects in experiments, it is essential to investigate various species of nonhuman primates in order to elucidate and interpret the diversity of neuroanatomy features among humans and nonhuman primates. To develop a research platform for this purpose, it is necessary to harmonize the scientific contributions of studies with the standards of animal ethics, animal welfare, and the conservation of brain information for long-term continuation of the field. In previous research, we first developed a gated data-repository of anatomical images obtained using 9.4-T ex vivo MRI of postmortem brain samples from 12 nonhuman primate species, and which are stored at the Japan Monkey Centre. In the present study, as a second phase, we released a collection of T2-weighted images and diffusion tensor images obtained in nine species: white-throated capuchin, Bolivian squirrel monkey, stump-tailed macaque, Tibet monkey, Sykes' monkey, Assamese macaque, pig-tailed macaque, crested macaque, and chimpanzee. Our image repository should facilitate scientific discoveries in the field of comparative neuroscience. This repository can also promote animal ethics and animal welfare in experiments with nonhuman primate models by optimizing methods for in vivo and ex vivo MRI scanning of brains and supporting veterinary neuroradiological education. In addition, the repository is expected to contribute to conservation, preserving information about the brains of various primates, including endangered species, in a permanent digital form.

Prevalence of Mycobacterium tuberculosis Complex among Wild Rhesus Macaques and 2 Subspecies of Long-Tailed Macaques, Thailand, 2018-2022.

We identified tuberculosis in 1,836 macaques from 6 wild rhesus (Macaca mulatta), 23 common long-tailed (M. fascicularis fascicularis), and 6 Burmese long-tailed (M. fascicularis aurea) macaque populations in Thailand. We captured, anesthetized, and collected throat, buccal, and rectal swab specimens from the macaques. We screened swabs for Mycobacterium tuberculosis complex (MTBC) using insertion sequence 6110-specific nested PCR. We found higher MTBC prevalence at both population and individual levels among M. mulatta than M. fascicularis fascicularis macaques; all 3 M. fascicularis aurea macaque populations were positive for tuberculosis. We found that throat swab specimens provided the best sample medium for detecting MTBC. Our results showed no difference in MTBC prevalence between male and female animals, but a higher percentage of adults were infected than subadults and juveniles. Although we detected no association between frequency of human-macaque interaction and MTBC prevalence, bidirectional zoonotic transmission should be considered a possible public health concern.

Gene flow from rhesus (Macaca mulatta) to cynomolgus macaques (M. fascicularis) and effects of introgressive hybridization on reproduction in two biomedically relevant non-human primate species.

BACKGROUND: We compared the reproductive patterns of wild Indochinese and Sundaic cynomolgus macaques (Mf) exhibiting different levels of genetic admixture with rhesus macaques (Mm). METHODS: Ten adult females from each Indochinese (WHM) and Sundaic (KN/KTK) Mf populations, which exhibited 50% and 15% of Mm autosomal SNPs, were selected as focal animals. Animals were observed for 12 months, and the frequencies of sexual proceptivity, attractivity and receptivity, number of newborns, and changes in sex skin were recorded. RESULTS: Both populations showed all three sexual behaviors throughout the year, but they were classified as moderately seasonal breeders because their 3-month birth counts were as high as ~50%. The fecundity of WHM was lower than the KN/KTK. Changes in sex skin of WHM were more prone to Mm's pattern than the KN/KTK. CONCLUSION: The introgressive gene flow from Mm to Mf does not affect Mf's sexual behaviors; however, it can impact fecundity and physiological (sex skin) changes.

Population Structure of Macaca fascicularis aurea, and their Genetic Relationships with M. f. fascicularis and M. mulatta Determined by 868 RADseq-Derived Autosomal SNPs-A consideration for biomedical research.

