Yuzuru Hamada

Differential Prefrontal White Matter Development in Chimpanzees and Humans

A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.

Contribution of the maxillary sinus to the modularity and variability of nasal cavity shape in Japanese macaques

The nasal cavity is essential for conditioning of inspired air, and its form likely impacts its function. Since humans and other anthropoids have reduced nasal turbinates when compared to other mammals, variation in relative surface area is mainly brought about by changes to overall nasal architecture. Previous studies of modern humans suggest that variation in the transverse dimensions of the nasal cavity is likely possible because of the presence of the maxillary sinuses. To understand the evolutionary origin of this adaptation, we investigated the nasofacial skeleton of Japanese macaques (Macaca fuscata). We applied computed tomography and geometric morphometrics to test how the nasal cavity shape is correlated with relative maxillary sinus volume and to evaluate how the nasal cavity shape is integrated with the external craniofacial shape. Our results show that the decreasing sinus volume is well associated with the relative expansion of nasal cavity at the middle region compared to the anterior and posterior openings. The nasal cavity shape is not integrated with the external craniofacial shape especially at the middle region as well as the posterior opening. Thus, the maxillary sinus in macaques may contribute to the modularity and variability of the nasal cavity shape, possibly facilitating the adaptive changes in the nasal airways of this species.

A photogrammetric method to evaluate nutritional status without capture in habituated free-ranging Japanese macaques (Macaca fuscata): a pilot study.

The quantification of nutritional status (e.g., total body fat) of animals is difficult, because the linear dimension (body length) required for the calculation of proxy parameters, such as the physique or body mass indices, cannot be measured without capture. One solution is photogrammetry of body length, provided the following two criteria are met: (1) the camera axes and subject are oriented vertically, and (2) anatomical landmarks are easily identified with low measurement error. By modifying Mori’s (Primates 20:371–397, 1979) approach, we devised an accurate photogrammetric method that uses a horizontal bar with an attached ruler for the monkey to traverse, and the anatomical landmarks of the eye and upper border of the ischial callosity to measure body length. We tested the applicability of this method on 11 adult female, habituated, free-ranging Japanese macaques (Macaca fuscata). Somatometric body length (crown–rump length and anterior trunk length) was statistically compared with the body length obtained using photogrammetry. The significant correlation of the photogrammetric body length with each somatometric measurement verified that the former could be employed to calculate various indices that are used to characterize fat mass (nutritional status) in Japanese macaques. The advantages and disadvantages of photogrammetry are also discussed.

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 Mffu2009×u2009Mfa 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 (Pu2009<u20090.05). 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.

Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding

We determined the magnitude of isotopic fractionation of carbon and nitrogen stable isotope ratios (as enrichment factors, Δδ13C and Δδ15N, respectively) between the tissues and diets of captive Japanese macaques (Macaca fuscata) using a controlled feeding experiment, to provide basic data for reconstructing their feeding habits. The Δδ13C and Δδ15N values, respectively, were 0.9xa0±xa00.2xa0‰ (meanxa0±xa0standard deviation, SD) and 3.0xa0±xa00.3xa0‰ for whole blood, 1.3xa0±xa00.2xa0‰ and 4.3xa0±xa00.3xa0‰ for plasma, and 0.8xa0±xa00.2xa0‰ and 3.0xa0±xa00.2xa0‰ for red blood cells. However, the Δδ13C and Δδ15N values for hair were 2.8xa0±xa00.3xa0‰ and 3.4xa0±xa00.2xa0‰, respectively. No difference was detected in the δ13C and δ15N values of hair sampled from different parts of the body. We investigated the effects of diet on δ13C in growing hair by alternating the diet of the macaques each month between two diets that differed markedly in δ13C. Hair regrown after shaving repeatedly recorded the δ13C of the diet consumed during the time of hair growth. On the other hand, hair naturally grown during the diet-change experiment did not show a clear pattern. One possible reason is that the hair had grown abnormally under unnatural indoor conditions and showed complicated isotope signatures. To reconstruct the long-term feeding history of Japanese macaques, we need to further clarify the relationships between the stable isotope signature of diet and various body tissues.

