Phylogeny of Snub-Nosed Monkeys Inferred from Mitochondrial DNA,Cytochrome B,and 12S rRNA Sequences

Snub-nosed monkeys (Rhinopithecus spp.) are confined to isolated mountainous regions in China and North Vietnam. Their systematic classification and phylogenetic relationship has been controversial. The structures of mitochondrial DNA cytochrome b and 12S rRNA show that the 4 species of Rhinopithecus are quite different from other colobines. It is reasonable to regard them as an independent genus, as determined by external features, morphometric characters and behavior. However, whether or not there should be a subdivision between the Vietnamese and Chinese species at the subgeneric level remains to be clarified; more evidence from a large range of Asian colobine species is needed. The Guizhou species, Rhinopithecus brelichi, is a valid species, which is more closely related to Pygathrix than the other species ( R. roxellana, R. bieti and R. avunculus) are. Results also indicate that 3 species—Rhinopithecus roxellana, R. bieti and R. avunculus—might have diverged from R. brelichi, but the phylogenetic relationship of R. avunculus is not clear.     

Systematic classification of Asian colobines

In order to study the differentiation of Asian colobines, fourteen variables were analysed in one way, on 123 skulls, includingRhinopithecus, Presbytis, Presbytiscus, Pygathrix, andNasalis with both cluster and differentiated functions tests. Information on paleoenvironment changes in China and South-East Asia since late Tertiary have been used to examine the influences of migratory habits and the distribution range in Asian colobines. The cladogram among different Asian colobines genera was made from the results of various analysis. Some new points or revisions were suggested: 1. Following the second migratory way, ancient species of Asian colobines perhaps passed through Xizang along the northern bank of Tethis sea and Heng-Duan Shan regions, across Yunnan into Vietnam, since the ancient continent between Yunnan and Xizang was already located in on eastern bank of Tethis sea. Thus, during the evolution, Asian colobines must have had two original centres, i.e. “Sundaland” and Heng-Duan Shan Chinese regions; 2. Pygatrix possesses a lot of cranial features more similar toPresbytiscus than toRhinopithecus. The small difference from the modification combinesPygatrix with other two genera as shown by Groves (1970), but it is better to putPygatrix andPresbytiscus together as one genus; 3.Nasalis (2n=48) may be the most primitive genus within Asian colobines. Some features shared withRhinopithecus, for example body size, terrestrial activities, limb proportion etc. ...seem to be considered as a common inheritance of symlesiomorphus characters; 4.Rhinopithecus, with reference to cranioface and cranium or to its origin, is a special genus of Asian colobine. It may represent the highest level of evolutionary position within various genera (Peng et al., 1985).     

Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences

DNA sequence data of the nuclear-encoded gamma1-gamma2-globin duplication region were used to examine the phylogenetic relationships of 16 cercopithecid (Old World monkey) species representing 12 extant genera. Morphology- and molecular-based hypotheses of Old World monkey branching patterns are generally congruent, except for generic relationships within the subtribe Papionina. The cercopithecids divide into colobines (leaf-eating monkeys) and cercopithecines (cheek-pouched monkeys). The colobines examined by the DNA data divide into an Asian clade (Nasalis, proboscis monkeys; Trachypithecus, langurs) and an African clade (Colobus, colobus monkeys). The cercopithecines divide into tribes Cercopithecini (Erythrocebus, patas monkey; Chlorocebus, green monkeys; Cercopithecus, guenons) and Papionini. Papionins divide into subtribes Macacina (Macaca, macaques) and Papionina (Papio, hamadryas baboons; Mandrillus, drills and mandrills; Theropithecus, gelada baboons; Lophocebus, arboreal mangabeys; Cercocebus, terrestrial mangabeys). In a morphologically based classification, Mandrillus is a subgenus of Papio, whereas Lophocebus is a subgenus of Cercocebus. In contrast, the molecular evidence treats Mandrillus as a subgenus of Cercocebus, and treats both Theropithecus and Lophocebus as subgenera of Papio. Local molecular clock divergence time estimates were used as a yardstick in a "rank equals age" system to propose a reduction in taxonomic rank for most clades within Cercopithecidae.     

