Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups
© Osterholz et al; licensee BioMed Central Ltd. 2008
Received: 18 September 2007
Accepted: 25 February 2008
Published: 25 February 2008
The evolutionary history of the Asian colobines is less understood. Although monophyly of the odd-nosed monkeys was recently confirmed, the relationships among the langur genera Presbytis, Semnopithecus and Trachypithecus and their position among Asian colobines remained unclear. Moreover, in Trachypithecus various species groups are recognized, but their affiliations are still disputed. To address these issues, mitochondrial and Y chromosomal sequence data were phylogenetically related and combined with presence/absence analyses of retroposon integrations.
The analysed 5 kb fragment of the mitochondrial genome allows no resolution of the phylogenetic relationships among langur genera, but five retroposon integrations were detected which link Trachypithecus and Semnopithecus. According to Y chromosomal data and a 573 bp fragment of the mitochondrial cytochrome b gene, a common origin of the species groups T. [cristatus], T. [obscurus] and T. [francoisi] and their reciprocal monophyly is supported, which is also underpinned by an orthologous retroposon insertion. T. [vetulus] clusters within Semnopithecus, which is confirmed by two retroposon integrations. Moreover, this species group is paraphyletic, with T. vetulus forming a clade with the Sri Lankan, and T. johnii with the South Indian form of S. entellus. Incongruence between gene trees was detected for T. [pileatus], in that Y chromosomal data link it with T. [cristatus], T. [obscurus] and T. [francoisi], whereas mitochondrial data affiliates it with the Semnopithecus clade.
Neither relationships among the three langur genera nor their position within Asian colobines can be settled with 5 kb mitochondrial sequence data, but retroposon integrations confirm at least a common origin of Semnopithecus and Trachypithecus. According to Y chromosomal and 573 bp mitochondrial sequence data, T. [cristatus], T. [obscurus] and T. [francoisi] represent true members of the genus Trachypithecus, whereas T. [vetulus] clusters within Semnopithecus. Due to paraphyly of T. [vetulus] and polyphyly of Semnopithecus, a split of the genus into three species groups (S. entellus - North India, S. entellus - South India + T. johnii, S. entellus - Sri Lanka + T. vetulus) seems to be appropriate. T. [pileatus] posses an intermediate position between both genera, indicating that the species group might be the result of ancestral hybridization.
The Old World monkeys are traditionally divided into the two subfamilies Cercopithecinae and Colobinae, which differ from each other by numerous morphological, behavioural and ecological characteristics [1–4]. While detailed information on the evolutionary history of cercopithecines (baboons, mangabeys, macaques and guenons) is at hand, knowledge on colobines is still scarce. Although some molecular studies [5–13] exist, they mainly focus on relationships within genera or species groups and not on the general phylogeny of the subfamily. Recently, a first mitochondrial phylogeny of colobine genera was established , which confirmed some previous assumptions, but also led to confusions, calling for further research to definitively elucidate their evolutionary history.
Based on distribution and morphology, the colobines are traditionally divided into an African and an Asian clade [3, 4], while Asian colobines are more diverse than their African relatives. Hence, the Asian forms are further split into the odd-nosed monkey (Pygathrix, Rhinopithecus, Nasalis, Simias) and langur (Presbytis, Trachypithecus, Semnopithecus) groups, which are both believed to be monophyletic. Accordingly, langurs were originally combined in the single genus Presbytis [15–17] or Semnopithecus , but based on neonatal colouration and cranial morphology, they were split into the three genera Semnopithecus, Trachypithecus and Presbytis , and a fourth genus (Kasi) was added . Alternatively, Semnopithecus was separated from Presbytis, with Trachypithecus forming a subgenus of the former [21–23], but recent classifications use a subdivision of langurs into the three genera Presbytis, Trachypithecus and Semnopithecus [3, 4, 24–26].
The phylogenetic relationships among the different Asian colobine genera are disputed. Although a common origin of the odd-nosed monkeys was recently confirmed , evidence for monophyly of its putative sister clade, the langur group, is still lacking. Moreover, available data depict Trachypithecus and Presbytis as sister taxa to the exclusion of Semnopithecus , which contradicts with traditional classifications, in which Trachypithecus and Semnopithecus are believed to form a clade to the exclusion of Presbytis [4, 21–23]. These findings raise the question of what positions the langur genera occupy among Asian colobines and whether the langurs form a monophyletic clade in general. Moreover, the affiliations of different Trachypithecus species groups, especially T. [vetulus] and T. [pileatus], are disputed, and hence, led to different classifications. Currently, only few genetic data are available [7, 9, 28], so that further information from other markers is required to definitively establish their relationships.
