Molecular phylogeny and biogeography of langurs and leaf monkeys of South Asia (Primates: Colobinae)

The two recently proposed taxonomies of the langurs and leaf monkeys (Subfamily Colobinae) provide different implications to our understanding of the evolution of Nilgiri and purple-faced langurs. Groves (2001) [Groves, C.P., 2001. Primate Taxonomy. Smithsonian Institute Press, Washington], placed Nilgiri and purple-faced langurs in the genus Trachypithecus, thereby suggesting disjunct distribution of the genus Trachypithecus. [Brandon-Jones, D., Eudey, A.A., Geissmann, T., Groves, C.P., Melnick, D.J., Morales, J.C., Shekelle, M., Stewart, C.-B., 2003. Asian primate classification. Int. J. Primatol. 25, 97-162] placed these langurs in the genus Semnopithecus, which suggests convergence of morphological characters in Nilgiri and purple-faced langurs with Trachypithecus. To test these scenarios, we sequenced and analyzed the mitochondrial cytochrome b gene and two nuclear DNA-encoded genes, lysozyme and protamine P1, from a variety of colobine species. All three markers support the clustering of Nilgiri and purple-faced langurs with Hanuman langur (Semnopithecus), while leaf monkeys of Southeast Asian (Trachypithecus) form a distinct clade. The phylogenetic position of capped and golden leaf monkeys is still unresolved. It is likely that this species group might have evolved due to past hybridization between Semnopithecus and Trachypithecus clades.     

Mitochondrial and nuclear markers suggest Hanuman langur (Primates: Colobinae) polyphyly: Implications for their species status

Recent molecular studies on langurs of the Indian subcontinent suggest that the widely-distributed and morphologically variable Hanuman langurs (Semnopithecus entellus) are polyphyletic with respect to Nilgiri and purple-faced langurs. To further investigate this scenario, we have analyzed additional sequences of mitochondrial cytochrome b as well as nuclear protamine P1 genes from these species. The results confirm Hanuman langur polyphyly in the mitochondrial tree and the nuclear markers suggest that the Hanuman langurs share protamine P1 alleles with Nilgiri and purple-faced langurs. We recommend provisional splitting of the so-called Hanuman langurs into three species such that the taxonomy is consistent with their evolutionary relationships.     

The Emergence of an Endangered Species: Evolution and Phylogeny of the <Emphasis Type="Italic">Trachypithecus geei</Emphasis> of Bhutan

Golden langurs (Trachypithecus geei) are an endangered primate species in Bhutan. We discuss their evolution in terms of phylogeny, ecology, and biogeography. We test the hypothesis that rivers and mountains in Bhutan isolated a population of capped langurs (Trachypithecus pileatus) that later speciated into the morphologically distinct T. geei. Trachypithecus, the genus to which both capped and golden langurs belong, spread north from a paleorefuge in south China, and Semnopithecus (gray langurs) spread east and northward from a refuge in south India. We show that the 2 genera both arrived in Bhutan and were separated from each other by the Sunkosh River and Black Mountains. Likewise, a population of capped langurs isolated from parental populations by rivers speciated into the distinct golden langurs. We conducted field surveys covering the entire range of langurs in Bhutan. The Sunkosh River and Black Mountain range in west Bhutan isolate gray langurs and golden langurs from each other. In the east, the Manas River system (Manas-Mangde) served as a barrier between golden and capped langurs. However, it is an imperfect barrier and a contact zone between the 2 species occurred on the banks of the Mangde River. Second, we reconstructed the evolutionary history of the langurs of Bhutan via molecular phylogenetic tools. We sequenced the cytochrome b region (cyt b) of the mitochondrial DNA (mtDNA) to model a phylogeny. It revealed the distinct evolutionary paths of the golden, capped, and gray langurs. As predicted, golden and capped langurs are closely related to each other and to other species in Trachypithecus from Southeast Asia. The gray langur of Bhutan grouped into a distinct clade with conspecifics in Semnopithecus from India and Nepal. The south Indian clade of gray langurs is more ancient, with the Bhutan and Nepal gray langurs having diverged later, which fits with the glacial models of ice sheet retreats and colonization of South Asia by gray langurs from south India north toward the Himalayas. Likewise, the golden and capped langur clade are the most derived and divergent from the older groups of Trachypithecus in Southeast Asia, which also fits with paleorefuge models of recolonization by Trachypithecus into the rest of Southeast Asia and north toward the Himalayas from paleorefuges in Southeast Asia. As predicted, golden and capped langurs are closely related to each other and gray langurs are only distantly related to them. The divergence between capped and golden langurs is more recent, while the split between Trachypithecus and Semnopithecus is more ancient and took place before the Pliocene.     

