Genetic characterization of long-tailed macaques (Macaca fascicularis) on Tabuan Island Indonesia

Protein and mitochondrial DNA variations (D-loop region PCR-RFLP) were analyzed for 7 serum and 40 clot samples collected from long-tailed macaques (Macaca fascicularis) living on Tabuan Island, Indonesia. Protein polymorphisms were examined electrophoretically for 5 and 12 kinds of protein in serum and erythrocytes, respectively. Each of the protein loci tested showed a monomorphic pattern. Polymorphisms were detected in the analysis of the D-loop-containing region of mtDNA (PCR-RFLP) using 32 restriction endonucleases. Two haplotypes, differing 1.03% in sequence divergence were observed, and both were previously undetected in other local populations. Based on genetic features and differences in pelage color as outlined inFooden's (1995) morphological analysis, the present results suggest that long-tailed macaques on Tabuan Island are a unique population. From the genetic analyses performed here, Tabuan monkeys are considered to be the same species group as those populations of Sumatra and Java (Fooden, 1995).     

Blood protein variation of a new population of gelada baboons (Theoropithecus gelada), in the Southern Rift Valley, Arsi Region, Ethiopia

Blood protein polymorphism of gelada baboon (Theropithecus gelada) to the south of the Rift Valley, Arsi Region, were examined for 36 genetic loci using three electrophoresis techniques for 48 blood samples from three localities, and compared with the northern geladas. New variant alleles and genetic markers of Hb-α, PA-2, and TBPA loci were detected. The distribution patterns of the variant alleles of Hb-α, PA-2, TBPA, Pi, Gc, PGM-II, and TBPA loci were localized in the geographic regions of south and north gelada populations, respectively. Genetic variability of southern geladas was estimated as P_poly=0.083 and , which was comparable to northern geladas. A remarkably high genetic differentiation between the two geographic populations was shown byNei's genetic distance=0.071 and G_ST value=0.420. Our results of genetic analysis suggest that the southern and northern gelada populations have been separated for several hundred thousand years, and gene flow between the two geographic populations is severely restricted. The southern gelada baboon may be regarded as a distinct subspecies.     

Genetic variability within and between the troops of toque macaque,Macaca sinica,in Sri Lanka

Genetic variability within and between the troops of toque macaque in Sri Lanka was studied from a population genetical perspective. Studies were made using electrophoretical blood protein variations as markers in order to clarify the genetic characteristics of the population of this species. A total of 256 samples from 20 troops which were collected in the field in 1981 to 1982 and 1983 to 1984 were examined for 32 blood protein loci. Eleven loci, that is, Tf, Alb, TBPA, Hb-α, PHI, PGM-II, CA-I, IDH, AK, ADA, and Ch-E showed the polymorphism in one or more troops. Of these 11 loci, 7 loci, that is, Tf, TBPA, Hb-α, PHI, PGM-II, CA-I, and IDH were highly polymorphic in most troops. The genetic variability within troops were quantified as H=0.0782 in average and this value was on higher level than other primates and comparable with that of continental macaques,Macaca fascicularis, in Thailand. The genetic differentiation between troops was quantified byG _ST andF _ST and these values were relatively smaller than those of other insular macaques.     

Hemoglobin polymorphism in macaques with reference to the evolution ofMacaca fascicularis andMacaca mulatta

Blood samples were collected fromMacaca fascicularis andMacaca mulatta living in indoor breeding groups and investigated electrophoretically. Hemoglobin polymorphism was observed in both species. Isoelectric focusing was performed on urea denaturated samples to test the hypothesis of a site duplication at theα-chain locus inM. fascicularis (Barnicot et al., 1970). The results of our investigations do not support the above mentioned hypothesis. Only one locus coding theα-chain was detected, and this is under the control of two alleles. Evolutionary events at the molecular level are discussed, as well asWheatley's hypothesis (1980) that malaria was an important force behind divergence in both species. InM. fascicularis hemoglobin variants might be similarily connected with malaria resistance as in man. We suggest that this was not an important process behind speciation in macaques.     