亚洲疣猴与猕猴牙齿的比较

为了研究亚洲疣猴牙齿形态与功能适应性之间的关系,建立异速生长公式比较分析生活于同一大陆的猕猴。主成份分析用来分析来自异速生长公式的残差。结果表明:疣猴出乎意料地展示了比猕猴更小的门齿。导致此结果的可能原因是:疣猴与猕猴之间的食物差异性。但是,这种差异小于亚-非大陆种类。也就是说,在过去的500万年左右的时间里,生活于同一大陆的疣猴和猕猴已经产生了一些对环境和食性的趋同性。当每一个疣猴属分别与猕猴进行比较时,它们之间的差异性揭示了地理分布的差异。金丝猴(Rhinopithecus)和长尾叶猴(Semnopithecus)具有比其他疣猴发达的臼齿。欧氏距离的结果说明疣猴和猕猴牙齿的差异性揭示了它们在系统发育方面的关系。     

A Phylogeny of Chinese Leaf Monkeys Using Mitochondrial ND3-ND4 Gene Sequences

The phylogeny of Chinese leaf monkeys, especially the snub-nosed monkeys (Rhinopithecus), has not been thoroughly investigated using molecular sequence data, perhaps due to their rarity in the wild and their poor representation in institutional collections. Despite several proposed classifications, systematic relationships of these species remain poorly defined and this has hindered their conservation. To clarify the phylogenetic relationships of the leaf monkey clade in China, we sequenced the mitochondrial ND3, ND4L, ND4, tRNA ^Arg , tRNA ^His , tRNA ^Ser , and tRNA ^Leu genes for Rhinopithecus bieti, R. roxellana, Trachypithecus francoisi, T. f. leucocephalus, and T. phayrei as well as Pygathrix nemaeus and Colobus guereza. We included a total of 2252 characters for each individual, excluding gaps in primary sequences. Our interpretation of the results from character-and distance-based phylogenetic analyses suggest that (1) Pygathrix nemaeus is sister to Rhinopithecus rather than to Trachypithecus though it is quite divergent from the former; (2) the Yunnan snub-nosed monkey, Rhinopithecus bieti, represents a valid species; (3) the white-headed leaf monkey is not a distinct species, but instead is a subspecies of Trachypithecus francoisi (T. f. leucocephalus), though it should still be considered a separate evolutionary significant unit (ESU); and (4) because two individuals of the Phayrei's leaf monkey, T. phayrei, are genetically distinct from one another, a more extensive revision of the taxonomy of this putative species in China is needed. These results, plus ongoing work on the molecular systematics of the entire Asian leaf monkey radiation, can provide a sound basis for identifying the appropriate units of conservation for this endangered group of primates.     

Asian colobine social structure: Ecological and evolutionary constraints

Both ecological and phylogenetic factors and their interaction influence primate social structure. Food resources, in particular, affect social structure parameters such as sex/age composition, group size, home range size, and individual density. As a group, the Asian colobines may be partially buffered from the impact of food constraints on social structure, given their specialized digestive physiology. Asian colobines are able to subsist on mature foliage, a relatively abundant and non-patchily distributed resource, when preferred foods are not available. In food limited populations, increases in group size or density should cause increases in home range size. We did not find this relationship for Asian colobines, however, and thus it would appear that the majority of Asian colobine populations are below carrying capacity. Food may be less of a limitation to populations than other factors, such as social stress. The formation of bands (associations between relatively stable groups) has been documented for bothNasalis andRhinopithecus, and based on recent data for severalPresbytis andTrachypithecus species, we predict that band formation is the norm for the Asian colobines, includingPygathrix. Group home ranges forPresbytis andTrachypithecus species typically overlap and both intergroup tolerance and intergroup aggression are observed. This suggests that groups form differentiated relationships, tolerating some groups but not others. Such differentiated relationships are the foundation of band formation.     

Mandibular morphometric variation among Chinese cercopithecoids and the unique structure of the snub-nosed monkey (<Emphasis Type="Italic">Rhinopithecus</Emphasis>) mandible

In order to understand how mandibular structure differs among the Chinese cercopithecoids (Rhinopithecus, Trachypithecus and Macaca), particularly the uniqueness of the snub-nosed monkeys (Rhinopithecus), we analysed ten mandibular measurements by principal components analysis (PCA), and examined scaling patterns. The results provided by the PCA illustrated differences due to size among the cercopithecoids and the relationship between colobines (Trachypithecus and Rhinopithecus) and cercopithecines, in which macaques (Macaca) are included. Allometric analysis indicated that, biomechanically, there is not a marked difference between macaques and leaf-eating monkeys. This may be associated with the fact that both share some similar ecology and niches in south and southwest China. The snub-nosed monkeys exhibit a significantly more robust mandible, evident in the symphysis, corpus, condyle, and masticatory momentum arm. This supports the hypothesis, based on the study of dental structure, that Rhinopithecus is a unique group in Asian Old World monkeys (OWMs) and has developed some unique characteristics in order to adapt to the tough food available in the severe cold climate of the Plateaux of Qinghai-Tibet, Yun-Gui and Qingling in China.     

Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus)

I aim to explicate the pattern of differences and relations between the sexes in two groups ofC. capucinus, in terms of phylogenetic, social and ecological predictors. I use three lines of evidence to develop predictions as to how male and femaleC. capucinus interact and how the sexes differ in behavior: (1) phylogenetic similarities to other species ofCebus; (2) a general model of sex differences in female-bonded social systems; and (3) ecological analogy of Old World monkeys. First, I conclude that phylogenetic affinity is a good predictor in thatC. capucinus are similar to other species ofCebus in many patterns of sex-differentiated behavior. An exception is that, unlikeC. apella andC. olivaceus, in which a single breeding male is reported to be highly conspicuous in each group,C. capucinus live in a decidedly multimale system. Secondly, the general model of sex differences in female philopatric, male-dispersal societies, which was originally developed for Old World species, also accurately predicts several aspects of social behavior inC. capucinus. Thirdly, a proposed ecological analogy betweenCercopithecus ascanius andspecies of Cebus is not substantiated in this study of C. capucinus, though the analogy is apparently well suited to the social dynamics of other species in the genusCebus.     

Snub‐nosed monkeys: Multilevel societies across varied environments

The ecology and behavior of the four species of Rhinopithecus, snub‐nosed monkeys, are rapidly becoming well known. New field studies reveal in depth the striking adaptations of these colobines. Diets range from those typical for tropical colobines to diets dominated by lichens. The monkeys form bands, at times consisting of more than 400 individuals; these bands are based on the one‐male, multi‐female units common in colobines. We review the diet, range use, and social organization of snub‐nosed monkeys, and then explore the power of socioecological theory to explain their multilevel social organization.     

Cranial morphology of the golden monkey (Rhinopithecus) and douc langur (Pygathrix nemaeus)

Because they have been less studied than most other non-human primates (partly due to the difficulties in accessing their habitat) the origins and phylogenetic relationships ofR. roxellana andR. bieti are controversial. These controversies may be clarified to some degree by adding information on the cranium. To this end, ten cranial dimensions analysed morphometrically here provide data about cranial differences among species of the genusRhinopithecus, and between species ofRhinopithecus andPygathrix nemaeus. Though more similar to each other than to any others in the same genus, the results show a significant separation betweenR. roxellana andR. bieti to the degree that they may be regarded as two different species. This confirms the conclusions of prior studies of external features, qualitative morphological characteristics and biochemical evidence (Yeet al, 1987; Zhang and Ryder, 1995; Jablonski, 1998; Penget al., 1988). The differences between these two species are mainly size-related, being highly correlated with cranial length. Other differences, probably non-size related shape differences, however, are highly correlated with cranial width. Sexual dimorphism plays a part in these findings. In relation to the other species, however, the results show that the Vietnam golden monkey (R. avunculus) has closer craniometric relationships with the douc langur (Pygathrix nemaeus) rather than with the three Chinese golden monkey species. Of these, the Gouzhou species (R. brelichi) shares more similarity withR. avunculus and is more separate fromRhinopithecus roxellana and R. bieti. The smaller differentiation between the two latter species could be due to their more recent separation following the dramatic elevation of Qinghai-Tibetan Plateau after the Middle Pleistocene.     

Biomechanical scaling of mandibular dimensions in New World Monkeys

Previous studies show that folivorous Old World monkeys have shorter, deeper mandibles and shorter, wider condyles than frugivorous ones. These morphologies have been related to leaf mastication in colobines and ingestion of large, tough fruits in cercopithecines. This study examines New World monkeys in order to determine whether they exhibit similar adaptations to diet. New World monkeys have relatively long, transversely thin mandibles and somewhat deep mandibles and narrow condyles. Except for their deep mandibles, folivorous New World monkeys (i.e., Alouatta) do not exhibit the mandibular and condylar specializations typical of cercopithecid folivores. Reliance on comparatively nonfibrous foods plus alterations in masticatory muscle ratios among New World monkeys partially accounts for observed differences between folivorous New and Old World monkeys. In addition, adaptations for howling in Alouatta appear to have a significant effect on mandibular morphology. A biomechanical interpretation of craniofacial scaling patterns suggests that the mandibles of New World monkeys are subjected to lower condylar loads and considerably less twisting of the mandibular corpus than those of comparable Old World monkeys.     