Primate numts and reticulate evolution of capped and golden leaf monkeys (Primates: Colobinae)

A recent phylogenetic study of langurs and leaf monkeys of South Asia suggested a reticulate evolution of capped and golden leaf monkeys through ancient hybridization between Semnopithecus and Trachypithecus. To test this hybridization scenario, I analysed nuclear copies of the mitochondrial cytochrome b gene (numts) from capped, golden and Phayre’s leaf monkeys. These numts were aligned with mitochondrial cytochrome b sequences of various species belonging to the genera Semnopithecus and Trachypithecus. In the phylogenetic tree derived from this alignment, the numts fell into three distinct clades (A, B and C) suggesting three independent integration events. Clade A was basal to Semnopithecus, and clades B and C were basal to Trachypithecus. Among the numts in clades A and C were sequences derived from species not represented in their respective sister mitochondrial groups. This unusual placement of certain numts is taken as additional support for the hybridization scenario. Based on the molecular dating of these integration events, hybridization is estimated to have occurred around 7.1 to 3.4 million years ago. Capped and golden leaf monkeys might have to be assigned to a new genus to reconcile their unique evolutionary history. Additionally, northeast India appears to be a ‘hot spot’ for lineages that might have evolved through reticulate evolution.     

Distribution and Abundance of Primates in Rain Forests of the Western Ghats,Karnataka, India and the Conservation of Macaca silenus

We assessed the distribution and abundance of 4 species of diurnal primates viz. lion-tailed macaque, bonnet macaque, Nilgiri langur and Hanuman langur, in 2 areas—Brahmagiri-Makut and Sirsi-Honnavara—in rain forests of the Western Ghats in the state of Karnataka, India. The Nilgiri langurs in Brahmagiri-Makut and the lion-tailed macaques in Sirsi-Honnavara are the northernmost populations of the 2 species in the Western Ghats. The 2 regions represent changes in ecological zones in the Western Ghats. In Brahmagiri-Makut, Hanuman langurs and bonnet macaques occupy lower elevations whereas Nilgiri langurs live in relatively higher altitudes. Only one group of lion-tailed macaques was in Brahmagiri-Makut. In the forests of Sirsi-Honnavara, 3 species of primates viz. lion-tailed macaque, bonnet macaque and Hanuman langur were in larger numbers throughout the forest. A self-sustainable single population of 32 groups of lion-tailed macaques occurred in Sirsi-Honnavara. Few subspecies of Hanuman langurs exist in the study regions. Due to local hunting practices, the relative abundance of primates in Brahmagiri-Makut is lower than that in Sirsi-Honnavara.     

Taxonomic Implications of a Field Study of Morphotypes of Hanuman Langurs (<Emphasis Type="Italic">Semnopithecus entellus</Emphasis>) in Peninsular India

The Hanuman langur is one of the most widely distributed and morphologically variable non-human primates in South Asia. Even though it has been extensively studied, the taxonomic status of this species remains unresolved due to incongruence between various classification schemes. This incongruence, we believe, is largely due to the use of plastic morphological characters such as coat color in classification. Additionally these classification schemes were largely based on reanalysis of the same set of museum specimens. To bring greater resolution in Hanuman langur taxonomy we undertook a field survey to study variation in external morphological characters among Hanuman langurs. The primary objective of this study is to ascertain the number of morphologically recognizable units (morphotypes) of Hanuman langur in peninsular India and to compare our field observations with published classification schemes. We typed five color-independent characters for multiple adults from various populations in South India. We used the presence-absence matrix of these characters to derive the pair-wise distance between individuals and used this to construct a neighbor-joining (NJ) tree. The resulting NJ tree retrieved six distinct clusters, which we assigned to different morphotypes. These morphotypes can be identified in the field by using a combination of five diagnostic characters. We determined the approximate distributions of these morphotypes by plotting the sampling locations of each morphotype on a map using GIS software. Our field observations are largely concordant with some of the earliest classification schemes, but are incongruent with recent classification schemes. Based on these results we recommend Hill (Ceylon Journal of Science, Colombo 21:277-305, 1939) and Pocock (Primates and carnivora (in part) (pp. 97–163). London: Taylor and Francis, 1939) classification schemes for future studies on Hanuman langurs.     

