Genetic variability in macaques: Correlations between biochemical and dermatoglyphic systems

The palmar dermatoglyphics of four groups of macaque, Macaca nemestrina, M. fuscata yakui, M. f. fuscata and M. fascicularis, were compared, and the genetic affinities of the four groups were assessed using a dermatoglyphic mean square distance measure. According to this measure the two subspecies of M. fuscata were dermatoglyphically more distant from one another than was M. fuscata fuscata from M. nemestrina, suggesting that the two insular populations of M. fuscata had evolved in genetic isolation. The distributions of specific dermatoglyphic patterns were then compared with the frequency distributions of alleles at different protein structural loci in other macaque populations. The results of the comparison were consistent in that insular populations showed reduction in variability for both kinds of systems. The implications of this correlation are discussed in terms of population size and natural selection.     

Male external genitalia and systematic relationships of the Japanese macaque (Macaca fuscata Blyth, 1875)

Penial morphology was studied in six preserved specimens of the Japanese macaque,Macaca fuscata. Structure of the glans penis and baculum inM. fuscata is essentially similar to that in the rhesus macaque,M. mulatta. With age the skin of the penis inM. fuscata apparently becomes progressively more darkly and extensively pigmented, and the baculum becomes progressively longer. One immature specimen examined, with penial skin unpigmented and baculum cartilaginous, appears to be abnormally retarded in penial development. Penial morphology suggests that the allopatric speciesM. fuscata, M. mulatta, M. cyclopis, andM. fascicularis constitute a closely interrelated group. Contrary to a previous report, there is no evidence that penial morphology inM. fuscata is transitional to that inM. radiata andM. sinica. InM. fuscata, M. mulatta, andM. fascicularis, latitudinal variation of body size and relative tail length conforms toBergmann's rule andAllen's rule; external proportions in three specimens ofM. cyclopis only partly conform to this pattern.     

Distributional pattern of serotonin-immunoreactive nerve fibers in the lateral geniculate nucleus of the rat,cat and monkey (Macaca fuscata)

Summary The distribution of serotonin-containing nerve fibers in the lateral geniculate nucleus (LGN) of the rat, cat, and monkey (Macaca fuscata) was studied by use of the peroxidase-antiperoxidase method and an antiserum against serotonin. In all three species, the pattern of fibers was denser in the ventral portion of the LGN (LGNv) than in the dorsal nuclear portion (LGNd). In the LGNd of rat, serotonin-immunoreactive fibers were evenly distributed in the form of a dense network, but in cat and monkey there were marked regional differences. Serotonin-immunoreactive elements were most numerous in the C complex and medial interlaminal nucleus of cat, and in the S layer and interlaminar zones of Macaca fuscata.Supported by a grant from the Ministry of Education, Science, and Culture of Japan (No. 57214028)     

Long distance mobility of male Japanese macaques evidenced by mitochondrial DNA

A 487-nucleotide sequence in the polymorphic D-loop region of matrilineally inherited mitochondrial DNA was compared in samples from 14 (9 adult males and 5 females or young) Japanese macaques (Macaca fuscata fuscata) of two troops at Gagyusan in Takahashi City, Okayama Prefecture, Japan. The majority (7 out of the sampled 9) of the adult males associated with the troops had nucleotide sequences of six distinct types, all of which were different from that of the Gagyusan troop females, whereas two young solitary males shared the same sequence. The present study exemplified a case in which the majority of adult males immigrated from outside the local population. Notably, two of the males were revealed to share the same sequence determined for a matriline 45 km away. Electronic Publication     

Clinical examinations of the Japanese monkey (Macaca fuscata)

Since 1962 clinical examinations have been performed on all 466 Japanese monkeys from the troops of the western part of Japan.During the external inspection we found a few cases of malformation of the hand and foot in some troops, but except for these they were in good physical condition, negative in tuberculin test and in Shigella and Salmonella infection.In all troops a high rate of helminthic infection was detected and there was a difference in the rate of occurrence of certain helminths betweenMacaca fuscata fuscata andM. fuscata yakui. No single case with the antibody to the B Virus was encountered, and it seems that no infection of the B Virus is present among the Japanese monkey.The free-ranging condition under which the Japanese monkey inhabits in troops seems to be satisfactory and they seem to have no serious problem of any kind at present.     