BACKGROUND: This study examined the population structure of Macaca fascicularis aurea and their genetic relationships with M. f. fascicularis and M. mulatta. METHODS: The study analyzed 868 RADseq-derived SNPs from samples representing the entire distribution range of M. f. aurea, including their inter- and intraspecific hybrid zones. RESULTS: The study supports a M. mulatta/Indochinese M. f. fascicularis, Sundaic M. f. fascicularis, and M. f. aurea trichotomy; M. f. aurea was genetically distinct from both forms of M. f. fascicularis and M. mulatta. Hybridization between M. f. aurea and M. f. fascicularis occurred in two directions: south-north (8°25' to 15°56') and west-east (98°28' to 99°02'). Low levels of M. mulatta introgression were also detected in M. f. aurea. CONCLUSION: This study showcases a complicated scenario of genetic relationships between the M. fascicularis subspecies and between M. fascicularis and M. mulatta and underscores the importance of these taxa's population structure and genetic relationships for biomedical research.

Secondary contact and genomic admixture between rhesus and long-tailed macaques in the Indochina Peninsula.

Understanding the process and consequences of hybridization is one of the major challenges in evolutionary biology. A growing body of literature has reported evidence of ancient hybridization events or natural hybrid zones in primates, including humans; however, we still have relatively limited knowledge about the pattern and history of admixture because there have been little studies that simultaneously achieved genome-scale analysis and a geographically wide sampling of wild populations. Our study applied double-digest restriction site-associated DNA sequencing to samples from the six localities in and around the provisional hybrid zone of rhesus and long-tailed macaques and evaluated population structure, phylogenetic relationships, demographic history, and geographic clines of morphology and allele frequencies. A latitudinal gradient of genetic components was observed, highlighting the transition from rhesus (north) to long-tailed macaque distribution (south) as well as the presence of one northern population of long-tailed macaques exhibiting unique genetic structure. Interspecific gene flow was estimated to have recently occurred after an isolation period, and the migration rate from rhesus to long-tailed macaques was slightly greater than in the opposite direction. Although some rhesus macaque-biased alleles have widely introgressed into long-tailed macaque populations, the inflection points of allele frequencies have been observed as concentrated around the traditionally recognized interspecific boundary where morphology discontinuously changed; this pattern was more pronounced in the X chromosome than in autosomes. Thus, due to geographic separation before secondary contact, reproductive isolation could have evolved, contributing to the maintenance of an interspecific boundary and species-specific morphological characteristics.

Locomotor Kinematics of Two Semi-Wild Macaque Species (Macaca assamensis and Macaca arctoides) in Thailand.

This project aimed to investigate primate locomotor kinematics noninvasively in the wild. Semi-wild Assamese and stump-tailed macaques were selected for the study, which was performed in Thailand. We investigated their locomotor kinematics and its relationship to habitat use. The macaques' positional behavior was recorded with two video cameras, and kinematic parameters were estimated during terrestrial quadrupedal locomotion, using the markerless method. The data analyzed so far revealed that stump-tailed macaques walk with longer, less frequent strides than Assamese macaques. Although stump-tailed macaques present a smaller angular excursion of the shoulder joint than Assamese macaques, they exhibited a relatively large shoulder girdle motion and anteroposterior translation of the shoulder, which increased their stride length. Additionally, stump-tailed macaques exhibited a digitigrade gait and elbow extension, suggesting a good adaptation to terrestrial locomotion. Assamese macaques, on the other hand, exhibited a gait that did not seem optimized for terrestrial locomotion, using the hands in a palmigrade posture and frequently flexing the fingers at varying degrees. The kinematic characteristics of the two species studied is consistent with previous field observations reporting that Assamese macaques are highly arboreal, whereas stump-tailed macaques are more terrestrial.

Whole Mitochondrial Genomic and Y-Chromosomal Phylogenies of Burmese Long-Tailed Macaque (Macaca fascicularis aurea) Suggest Ancient Hybridization between fascicularis and sinica Species Groups.