Of how much concern are the ‘least concern’ species? Distribution and conservation status of bonnet macaques,rhesus macaques and Hanuman langurs in Karnataka,India

We assessed the distribution and conservation status of bonnet macaques (Macaca radiata), rhesus macaques (Macaca mulatta) and Hanuman langurs (Semnopithecus entellus) in the state of Karnataka, India. Karnataka is situated in southwest India with an area of 191,791 km². A total of 9697 km of vehicular survey was made from November 2001 to July 2004. We also visited 107 temples/tourist spots to determine the presence of primates. Bonnet macaques and Hanuman langurs were widely distributed, whereas rhesus macaques were not found in the state. However, bonnet macaques were absent in a few districts in the northern plains and Hanuman langurs were absent in some districts of the southern plains. A total of 205 groups of bonnet macaques and 139 groups of Hanuman langurs were sighted. The relative encounter rate of both species differed across biogeographic zones. Bonnet macaques were largely encountered in the Western Ghats and the Southern Plateau whereas Hanuman langurs were abundant in the Western Ghats and Northern Plains. We found that bonnet macaques have been eliminated from about 48% temples/tourist spots where they occurred in the recent past. The Hanuman langur population of Dharwar–Haliyal Road was assessed during April 2003, and we found that the present population size was about 38% of a previous survey in 1961. Habitat change, hunting/trapping and translocation were the major factors causing a decline in the langur population.     

Functional decline of sweet taste sensitivity of colobine monkeys

For many primates, sweet taste is palatable and is an indicator that the food contains carbohydrates, such as sugars and starches, as energy sources. However, we have found that Asian colobine monkeys (lutungs and langurs) have low sensitivity to various natural sugars. Sweet tastes are recognized when compounds bind to the sweet taste receptor TAS1R2/TAS1R3 in the oral cavity; accordingly, we conducted a functional assay using a heterologous expression system to evaluate the responses of Javan lutung (Trachypithecus auratus) TAS1R2/TAS1R3 to various natural sugars. We found that Javan lutung TAS1R2/TAS1R3 did not respond to natural sugars such as sucrose and maltose. We also conducted a behavioral experiment using the silvery lutung (Trachypithecus cristatus) and Hanuman langur (Semnopithecus entellus) by measuring the consumption of sugar-flavored jellies. Consistent with the functional assay results for TAS1R2/TAS1R3, these Asian colobine monkeys showed no preference for sucrose or maltose jellies. These results demonstrate that sweet taste sensitivity to natural sugars is low in Asian colobine monkeys, and this may be related to the specific feeding habits of colobine monkeys.     

Reproductive Strategies of <Emphasis Type="Italic">Trachypithecus pileatus</Emphasis> in Arunachal Pradesh,India

We studied reproductive behavior of free-ranging capped langurs (Trachypithecus pileatus) in the Pakhui Wildlife Sanctuary, Arunachal Pradesh, India. Four species of primates —Trachypithecus pileatus, Macaca mulatta, M. assamensis, and Nycticebus bengalensis— live there. We studied the mating seasons, mating frequency, copulatory attempts, time spent in copulation, and interval between 2 successive copulations, gestation length, and interbirth interval of 4 groups of capped langurs during 2001–2003. We observed 2 mating seasons in a year. The first was larger, comprising 5 months (September–January), and the second was short, April and May. Mating was intensive in the morning session (0600–1000 h); 57% of total mating events occurred then. The average gestation period was 200 d. November was the most favorable month for breeding. In a year, 107 mating events occurred involving 5 adult females. Average time per mounting attempt is 12 s. Duration of mounting was the maximum in November. Interbirth interval was 23 months and 10 d. The birth season was 129 days, December–April; 53% of births occurred in February and March. Average birth rate is 0.386 birth/female/yr.     

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.     