Prenatal ontogeny of subspecific variation in the craniofacial morphology of the Japanese macaque (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

We cross-sectionally investigated prenatal ontogeny of craniofacial shape in the two subspecies of the Japanese macaque (Macaca fuscata fuscata and Macaca fuscata yakui) using a geometric morphometric technique to explore the process of morphogenetic divergence leading to the adult morphological difference between the subspecies. The sample comprised a total of 32 formalin-fixed fetal specimens of the two subspecies, in approximately the second and third trimesters. Each fetal cranium was scanned using computed tomography to generate a three-dimensional surface model, and 68 landmarks were digitized on the external and internal surface of each cranium to trace the growth-related changes in craniofacial shape of the two subspecies. The results of our study demonstrated that the two subspecies generally shared the same craniofacial growth pattern. Both crania tend to exhibit relative contraction of the neurocranium in the mediolateral and superoinferior directions, a more superiorly positioned cranial base, a more vertically oriented occipital squama, and a more anteriorly positioned viscerocranium as the cranial size increased. However, distinctive subspecific differences, for example relatively narrower orbital breadth, higher orbit, higher position of the nuchal crest, and more protrudent snout found in Macaca fuscata yakui were already present during the prenatal period. This study demonstrated that morphological differentiation in the craniofacial shape may occur at a very early stage of the fetal period even between closely related subspecies of the Japanese macaque.     

The palmar dermatoglyphics of Macaca fascicularis: A comparison with Macaca fuscata

An analysis of the palmar dermatoglyphics from a sizeable population of Macaca fascicularis is presented. These dermatoglyphics are then compared with those obtained by Mitsuo Iwamoto for M. fuscata fuscata and M. fuscata yakui to try and determine if they can be used to delineate species' boundaries. Finally the results as well as possible phylogenetic implications are discussed.     

Matrilineal rank Inheritance varies with absolute rank in Japanese macaques

In many cercopithecine primates, females form linear dominance hierarchies based on kinship. It is known that female rank follows the rules of matrilineal rank inheritance (MIR): (1) maternal rank inheritance, (2) maternal dominance, and (3) youngest ascendancy among sisters. Although, several determining such variation remain largely unknown. In this paper, I investigate the dominance relation-ships of 69 adult (>6 yr old) female Japanese macaques (Macaca fuscata fuscata) in a free-ranging provisioned troop living in Shiga-Heights (Nagano Prefecture, Japan) and report new evidence of intra-group variation. Dominance relationships among high-ranking females followed MRI within kin units, those among low-ranking females did not. Maternal rank inheritance and youngest ascendancy operated between mother/daughter dyads and sister dyads of high-rank, but not in the dyads of low-rank. The dominance ranks of females from low-ranking kin units were dispersed and less predictable. These findings suggest that MRI varies with absolute dominance rank, and are discussed in relation to other asymmetries between high-and low-rank     

NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan

A macaque population produced by the hybridization of native Japanese macaques (Macaca fuscata) and introduced Taiwanese macaques (M. cyclopis) in Wakayama Prefecture was shown to possess three DNA haplotypes of the natural resistance-associated macrophage protein 1 (NRAMP1). Based on genotyping and comparison with M. fuscata populations, it was revealed that the introduced M. cyclopis population was polymorphic for the NRAMP1 locus. Extensive crossbreeding of the introduced species with the native species was confirmed using this genetic marker and the proportion of M. cyclopis genes was 57.4%. Results of statistical tests suggested non-random mating in the hybrid population.     

