Unity in diversity: Lessons from macaque societies

The macaque radiation is as old as the hominin radiation, approximately 7 million years. After Homo, Macaca has the widest geographical range among primates, and both of these genera are present in tropical and temperate regions as well. Whereas the single extant representative of the genus Homo diverged through processes of cultural diversification, extant species of macaques emerged through processes of evolutionary diversification. Macaque societies are characterized by profound unity and great diversity, and can best be described as variations on the same theme. To understand macaque variation and adaptation, we must take into account the processes that insure the persistence of their societies across generations and environments.     

Non‐territorial Macaques Can Range Like Territorial Gibbons When Partially Provisioned With Food

Human food supplementation can affect components of animal socioecology by altering the abundance and distribution of available food. We studied the effect of food supplementation by comparing the ranging patterns and intergroup interactions of two groups of northern pigtailed macaques (Macaca leonina), a non‐territorial primate species. One group was partially reliant on food provisioning, whereas the other group foraged wild food. We also compared the macaques’ movement with that of a group of white‐handed gibbons (Hylobates lar), a territorial species inhabiting the same site. Home range, core area, and daily path lengths were significantly smaller for the semi‐provisioned group than for the wild‐feeding group. In contrast to wild‐feeding macaques, supplemented macaques showed higher fidelity to home range, core area, and particularly to the region where human food was most accessible and abundant. The relationship of daily path length and home range indicated a low defendability index for wild‐feeding macaques; the higher index for the semi‐provisioned group was consistent with the territorial pattern found in gibbons. Semi‐provisioned macaques showed further traits of territoriality with aggression during intergroup encounters. These findings indicate that human modification of food availability can significantly affect movement patterns and intergroup competition in macaques. The observed ranging dynamics related to food provisioning may decrease the efficiency of macaques as seed dispersers and increase predation on their home range, and thus have important consequences for plant regeneration and animal diversity.     

Interactions between visitors and Formosan macaques (Macaca cyclopis) at Shou‐Shan Nature Park,Taiwan

Ecotourism involving feeding wildlife has raised public attention and is a controversial issue, especially concerning nonhuman primates. Between July 2002 and April 2005, the behavior of monkeys and tourists was collected through scan samplings, focal samplings and behavior samplings at the Shou‐Shan Nature Park located in Taiwan's second largest city—Kaohsiung. In addition, the number of tourists and monkeys was counted in different hours and places within the park. Four hundred visitors were interviewed using a questionnaire to gather data on sex, age, purpose and frequency of visit to the park. The number of tourists was significantly higher during weekends than in weekdays in all locations. Humans dominated in the initiation of interspecies interactions—the overall ratio of human‐initiated and monkey‐initiated interactions was 2.44:1. Human–monkey conflicts accounted for only 16.4% of the total interactions (n=2,166), and adult human males and adult male macaques participated in higher rates than other age/sex groups in these conflicts. Visitors showed more affiliative behavior (15.9%) than agonistic behavior (8%) toward the macaques. In response to visitors' threat or attack, the Formosan macaques mostly showed submissive behavior with bared teeth, squealed or ran away to avoid confrontation (69.1%)—only few responded with counteraggression (18.7%). This study for the first time provided evidence that food provisioning increased both the frequency and duration of aggression among Formosan macaques (P<0.001). During food provisioning, the average frequency and the duration of agonistic events of macaques were more than 4 times higher compared with those without food provisioning. The average frequency of food provision by tourists was 0.73 times/hr—more than twice the incident that monkeys grabbed the food from tourists (0.34 times/hr). If people refrain from feeding monkeys and destroying the city park's natural vegetation, monkeys can be used to educate public about nature conservation in an urban setting. Am. J. Primatol. 71:214–222, 2009. © 2008 Wiley‐Liss, Inc.     