Comparative study of vocal communication in two Asian leaf monkeys, Presbytis johnii and Presbytis entellus

This paper presents comparative data on the vocal communication of two Asian leaf monkeys, the Nilgiri langur (Presbytis johnii) and South Indian common langur (Presbytis entellus), based on sound recordings and behavioural observations of free-ranging groups. Spectrographical analyses revealed a repertoire of 18 basic patterns for Nilgiri langurs, and 21 basic patterns for common langurs. The repertoires of the two langur species consist of both discretely structured vocal patterns, in which alterations of the physical parameters are restricted to intra-class variation, and those in which structural variations cause integration between different sections of the repertoire. Qualitative assessments of group scans indicate that in both species vocal behaviour is characterized by pronounced sex-differences in the use of the different elements of the vocal repertoire. Comparison of data available from different populations of P. entellus suggests population-specific modifications on both structural and behavioural levels. Moreover, characteristic elements of the vocal systems of the two Asian species demonstrate striking similarities to those described for the African black-and-white colobus.     

Variation in gaze-following between two Asian colobine monkeys

Gaze-following is a basic cognitive ability found in numerous primate and nonprimate species. However, little is known about this ability and its variation in colobine monkeys. We compared gaze-following of two Asian colobines—François’ langurs (Trachypithecus francoisi) and golden snub-nosed monkeys (Rhinopithecus roxellana). Although both species live in small polygynous family units, units of the latter form multilevel societies with up to hundreds of individuals. François’ langurs (N = 15) were less sensitive to the gaze of a human experimenter than were golden snub-nosed monkeys (N = 12). We then tested the two species using two classic inhibitory control tasks—the cylinder test and the A-not-B test. We found no difference between species in inhibitory control, which called into question the nonsocial explanation for François’ langur’s weaker sensitivity to human gaze. These findings are consistent with the social intelligence hypothesis, which predicted that golden snub-nosed monkeys would outperform François’ langurs in gaze-following because of the greater size and complexity of their social groups. Furthermore, our results underscore the need for more comparative studies of cognition in colobines, which should provide valuable opportunities to test hypotheses of cognitive evolution.     

Diet and Food Choice of Trachypithecus francoisi in the Nonggang Nature Reserve, China

We studied the diet and food choice of 1 group of Fran?ois’ langurs (Trachypithecus francoisi) from August 2003 to July 2004 in the Nonggang Nature Reserve, Guangxi province, China. The langurs consumed 90 plant species, including 14 unidentified species. Leaves constituted 52.8% of the diet (38.9% young leaves and 13.9% mature leaves). Fruits and seeds accounted for 17.2% and 14.2%, respectively. Flowers and other items—including petioles, stems, roots, and bark—contributed to 7.5% and 7.4% of the diet, respectively. The langur diet varied according to season. They fed on more young leaves from April to September. Consumption of seeds, petioles, and stems increased between October and March, when young leaves were scarce. The diet shift corresponded to higher dietary diversity during the young leaf-lean period. Though the langurs fed on many plant species, 10 species accounted for 62.2% of the diet, only 2 of which were among the 10 most common tree species in vegetation quadrants, and the percentage of feeding records on a plant species and the percentage of individuals of the species in vegetation quadrants does not correlate significantly. Fran?ois’ langurs fed selectively, and they did not base their diet simply on the abundance of plant species in the habitat.     

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.     

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。     

中国石山叶猴生态学研究进展

喀斯特石山是一类特殊环境,生存在喀斯特石山的动物形成特殊的行为机制以适应这一特殊的环境.石山叶猴是仅分布于喀斯特石山地区的珍稀濒危灵长类动物,属疣猴亚科乌叶猴属的一个种组,包括黑叶猴(Trachypithecus francoisi)、白头叶猴(T.leucocephalus)、德氏叶猴(T.delacouri)、金头...     

Comparison of locomotor behaviour between white-headed langurs Trachypithecus leucocephalus and Francois' langurs T.fran(c)oisi in Fusui, China

We studied the locomotor behaviour of white-headed langurs Trachypithecus leucocephalus and Fran(c)ois' langurs T.fran(c)oisi to test two hypotheses: (1) these monkeys have evolved locomotor ability to support their activities on limestone hills,and (2) Fran(c)ois' langurs have evolved more diverse locomotor skills than white-headed langurs. Data were collected from 1996 - 1998 and in 2005 in Fusui Nature Reserve,Guangxi,and showed that the two species had similar locomotor types,but Francois' langurs had more locomotor modes (26) than white-headed langurs (12). Quadrupedal walking and leaping were two major types,and white-headed langurs were more arboreal than Fran(c)ois' langurs. We suggest that,while keeping their ancestral locomotor types,the two species have evolved new types allowing them to live on limestone cliffs. Compared to white-headed langurs,Francois' langurs have more diverse locomotor modes that probably have allowed them to live in more habitat types. As an evolutionary outcome,Fran(c)ois' langurs have a larger distribution range.     