Macaca fascicularis aurea (Burmese long-tailed macaque) is 1 of the 10 subspecies of Macaca fascicularis. Despite having few morphological differences from other subspecies, a recent phylogeographic study showed that M. f. aurea is clearly distinct genetically from Macaca fascicularis fascicularis (common long-tailed macaque) and suggests that M. f. aurea experienced a disparate evolutionary pathway versus other subspecies. To construct a detailed evolutionary history of M. f. aurea and its relationships with other macaque species, we performed phylogenetic analyses and divergence time estimation of whole mitochondrial genomes (2 M. f. aurea, 8 M. f. fascicularis, and 16 animals of 12 macaque species) and 2871 bp of the Y chromosome (1 M. f. aurea, 2 M. f. fascicularis, and 5 animals of 5 macaque species) and haplotype network analysis of 758 bp of the Y chromosome (1 M. f. aurea, 2 M. f. fascicularis, and 21 animals of 19 macaque species). Whereas the Y chromosome of M. f. aurea clustered with those of the fascicularis species group in the phylogenetic and haplotype network analyses, its mtDNA clustered within the clade of the sinica species group. Based on this phylogenetic incongruence and the estimated divergence times, we propose that proto-M. f. aurea underwent hybridization with a population of the sinica species group between 2.5 and 0.95 MYA after divergence from the common ancestor of M. fascicularis. Hybridization and introgression might have been central in the evolution of M. f. aurea, similar to what occurred in the evolution of other macaque species and subspecies.

Age-related changes of sulcal imprints on the endocranium in the Japanese macaque (Macaca fuscata).

OBJECTIVES: The degree of expression of sulcal patterns on endocasts of nonhuman primates has been shown to depend primarily on species (brain size) and age of the individual. It has been suggested that brain details on endocasts are reproduced better in juvenile than adult primates. Here, we investigated age-related changes in the imprint of the major sulci on the endocranium of Japanese macaques (Macaca fuscata) from the juvenile period to adulthood. MATERIALS AND METHODS: Using CT scans of 25 (12 males, 13 females) cranial specimens from macaques, we generated virtual endocasts to assess imprints of the seven main sulci on the endocranial surface. Expression of each sulcal imprint was evaluated by imprint score method. RESULTS: The degree of expression of sulcal imprints differed between sulci. Arcuate, superior temporal, and principal sulci were well defined, whereas lunate and intraparietal sulci were poorly represented. Sulcal imprints showed significant age-related changes in Japanese macaques from juvenile to elderly. Sulcal imprints showed a slight decrease in degree of expression from the juvenile period (2-4 years) to adolescence (4-6 years), and then remained unchanged until mid-adulthood (15-16 years). The degree of expression of the sulcal imprints significantly decreased from mid-adulthood to old age (>20 years). CONCLUSIONS: The degree of expression of the sulcal imprints (relief forms) in inner table bone surface (endocranium) reveals significant age-related decreases in adults. The great decrease starts at around 20 years of age. The endocranial volume showed a significant age-related increase, and thus, it is suggested that the endocranial surface in macaques may be resorbed with advancing age.

Mitochondrial DNA and two Y-chromosome genes of common long-tailed macaques (Macaca fascicularis fascicularis) throughout Thailand and vicinity.

Macaca fascicularis fascicularis is distributed over a wide area of Southeast Asia. Thailand is located at the center of their distribution range and is the bridge connecting the two biogeographic regions of Indochina and Sunda. However, only a few genetic studies have explored the macaques in this region. To shed some light on the evolutionary history of M. f. fascicularis, including hybridization with M. mulatta, M. f. fascicularis and M. mulatta samples of known origins throughout Thailand and the vicinity were analyzed by molecular phylogenetics using mitochondrial DNA (mtDNA), including the hypervariable region 1, and Y-chromosomal DNA, including SRY and TSPY genes. The mtDNA phylogenetic analysis divided M. f. fascicularis into five subclades (Insular Indonesia, Sundaic Thai Gulf, Vietnam, Sundaic Andaman sea coast, and Indochina) and revealed genetic differentiation between the two sides of the Thai peninsula, which had previously been reported as a single group of Malay peninsular macaques. From the estimated divergence time of the Sundaic Andaman sea coast subclade, it is proposed that after M. f. fascicularis dispersed throughout Southeast Asia, some populations on the south-easternmost Indochina (eastern Thailand, southern Cambodia and southern Vietnam at the present time) migrated south-westwards across the land bridge, which was exposed during the glacial period of the late Pleistocene epoch, to the southernmost Thailand/northern peninsular Malaysia. Then, some of them migrated north and south to colonize the Thai Andaman sea coast and northern Sumatra, respectively. The SRY-TSPY phylogenetic analysis suggested that male-mediated gene flow from M. mulatta southward to M. f. fascicularis was restricted south of, but close to, the Isthmus of Kra. There was a strong impact of the geographical factors in Thailand, such as the Isthmus of Kra, Nakhon Si Thammarat, and Phuket ranges and Sundaland, on M. f. fascicularis biogeography and their hybridization with M. mulatta.