Japanese macaque microsatellite PCR primers for paternity testing

Capture and blood sampling in wild primate populations are difficult. For this reason, we need to use DNA extracted from the hair or feces of target animals. The polymerase chain reaction (PCR) method, which amplifies small volumes of DNA, provides an ideal means for studying DNA variations in wild populations. Three sets of PCR primers which amplify highly polymorphic (GT/AC)_n dinucleotide repetitive regions were synthesized from DNA sequences of Japanese macaques (Macaca fuscata). One of the primer pairs detected at least seven alleles in one captive Japanese macaque group. Also, the fathers of four offspring whose mothers had died in a captive group of Japanese macaques were identified. In such cases, the father cannot be determined by the previous DNA fingerprinting method based on the polymorphism of minisatellite DNA. These primers were further tested with some species of the Cercopithecidae, e.g. grivet monkeys (Cercopithecus aethiops tantalus) and hamadryas baboons (Papio hamadryas). The results obtained suggest that these primers can detect stably inherited polymorphic regions in each species.     

Genetic polymorphisms of blood proteins in the troops of Japanese macaques,Macaca fuscata: VI. Serum transferrin polymorphism

As the serum transferrin polymorphism was observed in several macaque species, we considered it as one of the best markers for the study of population genetics of Japanese macaques,Macaca fuscata. In this work the genetic variants of transferrin (Tf) of 1,451 blood samples from 37 troops of this species were tested. The troops showing the variation of Tf were Fukushima, Yugawara T, Ihama, Ryozenyama, Mikata I and II, Takahama, Takahama (Otomi), Arashiyama A, Minoh A and B, Kohchi, Mihara, Shimane, and Tomogashima. The wild-type allele of this species was Tf F, and the variant alleles detected in these troops were E, G⁻, G, and H′. The alleles E, G and H′ were probably identical with those reported in several macaque species byIshimoto (1972), but the identification of allele G⁻ could not be done.     

Nineteen new microsatellite DNA polymorphisms in pigtailed macaques (Macaca nemestrina)

Microsatellite loci known to be polymorphic in baboons (Papio hamadryas) and/or humans were tested in pigtailed macaques (Macaca nemestrina) from the Washington Regional Primate Research Center. Nineteen polymorphisms were identified in the macaques, with an average of 9.2 alleles per locus and an average heterozygosity of 0.76. Seven loci were analyzed using radiolabelled PCR primers and standard gel electrophoresis. Twelve loci were studied using fluorescently labelled primers and the Perkin-Elmer ABI 377 genotyping system. Of these 19 pigtailed macaque polymorphisms, 12 were used to perform paternity testing among captive animals. In a set of 15 infants, this panel of 12 genetic polymorphisms was sufficient to establish paternity in all cases. The number of alleles per locus in pigtailed macaques was compared with the number of alleles in a sample of baboons, and no significant correlation was observed. This indicates that population genetic processes such as genetic drift and recurrent mutation act rapidly enough on these loci to eliminate any relationship in levels of polymorphism across those two species. These 19 loci will be valuable for a range of genetic studies in pigtailed macaques, including paternity testing, analysis of population structure and differentiation among wild populations, and genetic linkage mapping.     

Morphometric analysis ofMacaca arctoides andM. thibetana in relation to other macaque species

As a first step in reviewing the classification of the two stump-tailed macaque species,Macaca arctoides andM. thibetana, as compared with other species of the genusMacaca, 72 linear dental and cranial variables of 11 macaque species were examined by morphometric analyses. The results indicate that the two stump-tailed species are the largest of the macaques and although rather similar overall, they exhibit significant differences in the pattern of variation in most of the five skull regions as shown by Principal Components and Canonical Variate Analyses. Euclidean Distances based on Canonical Variate scores indicate that the females ofM. arctoides andM. thibetana are more widely separated than eight other pairs of macaque species, and that the separations of the respective males are greater than those of three other pairs of species. These findings are consistent withFooden's classification of the stump-tailed macaques as two separate species (Fooden, 1976;Fooden et al., 1985). The present results suggest, as other researchers have proposed on the basis of external features, biochemistry and genetics, that the two stump-tailed macaque species andM. assamensis are closely related. The results also tentatively imply associations withM. fuscata andM. sylvanus but these require further study. The findings have implications for the assessment of the various Chinese Pleistocene macaque fossils.     