Mitochondrial cytochrome b gene sequences of old world monkeys: With special reference on evolution of Asian colobines

The classification and phylogenetic relationships of the Old World monkeys are still controversial. For Asian colobines, from three to nine genera were recognized by different primatologists. In the present study, we have sequenced a 424 bp mitochondrial tRNA^Thr gene and cytochrome b gene fragment fromMacaca mulatta, Mandrillus sphinx, Mandrillus leucophaeus, Semnopithecus entellus, Trachypithecus vetulus, T. johnii, T. phayrei, T. francoisi, Pygathrix nemaeus, Rhinopithecus roxellanae, R. bieti, R. avunculus, Nasalis larvatus, andColobus polykomos in order to gain independent information on the classification and phylogenetic relationships of those species. Phylogenetic trees were constructed with parsimony analysis by weighting transversions 5 or 10 fold greater than transitions. Our results support the following conclusions: (1) the Old World monkeys are divided into two subfamilies; (2) that among the colobines,Colobus, the African group, diverged first, andNasalis andRhinopithecus form a sister clade toPygathrix; (3) that there are two clades within leaf monkeys, i.e. 1)S. entellus, T. johnii, andT. vetulus, and 2)T. phayrei andT. francoisi; (4) thatRhinopithecus avunculus, R. roxellanae, andR. bieti are closely related to each other, and they should be placed into the same subgenus; (5) thatRhinopithecus is a distinct genus; and (6) that the ancestors of Asian colobines migrated from Africa to Asia during the late Pliocene or early Pleistocene.     

Phylogenetic incongruence between nuclear and mitochondrial markers in the Asian colobines and the evolution of the langurs and leaf monkeys

Evidence of incongruence between mitochondrial and nuclear gene trees is now becoming documented with increasing frequency. Among the Old World monkeys, this discordance has been well demonstrated in the Cercopithecinae, but has not yet been investigated in the Colobinae. The mitochondrial relationships between the colobine genera have recently been clarified and cluster Presbytis and Trachypithecus as sister taxa to the exclusion of Semnopithecus. This is incongruent with previous morphological hypotheses that suggest the latter two are sister taxa, and perhaps even congeneric. In addition to analyzing a previously published 10,896 bp mitochondrial dataset, we sequenced and analyzed a 4297 bp fragment of the X-chromosome in order to test the competing mitochondrial and morphological phylogenetic hypotheses. The results from the mitochondrial dataset again support a Presbytis+Trachypithecus group while the X-chromosomal dataset supported a Semnopithecus+Trachypithecus group. A Shimodaira-Hasegawa test performed on both datasets indicates that the mitochondrial and X-chromosomal trees are significantly better at explaining their respective datasets than alternative topologies (p<0.05). We suggest that differential lineage sorting or ancient hybridization may be the cause of this strong discordance between the mitochondrial and X-chromosomal markers in these taxa.     

Trachypithecus auratus sangiranensis,A New Fossil Monkey from Sangiran,Central Java,Indonesia

We describe a new extinct subspecies of the Javan lutung—Trachypithecus auratus sangiranensis—based on an isolated, tooth-bearing upper jaw. The specimen was in volcanic breccia situated between the Lower Pucangan and the Upper Kalibeng Formations 500 m south of the village of Sangiran, near Surakarta, central Java, Indonesia. The new fossil monkey bears morphological similarities to the two living species of leaf monkey from Java, Presbytis comata comata and Trachypithecus auratus auratus, and to the Middle Pleistocene form, Trachypithecus cristatus [=auratus] robustus, from Tegoean, central Java. It is significantly larger than any of these forms, and differs from them in details of dental anatomy. Because the greatest number of similarities are between the new fossil and Trachypithecus auratus subspecies, we designated the specimen as T. a. sangiranensis. The geochronological age of the breccia from which the fossil came, is 1.9± 0.05 Ma (million years), making T. a. sangiranensis one of the oldest fossil monkeys from eastern Asia.