Cranial adaptation to a high attrition diet in Japanese macaques

Primates with diets that require greater occlusal forces to process exhibit anteroposteriorly shorter, vertically deeper faces, more anteriorly placed masseter attachment areas, and broader, taller mandibular corpora compared to closely related species/populations. Japanese macaques (Macaca fuscata)eat different, perhaps mechanically tougher to process, foods than other macaques do. Accordingly, they should exhibit structural features of the skull related to dissipating great occlusal loads. To test this hypothesis I compared cranial variables amongst wild-caught, adult female skulls (n = 85) of M. fuscataand three other macaque species (M. mulatta, M. fascicularis,and M. nemestrina)and applied least-squares and reduced-major-axis regression analysis and principal components analysis (PCA) to 17 cranial variables reflecting facial, vault, and mandibular dimensions. When scaled for size, the Japanese macaque has a vertically deeper and anteroposteriorly shorter face,a broader but not taller mandibular corpus, and a more anteriorly placed masseter muscle than the other three macaques do. The first PCA axis isolates variation due to a suite of characters related to mechanical efficiency in dissipating occlusal loads (vertically deep face and broad corpus) and differentiates the Japanese macaques from the other species. This, coupled with reported dietary differences among species, suggests that Japanese macaques are selected for dissipating greater occlusal loads than other macaques are. The presence of a narrow mandible relative to cranial breadth and a hyperrobust mandibular corpus width suggests that axial torsion is a significant influence in the masticatory regime of M. fuscata.The lack of an increase in corpus height indicates that parasagittal bending is not as significant an influence. Geographic and climatic influences cannot account for the patterns of variation between M. fuscataand the other macaques.     

Cervical ripening and uterine contraction induced by prostaglandin E2-gel in pregnant Japanese monkeys (Macaca fuscata fuscata)

Effects of intracervical administration of PGE₂-gel were studied in pregnant Japanese monkeys (Macaca fuscata fuscata) near term. Administration of PGE₂-gel induced cervical ripening and an increase in maternal plasma PGE₂ but no change in PGF_2α. Ultrastructural observations of the connective tissue of the cervix after PGE₂-gel treatment revealed a decrease in the number of collagenous fibers. These results show that intracervical administration of PGE₂-gel induces cervical ripening without induction of labor in the Japanese monkey.     

Species recognition by five macaque monkeys

Sixteen monkeys of five macaque species (Macaca fuscata fuscata, M. mulatta, M. radiata, M. nemestrina, andM. arctoides) pressed a lever to see a variety of pictures (35 mm slides) of seven macaque species including their conspecifics. The subjects were allowed to see the same picture for the duration of the lever press and were able to see the same picture repeatedly by pressing the lever within 10 sec after the previous release of the lever. When 10 sec passed after releasing the lever, the next picture was set on the slide projector. All monkeys exceptM. arctoides and two infantM. fuscata fuscata pressed the lever to see their conspecifics for the longest duration. For all of the adult subjects, a multivariate analysis of variance (MANOVA) based on the mean duration of lever pressing responses (D) and the mean interval between the responses (I) revealed that the data for conspecific stimuli were distributed at significantly different locations from those for at least one of six close species on a two-dimensional space constructed with D and I. These results suggest that adult macaque monkeys visually discriminate their conspecifics from close species based on the still images of them.     

Differences in hair density of Japanese monkeys (Macaca fuscata fuscata) with locality and age

The hair density of free-ranging Japanese monkeys (Macaca fuscata fuscata) living in three different areas was investigated. The Japanese monkeys had thicker hair than other macaques. The hair density in the Japanese monkeys varied with locality: the northern monkeys had thicker hair than the southern ones. The density did not vary markedly with age up to 3 years of age, but then decreased gradually up to adult age (≧7 years old). The remarkable growth of the trunk suggested that the total number of hairs increased with age, especially during the period as a juvenile.     

Bone and Joint Disorders in Wild Japanese Macaques from Nagano Prefecture,Japan

I studied bone and joint disorders in wild Japanese macaques (Macaca fuscata fuscata) in order to discern some aspects of their life history from the skeletal material. The specimens comprise 107 nearly complete skeletons of subadults and adults that were killed as crop-raiding monkeys between 1997 and 1998 in Nagano Prefecture, Japan. The most frequent disorder is angular deformity due to fractures: 80 healed fractures in 31 of 52 males and 71 healed fractures in 26 of 55 females. Secondary osteoarthritis due to fractures is rare. Two males have osteochondritis dissecans bilaterally on the posterior surface of the lateral femoral condyles. Degenerative changes are common in the aged individuals. Fractures of the trunk—clavicle, scapula, vertebrae, ribs or hip—are frequent in the males. Contrarily, the majority of fractures in females are in the hands and feet. While most fractures in males appear to have occurred during adulthood, those in females occurred during childhood and senescence. Interindividual violence should not be regarded as a principal cause for fractures in males and females because there is no bite wound except perhaps for one case of an amputated digit. Fractures of the trunk in males were probably caused by impact forces against their shoulders or hips or both caused by rolling down a steep slope or falling out of trees, perhaps during intertroop transfers.     