To address all these issues, mitochondrial and Y chromosomal sequence data were phylogenetically related and combined with presence/absence analysis of retroposon integrations. This approach was used to simultaneously analyse paternal-, maternal- and biparental-inherited markers, which allow the detection of incongruence between different gene trees indicating possible hybridization or introgression events between different lineages [29–31]. To determine the phylogenetic position of the langur genera among Asian colobines, a 5 kb fragment of the mitochondrial genome was sequenced from eight colobine genera, and combined with presence/absence analysis of retroposon integrations. Retroposon insertion events are nearly homoplasy-free and precise excision of elements is highly unlikely [32, 33]. Accordingly, retroposon insertions are powerful informative markers, which were already successfully applied to elucidate phylogenetic relationships in various primate lineages [34–38]. To study relationships among different langur species groups and their genus affiliations, a 573 bp fragment of the mitochondrial cytochrome b gene and a 777 bp portion of the SRY (sex-determining region, Y chromosome) gene was sequenced from at least one representative per species group, and complemented with retroposon analysis.
Results and Discussion
Genus level phylogeny
To elucidate the phylogenetic relationships among the different langur genera and their position among Asian colobines, mitochondrial sequence studies were combined with presence/absence analysis of retroposon insertions.
The herein analysed 5 kb fragment of the mitochondrial genome was assembled from sequences derived from 1–2 kb long and partly overlapping PCR products, whereby no inconsistencies in overlapping sequence fragments were detected. As template material, mainly DNA extracted from feces was used, which minimizes the amplification of nuclear pseudogenes , and comparisons of the data with sequences already deposited at GenBank revealed only intra-species or -generic variation, indicating that no nuclear pseudogenes were amplified.
Although in general the mitochondrial data are suitable to elucidate relationships among the different genera, as indicated by the correct and significantly supported branching patterns among all other studied genera, the relationships among the langurs are unresolved, which is concordant with previous results . In contrast, the presence/absence analysis of retroposon integrations provides evidence for a monophyletic odd-nosed monkey clade and a common origin of Trachypithecus and Semnopithecus, which is in agreement with morphological hypotheses [1, 3, 4, 21–23]. Regardless which markers were used, the phylogenetic position of Presbytis among Asian colobines and accordingly the unity of the langurs remains unclear and needs further investigations.
Species group phylogeny
In order to settle affiliations among the different Trachypithecus species groups and their members, mitochondrial and Y chromosomal sequence data were combined with information on retroposon integrations.
With some exceptions, the Y chromosomal data provide a similar picture (Fig. 5b), but due to the low number of polymorphic sites, support values are in general not as high as in the mitochondrial tree. According to the reconstructions, the species groups are divided into two major clades, with one comprising T. [obscurus], T. [cristatus], T. [francoisi] and T. [pileatus], and the other, T. [vetulus] and Semnopithecus. Relationships among the latter are not resolved. All alternative tree topologies, in which either T. [vetulus] belongs to Trachypithecus or T. pileatus groups with Semnopithecus, were rejected (P < 0.05).
Retroposon insertions further deepened our knowledge on the species group relationships. Altogether, three informative integrations were analysed (Fig. 5c), with one occurring in T. [obscurus], T. [cristatus] and T. [francoisi], and the other two in T. [vetulus] and Semnopithecus. Interestingly, all three integrations are absent in T. pileatus.
With the exception of the varying position of T. [pileatus], the affiliations of the remaining species groups are congruent among different gene trees. Accordingly, all analysed markers relate T. [vetulus] with Semnopithecus, indicating that this species group is a real member of the genus Semnopithecus and not of Trachypithecus as assumed by morphological similarities . These similarities may be the results of adaptations to similar ecological conditions (Semnopithecus is semi-terrestrial and lives in deciduous forest, whereas Trachypithecus including T. [vetulus] is arboreal and occurs in wet evergreen forests). Although the Y chromosomal data allow no resolution within the Semnopithecus – T. [vetulus] clade, the mitochondrial data indicate paraphyly of the two T. [vetulus] species, with T. vetulus clustering with S. entellus from Sri Lanka and T. johnii with S. entellus from South India, which is concordant with their geographical distribution. These findings indicate paraphyly of S. entellus, whereby North Indian representatives form a further distinct lineage. Accordingly, the langurs of the Indian subcontinent should be split into three species groups, with one occurring solely on Sri Lanka, one in Southern India and a third one in Northern India, whereas the Gondavari river seems to be barrier between the latter two.