Influence of the MHC genotype on the progression of experimental SIV infection in the Mauritian cynomolgus macaque

Experimental infection of Mauritian cynomolgus macaques by simian immunodeficiency virus is a representative model of HIV infection, currently in favour for evaluating the efficacy of new preventive or curative treatments. Extensive studies of major histocompatibility complex (MHC) polymorphism by microsatellites revealed seven haplotypes (H1–H7). We present statistical evidence of the influence of MHC polymorphism on the set-point plasma viral load (PVL). Our analysis was based on the study of 45 Mauritian cynomolgus macaques inoculated by intravenous or intrarectal injection of a 50 AID50 dose of the SIVmac251 virus. The animals received no treatment before or after the inoculation. MHC polymorphism was investigated by means of 20 microsatellites distributed across the MHC and by DRB genotyping using the DGGE sequencing method. Statistical analysis with Unphased software revealed that two markers located in the class IB region significantly influenced the Log PVL and that three class IB haplotypes were significantly associated with lower (H2 or H6) or higher (H4) set-point Log PVL values. Although the impact of MHC on Log PVL was found to be low (around one Log10), it is important to dispose of animals paired for their MHC genotypes, each animal tested for a given treatment and its untreated control, to minimize the influence of the MHC and clearly reveal the effect of the treatment.     

Blood-protein allele frequencies and phylogenetic relationships in Macaca: A review

Allele-frequency data have been assembled for 35 blood-protein loci in 17 of 19 recognized species of Macaca based on 29 published electrophoretic studies; studies of inbred captive colonies have been excluded. Data for 22 polymorphic loci are tabulated in detail for 43 geographic populations of these species. Calculated F_ST values provide a measure of intergroup genetic differentiation at various hierarchical levels—troop, locality, province, country or island, species, species group; polymorphism indices measure genetic variation. The greatest intraspecific genetic differentiation occurs at the level of island populations within species. The pattern of genetic variation among island populations appears to be relictual, suggesting that the reduced genetic variability of island populations of macaques is a result of postisolation genetic drift rather than founder effect. Interspecific relationships were investigated by means of a jackknifed Fitch-Margoliash algorithm, using Papio as outgroup. Phylogenetic inferences based on morphology and zoogeography. The reduced genetic variability that frequently characterizes insular macaque populations complicates phylogenetic interpretation of blood-protein evidence.     

Malaria in macaques

Seven species of malaria naturally infect eight species of macaques in southwestern India, Sri Lanka, and Southeast Asia. Within malarious areas, the frequency of infections in infected species of macaques varies from 9 to 61%. Natural malarial infections in macaques are relatively benign. The proved or probable vectors of macaque malaria are seven species of mosquitoes that belong to the Leucosphyrus Group of the genus Anopheles. The geographic distribution of macaque malaria apparently is determined by the distribution of the Leucosphyrus Group of mosquitoes, which in turn apparently is determined by the distribution of tropical evergreen rain forest. Experimental infections with three species of macaque malaria frequently are lethal to populations or species of macaques that inhabit areas outside the geographic ranges of the parasites. In populations or species of macaques that are sympatric with experimentally virulent species of malaria, partial resistance probably evolved as a consequence of natural selection acting on favorable mutations.     

Molecular diversity of local Norwegian meadow fescue (Festuca pratensis Huds.) populations and Nordic cultivars—consequences for management and utilisation

Genetic diversity and relatedness were studied in 30 Norwegian local populations of meadow fescue (Festuca pratensis Huds.) using amplified fragment length polymorphism (AFLP) markers. The populations were also compared with 13 Nordic meadow fescue cultivars in order to analyse the distribution of variation in local populations and cultivars and to elucidate relationships between local populations and cultivars. Analysis of molecular variance (amova) analysis showed that most of the variation was present within populations and that little variation was found between local populations and cultivars. Separate amova analyses of local populations and cultivars revealed a higher level of variation within registered cultivars than within local populations. A cluster analysis based on corrected average pairwise differences between populations showed that the populations could be divided into three clusters, of which one also contained the cultivars. These results were supported by principal coordinates analysis. The results indicate that the Norwegian meadow fescue has a narrow genetic basis and that the local populations in Norway can be divided into three groups following the most probable routes of introduction of the species into Norway. The inland populations are closely related to the cultivars and have most probably been established as a result of migration from sown meadows. The western and southern populations probably originate from human activity—for example, trade—to the coastal western and northern parts of the country and to the central parts of southern Norway.     