Normal hematological indices, blood chemistry and histology and ultrastructure of pancreatic islets in the wild Indian bonnet monkeys (Macaca radiata radiata)

The present study is aimed at determining some haematological and biochemical parameters in the wild Indian bonnet monkeys as also the microscopic and ultrastructural characteristics of their pancreatic islets. Adult wild Indian bonnet monkeys (Macaca radiata radiata) of both sexes weighing between 2.5 and 4 kg were used in these experiments. Their platelet, reticulocyte and total leukocyte counts and the blood concentrations of hemoglobin and plasma proteins and the serum concentrations of aspartate amino transferase, alanine amino transferase and calcium are similar to the values reported for M. mulatta. Plasma glucose is lower when compared with reported values of M. mulatta and M. fascicularis. Insulin levels are comparable with those of M. mulatta and M. nigra. Histology of islets is similar to that of humans. Ovoid cell collections of islet cells are scattered throughout the pancreas. Ultrastructure of A, B and D cells is similar to humans. These findings suggest that this relatively underutilized macaques may be a suitable model for biomedical research.     

Mitochondrial DNA Diversity in two populations of Taiwanese macaque (Macaca cyclopis)

Current genetic composition of a population is influenced by site-specific demographic history. We compared genetic diversity in two populations of Taiwanese macaques (Macaca cyclopis) with different site characteristics. Mitochondrial DNA variation in 145 individuals from one central, continuous population (Yushan) and one peripheral, isolated population (Shoushan) was ascertained by sequencing and PCR–SSCP of the 5 end hypervariable segment of the control region amplified from hair and fecal samples. All the samples from Yushan were of the same haplotype whereas those from Shoushan fell into 13 haplotypes. The mtDNA homogeneity in Yushan may indicate a local concentration of troops status of the population or the result of population bottleneck in the recent past by severe hunting. The relatively higher genetic diversity in the Shoushan population was contributed by released or escaped captive macaques. In addition, a simple method for preserving fecal sample as a DNA source is also recommended in the study.     

Energetic costs of bipedal and quadrupedal walking in Japanese macaques

We investigated the energetic costs of quadrupedal and bipedal walking in two Japanese macaques. The subjects were engaged in traditional bipedal performance for years, and are extremely adept bipeds. The experiment was conducted in an airtight chamber with a gas analyzer. The subjects walked quadrupedally and bipedally at fixed velocities (<5 km/hr) on a treadmill in the chamber for 2.5-6 min. We estimated energy consumption from carbon dioxide (CO2) production. While walking bipedally, energetic expenditure increased by 30% relative to quadrupedalism in one subject, and by 20% in another younger subject. Energetic costs increased linearly with velocity in quadrupedalism and bipedalism, with bipedal/quadrupedal ratios remaining almost constant. Our experiments were relatively short in duration, and thus the observed locomotor costs may include presteady-state high values. However, there was no difference in experimental duration between bipedal and quadrupedal trials. Thus, the issue of steady state cannot cancel the difference in energetic costs. Furthermore, we observed that switching of locomotor mode (quadrupedalism to bipedalism) during a session resulted in a significant increase of CO2 production. Taylor and Rowntree ([1973] Science 179:186-187) noted that the energetic costs for bipedal and quadrupedal walking were the same in chimpanzees and capuchin monkeys. Although the reason for this inconsistency is not clear, species-specific differences should be considered regarding bipedal locomotor energetics among nonhuman primates. Extra costs for bipedalism may not be great in these macaques. Indeed, it is known that suspensory locomotion in Ateles consumes 1.3-1.4 times as much energy relative to quadrupedal progression. This excess ratio surpasses the bipedal/quadrupedal energetic ratios in these macaques.     

分子标记在猕猴遗传多样性研究中的应用

分子标记目前已成为研究遗传多样性的主要工具,为此,简要综述了几种常用的分子标记(RFLPs、RAPD、mtDNA、微卫星DNA、SNPs)的检测方法及其在猕猴种群遗传多样性研究中的应用,为国内猕猴遗传多样性的研究提供参考。     

Evolutionary and biochemical differences between human and monkey acidic mammalian chitinases