Mitochondrial data support an odd-nosed colobine clade

To obtain a more complete understanding of the evolutionary history of the leaf-eating monkeys we have examined the mitochondrial genome sequence of two African and six Asian colobines. Although taxonomists have proposed grouping the "odd-nosed" colobines (proboscis monkey, douc langur, and the snub-nosed monkey) together, phylogenetic support for such a clade has not been tested using molecular data. Phylogenetic analyses using parsimony, maximum likelihood, and Bayesian methods support a monophyletic clade of odd-nosed colobines consisting of Nasalis, Pygathrix, and Rhinopithecus, with tentative support for Nasalis occupying a basal position within this clade. The African and Asian colobine lineages are inferred to have diverged by 10.8 million years ago (mya or Ma). Within the Asian colobines the odd-nosed clade began to diversify by 6.7 Ma. These results augment our understanding of colobine evolution, particularly the nature and timing of the colobine expansion into Asia. This phylogenetic information will aid those developing conservation strategies for these highly endangered, diverse, and unique primates.     

Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub‐nosed monkey (SNJ R. roxellana)

Shennongjia Rhinopithecus roxellana (SNJ R. roxellana) is the smallest geographical population of R. roxellana. The phylogenetic relationships among its genera and species and the biogeographic processes leading to their current distribution are largely unclear. To address these issues, we resequenced and obtained a new, complete mitochondrial genome of SNJ R. roxellana by next‐generation sequencing and standard Sanger sequencing. We analyzed the gene composition, constructed a phylogenetic tree, inferred the divergence ages based on complete mitochondrial genome sequences, and analyzed the genetic divergence of 13 functional mtDNA genes. The phylogenetic tree and divergence ages showed that R. avunculus (the Tonkin snub‐nosed monkey) was the first to diverge from the Rhinopithecus genus ca. 2.47 million years ago (Ma). Rhinopithecus bieti and Rhinopithecus strykeri formed sister groups, and the second divergence from the Rhinopithecus genus occurred ca. 1.90 Ma. R. roxellana and R. brelichi diverged from the Rhinopithecus genus third, ca. 1.57 Ma. SNJ R. roxellana was the last to diverge within R. roxellana species in 0.08 Ma, and the most recent common ancestor of R. roxellana is 0.10 Ma. The analyses on gene composition showed SNJ R. roxellana was the newest geographic population of R. roxellana. The work will help to develop a more accurate protection policy for SNJ R. roxellana and facilitate further research on selection and adaptation of R. roxellana.     

Digestive strategy of the asian colobine genusTrachypithecus

The Asian colobines,Trachypithecus obscurus andT. cirstantus, eat plant-based diets containing 55–80% leaves. The structural polysaccharides in leaves and other plant parts require microbial fermentation before they can be used as an energy source by the monkeys. The major compartments of the gastro-intestinal tract ofTrachypithecus are a voluminous haustrated stomach, a long small itnestine and capacious haustrated hindgut, all of which contribute to the digestive strategy of these two species. Results of digesta marker passage studies indicate there is prolonged retention of digesta for fermentation in both the stomach and haustrated colon. The digestive strategy of these colobines is defined as gastro-colic fermentation, unlike that of other forestomach fermenters in which the hindgut fermentation is of secondary importance.     

A phylogenetic analysis of the palm subtribe Oncospermatinae (Arecaceae) based on morphological characters

Subtribe Oncospermatinae (Arecaceae: Arecoideae: Areceae) is a diverse group of spiny Old World palms. The subtribe includesOncosperma, a widespread Asian genus of five species, along with seven monotypic genera, all endemic to the Seychelles and Mascarene Islands of the western Indian Ocean. A phylogenetic analysis was conducted in order to test the monophyly of subtribe Oncospermatinae with respect to other Old World genera of tribe Areceae. A matrix of 38 morphological characters was scored for 29 taxa, including 11 species of the Oncospermatinae. A single most parsimonious tree was found, resolving the subtribe as a polyphyletic group of two distinct clades. One clade containingAcanthophoenix, Deckenia, Oncosperma, andTectiphiala was placed as sister to a large group that includes members of subtribes Archontophoenicinae, Arecinae, Iguanurinae, and Ptychospermatinae. The other clade of Oncospermatinae, including the Seychelles endemic generaNephrosperma, Phoenicophorium, Roscheria, andVerschaffeltia, was resolved as sister to the Madagascar endemic subtribe Masoalinae, and may have arisen in the western Indian Ocean region.     