Genetic analysis of samples from wild populations opens new perspectives on hybridization between long-tailed (Macaca fascicularis) and rhesus macaques (Macaca mulatta).

In the past decade, many researchers have published papers about hybridization between long-tailed and rhesus macaques. These previous works have proposed unidirectional gene flow with the Isthmus of Kra as the zoogeographical barrier of hybridization. However, these reports analyzed specimens of unknown origin and/or did not include specimens from Thailand, the center of the proposed area of hybridization. Collected specimens of long-tailed and rhesus macaques representing all suspected hybridization areas were examined. Blood samples from four populations each of long-tailed and rhesus macaques inhabiting Thailand, Myanmar, and Laos were collected and analyzed with conspecific references from China (for rhesus macaques) and multiple countries from Sundaic regions (for long-tailed macaques). Ninety-six single nucleotide polymorphism (SNP) markers specifically designed to interrogate admixture and ancestry were used in genotyping. We found genetic admixture maximized at the hybrid zone (15-20°N), as well as admixture signals of varying strength in both directions outside of the hybrid zone. These findings show that the Isthmus of Kra is not a barrier to gene flow from rhesus to long-tailed populations. However, to precisely identify a southernmost barrier, if in fact a boundary rather than simple isolation by distance exists, the samples from peninsular Malaysia must be included in the analysis. Additionally, a long-tailed to rhesus gene flow boundary was found between northern Thailand and Myanmar. Our results suggest that selection of long-tailed and rhesus macaques, the two most commonly used non-human primates for biomedical research, should take into account not only the species identification but also the origin of and genetic admixture within and between the species.

Assessment of the hybridization between rhesus (Macaca mulatta) and long-tailed macaques (M. fascicularis) based on morphological characters.

OBJECTIVES: Hybridization between rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques has become a focal point of interest. The majority of such studies have evaluated their genetics, but not their morphological characters. MATERIALS AND METHODS: We analyzed morphological characters of eight free-ranging populations of Indochinese rhesus and long-tailed macaques distributed at the proposed hybrid zone (15.75-21.58° N) in comparison with one population each of Chinese and Indian-derived rhesus macaques and three populations of Sundaic long-tailed macaques. RESULTS: Chinese and Indian rhesus macaques had a heavier body mass, longer crown-rump length, shorter relative facial length and relative tail length, and a greater contrast of reddish and yellowish dorsal pelage color than the Sundaic long-tailed macaques for which the latter three parameters could be used to visually discriminate between the two species. Although the morphological characters of Indochinese rhesus and long-tailed macaques were intermediate between the Chinese/Indian rhesus and Sundaic long-tailed macaques, they were more similar to their respective conspecifics. The species-specific characters of a shorter tail (<70%) and a bipartite pelage color pattern were retained in the Indochinese rhesus macaques while the longer tail (>90%) and no bipartite pattern was found in the Indochinese long-tailed macaques. No morphological cline was observed across the species and the variations were abrupt to some extent. DISCUSSION: The hybridization between rhesus and long-tailed macaques may be results of multiple contacts and isolations over a long period of time, thus their evolutionary history should not be drawn solely by genetic or morphological analysis.

Morphological characteristics and genetic diversity of Burmese long-tailed Macaques (Macaca fascicularis aurea).