Two macaque fossil teeth from the Japanese Pleistocene

Two fossil teeth of the Pleistocene macaque of Japan are stated to be those ofMacaca cf.fuscata. One of them is a lower canine tooth found in the Shiriya mine in northern Japan. It has been thought that the fossil assemblage of the Shiriya mine is of the late Pleistocene. The canine concerned is not distinguishable from the lower right one of the living female Japanese monkey. The other is a lower molar taken from the Ando quarry in western Japan. The fossil assemblage from the Ando quarry or from sites neighbouring the quarry indicates that the age of the molar can be traced back to the middle Pleistocene. The molar concerned has a somewhat buccolingually depressed crown as compared with that of the living Japanese monkey (Macaca fuscata).     

Threat calls in alliance formation by members of a captive group of Japanese monkeys

The vocal behavior of threat calls was investigated in a captive group of Japanese monkeys (Macaca fuscata fuscata). The vocalizations were heard most often when they undertook winner-support during triadic agonistic interactions. The likelihood of call emission in support of the winner was affected by the attributes of the participants, and not by the types of agonistic behavior. The calls were emitted by intermediate ranking animals frequently in support of high ranking animals and in support of females. The calling behavior of winner-supporters appears to advertise the partner and distant group members of their support for reciprocation in the near future.     

Sequential analysis of the social behavior of infants in groups of Japanese monkeys (Macaca fuscata fuscata)

We employed techniques of behavioral entropy to carry out a quantitative analysis of sequences of behavioral patterns evident in the interaction between infants and other members of a group of Japanese monkeys (Macaca fuscata fuscata). The group concerned included examples both of monkeys in captivity and in the wild state. The results were examined as a function of the animal age and environmental differences (cage-field). An example is given to illustrate the use of information theory. Findings partially confirmed that the variability of social behavior decreases as the age of the animals increases.     

Population genetical study of Japanese macaques,Macaca fuscata,in the shimokita A1 troop,with special reference to genetic variability and relationships to Japanese macaques in other troops

The genetic variations of 35 individuals of the Shimokita A1 troop of mainland Japanese macaques,Macaca fuscata fuscata, which live at the northern end of the habitat of the species, were investigated using 33 electrophoretically detectable blood protein loci. Among the loci examined, six were polymorphic. The average heterozygosity per individual was calculated as 0.0442. This was the highest value among all troops of Japanese macaques so far investigated. The mainland macaques of the Shimokita A1 troop were more differentiated genetically from other mainland macaque troops than were Yaku macaques, the subspeciesM. f. yakui.     

A morphometric analysis of the Japanese macaque (Macaca fuscata) mandibular cheek teeth from the Torihama Shell-midden, Early Jomon Period, Fukui Prefecture, Japan

We quantitatively examined the differences in the size and proportion of the Japanese macaque (Macaca fuscata) by comparing the Early Jomon specimens from Torihama shell-midden, Fukui Prefecture and modern specimens from Fukui Prefecture. The purpose of this study was to explore the temporal change in the proportion and size of teeth of the Japanese macaques based on the quantified data. The result of measurements of lower premolars and molars demonstrated that sexual dimorphism was evident only among the modern specimens where the females were significantly smaller than males. The size of male Torihama specimens was within the range of the modern population, whereas the size of the female Torihama specimens was significantly larger than the modern female population. The proportional pattern of premolars and molars for male and female Torihama specimens also differed. The results may suggest a possible difference in the degree of size reduction between males and females since the last glacial period.Morphometric analysis of mandibular cheek teeth from Torihama Shell-midden     

Changes of dominance rank,age, and tenure of wild Japanese macaque males in the Kinkazan a troop during seven years

Male age-rank and tenure-rank relationships were studied for seven years in unprovisioned Japanese macaque (Macaca fuscata fuscata) troop on Kinkazan Island, Japan. Males whose estimated ages were between 15 and 19 yr old monopolized the highest ranks, while older males whose estimated ages were ≥ 20 yr old tended to decline in rank, resulting in a humped age-rank curve. The ranks of males tended to rise as their tenure in the troop increased. The departure of higher-ranking males was the social mechanism for changes in rank, suggesting that the disappearance of higher-ranking males plays an important role in determining rank dominance.