The Hand of Cercopithecoides williamsi (Mammalia,Primates): Earliest Evidence for Thumb Reduction among Colobine Monkeys

Thumb reduction is among the most important features distinguishing the African and Asian colobines from each other and from other Old World monkeys. In this study we demonstrate that the partial skeleton KNM-ER 4420 from Koobi Fora, Kenya, dated to 1.9 Ma and assigned to the Plio-Pleistocene colobine species Cercopithecoides williamsi, shows marked reduction of its first metacarpal relative to the medial metacarpals. Thus, KNM-ER 4420 is the first documented occurrence of cercopithecid pollical reduction in the fossil record. In the size of its first metacarpal relative to the medial metacarpals, C. williamsi is similar to extant African colobines, but different from cercopithecines, extant Asian colobines and the Late Miocene colobines Microcolobus and Mesopithecus. This feature clearly links the genus Cercopithecoides with the extant African colobine clade and makes it the first definitive African colobine in the fossil record. The postcranial adaptations to terrestriality in Cercopithecoides are most likely secondary, while ancestral colobinans (and colobines) were arboreal. Finally, the absence of any evidence for pollical reduction in Mesopithecus implies either independent thumb reduction in African and Asian colobines or multiple colobine dispersal events out of Africa. Based on the available evidence, we consider the first scenario more likely.     

Survey of Nonhuman Primates for Antibodies Reactive With Epstein-Barr Virus (EBV) Antigens and Susceptibility of Their Lymphocytes for Immortalization With EBV

The susceptibility to transformation with Epstein-Barr virus (EBV) and the prevalence of antibodies reactive to EBV were examined in 43 primate species. In vitro EBV infection was revealed in lymphocytes from Old World monkeys, including patas monkeys and the colobines, as well as in lymphocytes from the apes. Antibodies reactive to EBV-early antigen/viral capsid antigen (EA/VCA) were detected in all the species of Old World monkeys and apes examined and in two out of seven species of New World monkeys.     

Tropical Asian species show that the Old World clade of ‘spiny solanums’ (Solanum subgenus Leptostemonum pro parte: Solanaceae) is not monophyletic

The tropical Asian taxa of the species‐rich genus Solanum (Solanaceae) have been less well studied than their highly diverse New World relatives. Most of these tropical Asian species, including the cultivated brinjal eggplant/aubergine and its wild progenitor, are part of the largest monophyletic Solanum lineage, the ‘spiny solanums’ (subgenus Leptostemonum or the Leptostemonum clade). Here we present the first phylogenetic analysis of spiny solanums that includes broad sampling of the tropical Asian species, with 42 of the 56 currently recognized species represented. Two nuclear and three plastid regions [internal transcribed spacer (ITS), waxy, ndhF‐rpL32, trnS‐trnG and trnT‐trnF] were amplified and used to reconstruct phylogenetic relationships using maximum likelihood and Bayesian methods. Our analyses show that Old World spiny solanums do not resolve in a single clade, but are part of three unrelated lineages, suggesting at least three independent introductions from the New World. We identify and describe several monophyletic groups in Old World solanums that have not been previously recognized. Some of these lineages are coherent in terms of morphology and geography, whereas others show considerable morphological variation and enigmatic distribution patterns. Tropical Asia occupies a key position in the biogeography of Old World spiny solanums, with tropical Asian taxa resolved as the closest relatives of diverse groups of species from Australia and Africa.     

金丝猴(RHINOPITHECUS)肌肉系统某些特征的比较研究

本文对金丝猴与其他灵长类之间和三种金丝猴之间特征不同的56条肌作了比较研究。结果表明:三种金丝猴的肌肉系统存在一些差异。纠正了Patterson(1942)对一例川金丝猴的一些错误观察记录。在金丝猴属的肌学方面除与猴超科共有的大部分特征外,还具有与类人猿和人相似的特征。在猴类中,金丝猴的肌肉系统更多地与叶猴相似,其中一些特征较叶猴更为进化。从进化观点看,金丝猴的肌学特征似介于叶猴与类人猿之间,故它们比其他猴超科动物更为进化。     

金丝猴(Rhinopithecus)的某些结构特征

本文在对金丝猴的三个种群作系统解剖的基础上,与其他灵长类以及金丝猴的三个种群之间进行了比较。结果表明:在金丝猴与其他灵长类进行比较的44个项目中,金丝猴特有者9项;与叶猴相同而与其他灵长类不同者4项;与疣猴类的共同特征9项;与叶猴、类人猿和人相似而为其他猴类所不具备的特征有5项;与类人猿和人相似而为叶猴和其他猴类所不具备的特征有17项。因此,我们认为金丝猴的地位在叶猴之上,是猴超科(Cercopithecoidea) 中最进化的一个属,在灵长类系统发育中处于猴类与猿类之间的中间地位。在金丝猴三个种群之间互异比较中,相互不同的特征均超过60％,似乎完全有理由把它分立为三个种。