Macaca fascicularis aurea (Mfa) is the only macaque which has been recorded to use stone tools to access encased foods. They live in close contact with M. fascicularis fascicularis (Mff) in southwestern Thailand and the hybrids were reported [Fooden, 1995]. Although Mff and Mfa can be seen in the same habitat types, tool-use behavior has never been reported in Mff. Thus, comparing the morphological characteristics and genetics between Mfa and Mff should help elucidate not only the morphological differences and genetic divergence between these subspecies but also potentially the relationship between genetics and their tool use behavior. We surveyed Mfa and Mff in Myanmar and Thailand, ranging from 16° 58' to 7° 12' N. Fecal or blood samples were collected from eight, five, and four populations of Mfa, Mff, and Mff × Mfa morphological hybrids along with three individuals of captive Chinese M. mulatta (Mm), respectively, for mtDNA and Y-chromosome (TSPY and SRY genes) DNA sequence analyses. In addition, eight populations were captured and measured for 38 somatometric dimensions. Comparison of the somatic measurements revealed that Mfa had a statistically significantly shorter tail than Mff (P < 0.05). Based on the mtDNA sequences, Mfa was separated from the Mm/Mff clade. Within the Mfa clade, the mainland Myanmar population was separate from the Mergui Archipelago and Thailand Andaman seacoast populations. All the morphological hybrids had the Mff mtDNA haplotype. Based on the Y-chromosome sequences, the three major clades of Mm/Indochinese Mff, Sundaic Mff, and Mfa were constructed. The hybrid populations grouped either with the Mm/Indochinese Mff or with the Mfa. Regarding the genetic analysis, one subspecies hybrid population in Thailand (KRI) elicited tool use behavior, thus the potential role of genetics in tool use behavior is raised in addition to the environmental force, morphological suitability, and cognitive capability. Am. J. Primatol. 78:441-455, 2016. © 2015 Wiley Periodicals, Inc.

Hybridization and its impact on the ontogenetic allometry of skulls in macaques.

The role of hybridization in morphological diversification is a fundamental topic in evolutionary biology. However, despite the accumulated knowledge on adult hybrid variation, how hybridization affects ontogenetic allometry is less well understood. Here, we investigated the effects of hybridization on postnatal ontogenetic allometry in the skulls of a putative hybrid population of introduced Taiwanese macaques (Macaca cyclopis) and native Japanese macaques (Macaca fuscata). Genomic analyses indicated that the population consisted of individuals with varying degrees of admixture, formed by male migration from Japanese to Taiwanese macaques. For overall skull shape, ontogenetic trajectories were shifted by hybridization in a nearly additive manner, with moderate transgressive variation observed throughout development. In contrast, for the maxillary sinus (hollow space in the face), hybrids grew as fast as Taiwanese macaques, diverging from Japanese macaques, which showed slow growth. Consequently, adult hybrids showed a mosaic pattern, that is, the maxillary sinus is as large as that of Taiwanese macaques, while the overall skull shape is intermediate. Our findings suggest that the transgressive variation can be caused by prenatal shape modification and nonadditive inheritance on regional growth rates, highlighting the complex genetic and ontogenetic bases underlying hybridization-induced morphological diversification.

Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain.

Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.

Testing Sex-Biased Admixture Origin of Macaque Species Using Autosomal and X-Chromosomal Genomic Sequences.

The role of sex-specific demography in hybridization and admixture of genetically diverged species and populations is essential to understand the origins of the genomic diversity of sexually reproducing organisms. In order to infer how sex-linked loci have been differentiated undergoing frequent hybridization and admixture, we examined 17 whole-genome sequences of seven species representing the genus Macaca, which shows frequent inter-specific hybridization and predominantly female philopatry. We found that hybridization and admixture were prevalent within these species. For three cases of suggested hybrid origin of species/subspecies, Macaca arctoides, Macaca fascicularis ssp. aurea, and Chinese Macaca mulatta, we examined the level of admixture of X chromosomes, which is less affected by male-biased migration than that of autosomes. In one case, we found that Macaca cyclopis and Macaca fuscata was genetically closer to Chinese M. mulatta than to the Indian M. mulatta, and the admixture level of Chinese M. mulatta and M. fuscata/cyclopis was more pronounced on the X chromosome than on autosomes. Since the mitochondrial genomes of Chinese M. mulatta, M. cyclopis, and M. fuscata were found to cluster together, and the mitochondrial genome of Indian M. mulatta is more distantly related, the observed pattern of genetic differentiation on X-chromosomal loci is consistent with the nuclear swamping hypothesis, in which strong, continuous male-biased introgression from the ancestral Chinese M. mulatta population to a population related to M. fuscata and M. cyclopis generated incongruencies between the genealogies of the mitochondrial and nuclear genomes.