Monophyly of each of T. [obscurus], T. [cristatus] and T. [francoisi] and their close affiliation is depicted in all gene trees, so that all of them can be regarded as true members of Trachypithecus. These findings confirm previous molecular studies [8–11, 13] and are in general agreement with recent classifications [4, 26].
The only discrepancies between different gene trees were obtained for T. [pileatus]. Whereas the mitochondrial data link the species group with Semnopithecus and T. [vetulus], the Y chromosomal data affiliates it with T. [obscurus], T. [cristatus] and T. [francoisi]. These findings might be explained by incomplete lineage sorting of ancestral mitochondrial or Y chromosomal haplotypes. Accordingly, the ancestor of Trachypithecus, Semnopithecus and T. [pileatus] carried multiple DNA lineages with one lineage being randomly fixed in two taxa, but not in the third. Alternatively, the varying position of T. [pileatus] in different gene trees might be explained by past hybridization between Semnopithecus and Trachypithecus. As depicted by the three retroposon insertions, this putative hybridization event would have occurred between ancestral forms of Semnopithecus and Trachypithecus, before both genera diverged into distinct species groups. The hybridization hypothesis is also supported by some intermediate morphological characteristics  and the distribution of T. [pileatus], which is sandwiched between those of Semnopithecus and other Trachypithecus species groups (Fig. 1, Fig. 2).
The present study provides detailed insights into the evolutionary history of Asian colobines and underpins the tremendous power of retroposon integrations as cladistic markers. Although mitochondrial data proved to be useful to elucidate and confirm several relationships among studied taxa, the data set failed to resolve the affiliations among the langur genera and to settle their position among Asian colobines. In contrast, retroposon insertions provided clear evidence for a sister grouping of Semnopithecus and Trachypithecus, but no integrations were detected, which link Presbytis either with the other two langur genera or with the odd-nosed monkeys, so that further research is required to solve this issue. Moreover, to definitively explain the evolutionary history of colobines, further molecular markers should be analysed, especially regarding possible discrepancies among gene trees due to hybridization or introgression, as such events are important speciation mechanisms in primates , and as it was possibly detected in the present study in the case of T. [pileatus].
Proposed classification of Semnopithecus and Trachypithecus species based on the herein presented data.
S. entellus* (North India)
S. entellus* (South India)
S. entellus* (Sri Lanka)
Sample collection, DNA extraction and preventing contaminations
Species analysed, their origin, material type and GenBank accession numbers.
mtDNA (5 kb)
mtDNA (573 bp)
SRY (777 bp)
part of 5 kb
Semnopithecus entellus (North India)
part of 5 kb
S. entellus (South India)
S. entellus (Sri Lanka)
part of 5 kb
Mitochondrial sequence analysis
Primers for amplifying and sequencing the 5 kb mitochondrial fragment.
To determine phylogenetic affiliations of species groups, a 573 bp long fragment of the mitochondrial cytochrome b gene was analysed from all species of the different groups (Table 2). The generation of sequences followed laboratory methods as described [9, 11, 13]. The final alignment, which was easily generated by eye due to the absence of insertions or deletions, comprised 19 individuals including the outgroup taxon Presbytis melalophos. Phylogenetic trees were constructed as described above. As best-fitting model, MODELTEST selected the TIM + I (= 0.5977) + Γ (= 2.3137) model, which was applied for NJ and ML reconstructions. As for the 5 kb fragment, several alternative tree topologies, in which T. [vetulus] is recognized as monophyletic, either T. [vetulus] or T. [pileatus] belongs to Trachypithecus, or even both are members of Trachypithecus, were tested.
Y chromosomal sequence analysis
The SRY gene was selected as it represents a single-copy gene and as it is proved to be informative in reconstructing the Y chromosomal evolutionary history of macaques . PCR conditions and primers were applied as described . To amplify the SRY gene from fecal material, two overlapping fragments were generated with published primers  and the newly generated internal primers 5'-TGGGCGGAGTTGAGAGGGGT-3' and 5'-TAGCGGTCCCGTTGCTGCGG-3'. The final alignment of 777 bp comprised 15 taxa representing all species groups of the genera Semnopithecus and Trachypithecus as well as Presbytis melalophos, which was used as outgroup. To reconstruct NJ and ML trees, the K80 model of sequence evolution, determined with MODELTEST, was used. MP trees were generated as described above. The reliability of the depicted position of T. [vetulus] and T. [pileatus] was tested in PAUP by using alternative tree topologies, in which either T. [vetulus] belongs to Trachypithecus or T. pileatus groups with Semnopithecus.