Microsatellite markers for an invasive tetraploid tree,Chinese tallow (Triadica sebifera)

We present six polymorphic microsatellite loci for Chinese tallow tree (Triadica sebifera, Euphorbiaceae), which is native to East Asia and is an aggressive, invasive species in the southeastern USA, particularly along the Coastal Plain. Microsatellite loci were tested for polymorphism across a total of 79 individuals from populations across the native range of China and in introduced populations of the southeastern USA, California, Hawaii, and Australia. Across these samples, we found a high level of polymorphism, suggesting they will be useful for deducting the introduction history of this invasive species.     

Blood groups of bonnet macaques (Macaca radiata), with a brief introduction to seroprimatology

The human-type A-B-O blood groups of 52 bonnet macaques (Macaca radiata) were determined. Application of method of population genetics indicated the gene frequences to be O = 0.173, A = 0.480 and B = 0.347. Cross testing of sera and red cells of the bonnet macaques revealed two blood-type-specific isoagglutinins, one of them strong enough for use as a blood typing reagent. No blood group polymorphism was revealed by testing bonnet macaque red cells with isoantisera produced in rhesus monkeys (M. mulatta) and in crab-eating macaques (M. fascicularis). The rhesus and crab-eating macaque isoantisera reacted either with all or with none of the bonnet macaque red cells tested.     

Diversity of TRIM5α and TRIMCyp sequences in cynomolgus macaques from different geographical origins

The TRIM5α restriction factor can protect some species of monkeys, but not humans, from HIV infection. It has also emerged that some monkeys have a cyclophilin A domain retrotransposed into the TRIM5 locus resulting in the expression of a TRIMCyp protein with anti-retroviral activity. A high degree of sequence variation in the primate TRIM5 gene has been reported that varies between populations of rhesus macaques, a widely used non-human primate model of HIV/AIDS, and recently shown to correlate with susceptibility to simian immunodeficiency viruses in this species. Cynomolgus macaques are also used widely in HIV research. A non-indigenous population on Mauritius has highly restricted genetic diversity compared with macaques from Indonesia. The relative allelic diversity of TRIM5α and TRIMCyp within these two sub-populations may impact on the susceptibility of the macaques to simian immunodeficiency virus thereby influencing the outcome of studies using these monkeys. We sought to establish the genetic diversity of these alleles in cynomolgus macaques. We identified seven TRIM5α alleles in Indonesian macaques, three of which are novel, but only three in the Mauritian-origin macaques. Strikingly, 87% of Indonesian, but none of the Mauritian macaques, possessed a retrotransposed Cyp domain. A splice acceptor site single-nucleotide polymorphism that allows formation of a TRIMCyp protein was absent for the TRIM5α alleles found in the Mauritian macaques. The level of allelic diversity reported here is greater than previously proposed for cynomolgus macaque species.     

Biometrical variability of foliage and cone characters inCupressus bakeri (Cupressaceae)

Biometrical variability of foliage, cones, and seeds were analyzed in 8 native populations (throughout the range) of a relictual species,Cupressus bakeri Jeps. (Cupressaceae) from California and Oregon. The partition of variation within and among populations for this rare plant was investigated and the justification for subspecies status was reviewed. Morphological characters varied significantly, with more of the variation among populations than at the population level. Multivariate analyses indicated close affinities among populations on serpentine sites suggesting the presence of a serpentine race. However, the high degree of variation among populations did not permit their clear separation into the two subspecies described byWolf (1948). We conclude thatC. bakeri should be treated as a monotypic species.     