Comparative analysis of oral-gut microbiota between captive and wild long-tailed macaque in Thailand.

Long-tailed macaques (Macaca fascicularis), distributed in Southeast Asia, are generally used in biomedical research. At present, the expansion of human communities overlapping of macaques' natural habitat causes human-macaque conflicts. To mitigate this problem in Thailand, the National Primate Research Center of Thailand, Chulalongkorn University (NPRCT-CU), was granted the permit to catch the surplus wild-born macaques and transfer them to the center. Based on the fact that the diets provided and the captive environments were different, their oral-gut microbiota should be altered. Thus, we investigated and compared the oral and fecal microbiome between wild-born macaques that lived in the natural habitats and those transferred to and reared in the NPRCT-CU for 1 year. The results from 16S rRNA high-throughput sequencing showed that the captive macaques had distinct oral-gut microbiota profiles and lower bacterial richness compared to those in wild macaques. The gut of wild macaques was dominated by Firmicutes which is probably associated with lipid absorption and storage. These results implicated the effects of captivity conditions on the microbiome that might contribute to crucial metabolic functions. Our study should be applied to the animal health care program, with respect to microbial functions, for non-human primates.

Geometric characters of the radius and tibia in Macaca mulatta and Macaca fascicularis.

We performed comparative analyses of four cross-sections of the distal radius and tibia in two species of macaque to clarify the relationships between bone morphology and locomotor type. The lengths of bones and five bone geometric properties in each section were examined and compared separately in both female and male Macaca mulatta and Macaca fascicularis. In M. mulatta, there were no significant gender-specific differences in either the radius or the tibia. In contrast, the radius and tibia of male M. fascicularis had greater geometric parameters in the 20% and 40% positions relative to the 5% and 10% positions from the distal end than those of their female counterparts. The radius and tibia of M. mulatta were relatively longer than those of M. fascicularis, and the sectional parameters of the tibia of M. mulatta were relatively larger than those of M. fascicularis. Standardization of the log-transformed bone length between the species revealed larger radial cortical bone areas in M. fascicularis. In contrast, there were minimal differences in the tibial cortical bone areas between the two species. This study suggests that the observed distinctions in bone geometry in female and male M. fascicularis may be due to gender-specific differences in the muscle weights of the forearm and calf, which may underlie the divergence in the leaping abilities of females and males of this species. Taken together, these results of interspecies comparisons may be related to the fact that arboreal primates such as M. fascicularis undergo compressive mechanical stress due to the forelimb lead that occurs as the animal descends a sloping trunk or bridges a tree gap downward, while terrestrial primates such as M. mulatta move on nearly flat substrates. Differences in fore- and hind-limb bone properties between the two species are discussed with regard to functional morphology and locomotor type.

Skeletal determinants of tail length are different between macaque species groups.

Macaques (genus Macaca) are known to have wide variation in tail length. Within each species group tail length varies, which could be associated with a phylogenetic trend seen in caudal vertebral morphology. We compared numbers and lengths of caudal vertebrae in species of the fascicularis group, M. assamensis (sinica group), M. nemestrina (silenus group), and those obtained from reports for an additional 11 species. Our results suggest different trends in number and lengths. The caudal vertebral length profiles revealed upward convex patterns for macaques with relative tail lengths of ≥15%, and flat to decreasing for those with relative tail lengths of ≤12%. They varied between species groups in terms of the lengths of proximal vertebrae, position and length of the longest vertebra, numbers and lengths of distal vertebrae, and total number of vertebrae. In silenus and sinica group, the vertebral length is the major skeletal determinant of tail length. On the other hand, the vertebral number is the skeletal determinant of tail length in the fascicularis group. Tail length variation among species groups are caused by different mechanisms which reflect the evolutionary history of macaques.