Variability of tail length in hybrids of the Japanese macaque (Macaca fuscata) and the Taiwanese macaque (Macaca cyclopis)

In primates, tail length is subject to wide variation, and the tail may even be absent. Tail length varies greatly between each species group of the genus Macaca, which is explained by climatic factors and/or phylogeographic history. Here, tail length variability was studied in hybrids of the Japanese (M. fuscata) and Taiwanese (Macaca cyclopis) macaque, with various degrees of hybridization being evaluated through autosomal allele typing. Relative tail length (percent of crown–rump length) correlated well with the number of caudal vertebrae. Length profiles of caudal vertebrae of hybrids and parent species revealed a common pattern: the length of several proximal-most vertebrae do not differ greatly; then from the third or fourth vertebra, the length rapidly increases and peaks at around the fifth to seventh vertebra; then the length plateaus for several vertebrae and finally shows a gentle decrease. As the number of caudal vertebrae and relative tail length increase, peak vertebral length and lengths of proximal vertebrae also increase, except that of the first vertebra, which only shows a slight increase. Peak vertebral length and the number of caudal vertebrae explained 92xa0% of the variance in the relative tail length of hybrids. Relative tail length correlated considerably well with the degree of hybridization, with no significant deviation from the regression line being observed. Thus, neither significant heterosis nor hybrid depression occurred.

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.

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

OBJECTIVESnHybridization 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.nnnMATERIALS AND METHODSnWe 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.nnnRESULTSnChinese 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.nnnDISCUSSIONnThe 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.

Use of photogrammetry as a means to assess hybrids of rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques are the most commonly used non-human primate models for biomedical research, but it is difficult to identify these two species in the hybrid zone (15–20°N). In this work, we used morphological values obtained via photogrammetry to assess hybrids of rhesus and long-tailed macaques at Khao Khieow Open Zoo (KKZ; 13°21′N, 101°06′E), eastern Thailand. Long-tailed and rhesus macaques have species-specific tail lengths and contrasts of their yellowish pelages. The accuracy and precision of the relative tail length (%RTL) and the contrast of the yellow hue (Cb*) of the pelage, as obtained from photographs, were compared with the corresponding direct measurements (morphometrics). The photogrammetric and morphometric measurements of %RTL and Cb* were highly significantly correlated (rxa0=xa00.989 and 0.980, pxa0<xa00.001), and there were no significant differences between the two datasets (t test, pxa0=xa00.13 and 0.41; nxa0=xa042 and 17 for %RTL and Cb*, respectively). The reproducibilities of the %RTL and Cb* measurements (calculated in the photogrammetric case by taking photographs of the same macaques in two different environments) were significantly correlated between the datasets (rxa0=xa00.983 and 0.914, pxa0<xa00.001 and 0.005), and there were no significant differences between the datasets (t test, pxa0=xa00.539 and 0.344; nxa0=xa030 each for %RTL and Cb*, respectively). The %RTL and Cb* data were combined with data on the crown and cheek hair patterns and sex skin reddening of the macaques, and this combined data set was then analyzed by multiple correspondence analysis and agglomerative hierarchical cluster analysis, leading to the categorization of the rhesus macaques, long-tailed macaques, and hybrids at KKZ into five groups. Thus, photogrammetry can be utilized to identify macaque species or hybrids when species identification relies mainly on tail length and pelage color.

Tubular anomalous bones found in both thighs of a long-tailed macaque (Macaca fascicularis)

Tubular anomalous bones were found in both thighs of a 6-year-old male long-tailed macaque (Macaca fascicularis) bred in captivity. The bones had jagged ends and protruded from the skin. Radiographs showed that they developed in the femurs at the middle and elongated. They were removed with surgery under anesthesia. Histological analysis revealed that these bones had the same histological structure as the femur, though they were composed of primary and secondary osteon regions. This finding indicated that the new bones developed from the old bone piece(s), acquired a tubular shape, and elongated. It is suggested that the anomalous bones were produced not by the congenital deformity but by regeneration from fragments of the fractured femur that were embedded in the bone marrow; these acquired a tubular pattern and elongated.