Acidic mammalian chitinase (AMCase), an enzyme implicated in the pathology of asthma, is capable of chitin cleavage at a low pH optimum. The corresponding gene (CHIA) can be found in genome databases of a variety of mammals, but the enzyme properties of only the human and mouse proteins were extensively studied. We wanted to compare enzymes of closely related species, such as humans and macaques. In our attempt to study macaque AMCase, we searched for CHIA-like genes in human and macaque genomes. We found that both genomes contain several additional CHIA-like sequences. In humans, CHIA-L1 (hCHIA-L1) is an apparent pseudogene and has the highest homology to CHIA. To determine which of the two genes is functional in monkeys, we assessed their tissue expression levels. In our experiments, CHIA-L1 expression was not detected in human stomach tissue, while CHIA was expressed at high levels. However, in the cynomolgus macaque stomach tissue, the expression pattern of these two genes was reversed: CHIA-L1 was expressed at high levels and CHIA was undetectable. We hypothesized that in macaques CHIA-L1 (mCHIA-L1), and not CHIA, is a gene encoding an acidic chitinase, and cloned it, using the sequence of human CHIA-L1 as a guide for the primer design. We named the new enzyme MACase (Macaca Acidic Chitinase) to emphasize its differences from AMCase. MACase shares a similar tissue expression pattern and pH optimum with human AMCase, but is 50 times more active in our enzymatic activity assay. DNA sequence of the mCHIA-L1 has higher percentage identity to the human pseudogene hCHIA-L1 (91.7%) than to hCHIA (84%). Our results suggest alternate evolutionary paths for human and monkey acidic chitinases.     

Identification of Country of Origin and Admixture Between Indian and Chinese Rhesus Macaques

We describe a restriction analysis that distinguishes between rhesus macaques of unmixed Indian and Chinese ancestry and between western and eastern Chinese ancestry. We amplified a 254-bp fragment of mitochondrial DNA (mtDNA) that contains restriction sites hypothesized to be diagnostic of country of origin for samples from 534 and 567 individuals alleged to be of solely Indian or solely Chinese origin, respectively. After digestion with the MaeIII, SmlI, and BccI restriction enzymes, the polymerase chain reaction (PCR) products of only 3 of the 1101 samples exhibited restriction patterns uncharacteristic of their alleged country of origin. A sample comprising 392 of these rhesus macaques was genotyped for 24 nuclear microsatellite (STR) loci. Principal coordinates analysis confirmed marked genetic similarity of regional populations within each country but a substantial difference between Indian and Chinese rhesus macaques. Using STRUCTURE (Pritchard and Wen, 2003),we assigned probabilities of Chinese and Indian ancestry to each sample based on its STR genotypes. We assigned all the unmixed rhesus macaques to their correct countries of origin with probabilities >0.95. We constructed an artificial sample of 1st-generation hybrid Indian/Chinese rhesus macaques by randomly sampling from the genotypes of Indian and Chinese individuals. STRUCTURE assigned robabilities of Chinese and Indian ancestry to hybrids that closely corresponded with the proportions of alleles in that sample drawn from unmixed Chinese and Indian rhesus macaques.     

Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal

Indian-origin rhesus macaques (Macaca mulatta) have long served as an animal model for the study of human disease and behavior. Given the current shortage of Indian-origin rhesus, many researchers have turned to rhesus macaques from China as a substitute. However, a number of studies have identified marked genetic differences between the Chinese and Indian animals. We investigated the genetic characteristics of a third rhesus population, the rhesus macaques of Nepal. Twenty-one rhesus macaques at the Swoyambhu Temple in Kathmandu, Nepal, were compared with more than 300 Indian- and Chinese-origin rhesus macaques. The sequence analyses of two mitochondrial DNA (mtDNA) loci, from the HVS I and 12 S rRNA regions, showed that the Nepali animals were more similar to Indian-origin than to Chinese-origin animals. The distribution of alleles at 24 short tandem repeat (STR) loci distributed across 17 chromosomes also showed greater similarity between the Nepali and Indian-origin animals. Finally, an analysis of seven major histocompatibility complex (MHC) alleles showed that the Nepali animals expressed Class I alleles that are common to Indian-origin animals, including Mamu-A*01. All of these analyses also revealed a low level of genetic diversity within this Nepali rhesus sample. We conclude that the rhesus macaques of Nepal more closely resemble rhesus macaques of Indian origin than those of Chinese origin. As such, the Nepali rhesus may offer an additional resource option for researchers who wish to maintain research protocols with animals that possess key genetic features characteristic of Indian-origin rhesus macaques.