Chromosomal polymorphism in natural populations of Drosophila pavani

Summary D. pavani Brncic 1957, is a neotropical species found in Chile and in a part of Argentina along the eastern slope of the Andes. The present paper describes the mitotic and salivary gland chromosomes of this species and gives a composite map of the Standard gene arrangement.Natural populations ofD. pavani are polymorphic with respect to the gene orders in their chromosomes. The observed variations in the gene arrangements are due to complex included and overlapping paracentric inversions. In none of the populations or in the crosses studied were found the hypothetical intermediate steps needed for the establishment of the phylogeny of the gene orders present in nature.The qualitative and quantitative data on the distribution and frequency of inversions show no pronounced geographic variations. The high incidence of inversion heterozygotes and the absence of the intermediate steps between the gene arrangements found in nature, seem to indicate an adaptive nature of the polymorphism observed inD. pavani This work has been supported in part by a grant from the Rockefeller Foundation.     

喀斯特石山生境中熊猴的雨季食物组成

开展食物组成研究为人们了解灵长类对栖息地的反应提供了很好的途径,对深刻理解动物的行为可塑性及适应性具有重要意义。猕猴属(Macaca)为果食性灵长类,但是不同种类的食性差异很大;即使便同一物种,其不同地理种群也因其栖息环境不同,食物组成存在差异。一般说来,热带地区的种类比生活在较高纬度的种类采食更多的果实。于2012年7—9月,采用瞬时扫描法对广西弄岗自然保护区石山中的两群熊猴(Macaca assamensis)进行了跟踪和观察,对猴群的雨季食物组成及其日时段变化规律进行了研究。结果表明:研究期间熊猴共采食45种植物,其中乔木30种,灌木3种,藤本11种,草本1种。平均每月采食植物22.3种。嫩叶和果实是熊猴的主要食物,分别占食物组成的52.4%和46.1%(其中未成熟果实占21.3%,成熟果实占24.8%)。另外,花占食物组成的0.9%,成熟叶和其它部位分别占0.3%。石山特有植物芸香竹(Bonia saxatilis)的嫩叶提供了43.8%的食物。9种主要植物分别占食物组成的2%,共为猴群提供了85.5%的食物。分析还发现熊猴并不是严格按照环境中的植物生物量来选择食物。嫩叶在弄岗熊猴的食物中的比例高于其他地理种群,而果实低于其他地理种群,这可能与喀斯特石山中果实的丰富度和可利用性较低有关。熊猴一天中不同时间段的食物组成并不相同,主要表现在:熊猴上午时间段对成熟果实和总果实的采食比例高于下午时间段,而嫩叶的采食比例低于下午时间段。另外,不同时间段的食物组成受外界温度的影响,表现为温度与嫩叶的觅食比例成正比,与成熟果实和总果实的觅食比例成反比。这可能与猴群采取的能量平衡策略有关。对熊猴的食物组成的日时段变化规律进行首次报道,研究结果将有助于深入理解熊猴对喀斯特石山生境的适应策略。     

Comparative genetics of a highly divergent DRB microsatellite in different macaque species

The DRB region of the major histocompatibility complex (MHC) of cynomolgus and rhesus macaques is highly plastic, and extensive copy number variation together with allelic polymorphism makes it a challenging enterprise to design a typing protocol. All intact DRB genes in cynomolgus monkeys (Mafa) appear to possess a compound microsatellite, DRB-STR, in intron 2, which displays extensive length polymorphism. Therefore, this STR was studied in a large panel of animals, comprising pedigreed families as well. Sequencing analysis resulted in the detection of 60 Mafa-DRB exon 2 sequences that were unambiguously linked to the corresponding microsatellite. Its length is often allele specific and follows Mendelian segregation. In cynomolgus and rhesus macaques, the nucleotide composition of the DRB-STR is in concordance with the phylogeny of exon 2 sequences. As in humans and rhesus monkeys, this protocol detects specific combinations of different DRB-STR lengths that are unique for each haplotype. In the present panel, 22 Mafa-DRB region configurations could be defined, which exceeds the number detected in a comparable cohort of Indian rhesus macaques. The results suggest that, in cynomolgus monkeys, even more frequently than in rhesus macaques, new haplotypes are generated by recombination-like events. Although both macaque species are known to share several identical DRB exon 2 sequences, the lengths of the corresponding microsatellites often differ. Thus, this method allows not only fast and accurate DRB haplotyping but may also permit discrimination between highly related macaque species.