Presence/absence analysis of retroposon insertions.
SENT, TOBS, PMEL, PNEM, NLAR
SENT, TOBS, PMEL, PNEM, NLAR
SENT, TOBS, PMEL, PNEM, NLAR
SENT, TOBS, PMEL, PNEM, NLAR
SENT, TOBS, PMEL, PNEM, NLAR
TOBS, PMEL, PNEM, NLAR
SENT, TOBS, PMEL, PNEM, NLAR
SENT, TVET, TDEL, TOBS, TAUR
PMEL, PNEM, NLAR
PMEL, PNEM, NLAR
PMEL, PNEM, NLAR
PMEL, PNEM, NLAR, CGUE
PMEL, PNEM, NLAR, CGUE
PNEM, NLAR, RAVU
SENT, TOBS, PMEL, CGUE
TDEL, TOBS, TAUR
TPIL, SENT, TVET, PMEL, PNEM
SENT, TVET, TJOH
TPIL, TDEL, TOBS, TAUR, PMEL, NLAR
SENT, TVET, TJOH
TPIL, TDEL, TOBS, TAUR, PMEL, NLAR
To detect new loci, a subtractive hybridization approach  was performed with some modifications. As tracer and driver, different colobine genera were selected. Genomic DNA of tracer and driver was digested with RSAI (Fermentas), and subsequently, the adapters AdapA1/AdapAA1 (5'-TGTAGCGTGAAGACGACAGAAAGGGCGTGGTGCGGAGGGCGGT-3'/5'-ACCGCCCTCCG-3') and AdapA2/AdapAA2 (5'-TGTAGCGTGAAGACCTGTCTTAGGGCGTGGTGGCCAGGGCCGT-3'/5'-ACGGCCCTGGC-3') were ligated to the tracer fragments. Each of ~15 ng tracerA1 and tracerA2 were hybridized with ~1,500 ng driver for 20 h at 60°C. 2 μl of the hybridization result was used as template to amplify solely tracer fragments using the adapter primers A1 (5'-TGTAGCGTGAAGACGACAGAA-3') and A2 (5'-TGTAGCGTGAAGACCTGTCTT-3'). The PCR program consisted of a pre-extension step at 72°C for 6 min to fill in adaptor ends, followed by 25 cycles, each with a denaturation step at 95°C for 1 min, annealing at 60°C for 1 min and extension at 72°C for 2 min. To enrich fragments with Alu insertions, a semi-nested PCR was added using either primer A1 or A2 and the Alu-specific AluY (5'-GGAGAATGGCGTGAACCCGGGA-3') oligonueclotide. The PCR products were separated on agarose gels and fragments over 500 bp were excised from the gel. After purification, the fragments were cloned into the pGEMTeasy vector (Promega) and transformed into electro-competent TOP10 cells (Invitrogen). Bacterial clones were collected in 96-well microtiter plates and re-screened via PCR with the primers A1 or A2 and AluY. Positive clones were sequenced and analysed with REPEATMASKER and BLAST as implemented in NCBI and EMBL. Based on the generated alignments, locus-specific primers were constructed, with the forward primer occupying a region 5'-end upstream of the insertion site, which is conserved among the colobine and human or chimp sequences. Due to the absence of the 3'-end downstream sequence of the tested colobine species, reverse primers were constructed solely on the basis of human or chimp sequences. Subsequently, the presence or absence of respective Alu insertions in different colobine species was tested via PCR. The orthology of insertions was confirmed by sequencing of at least one species per genus or species group. Sequences were deposited at GenBank and are available under the accession numbers EU004484–EU004537 and EU006662–EU006692.
Species names in square brackets () indicate species groups.
We are grateful to the staff of the zoos in Cologne, Dresden, Hannover, Krefeld, Erfurt, Stuttgart, Wuppertal, Howletts, Bristol and Singapore, and to Manfred Ade (Naturhistorisches Museum Berlin, Germany), Linda Vigilant (Max-Planck-Institute of Evolutionary Anthropology, Leipzig, Germany), Kai-Olaf Krüger (Angkor Centre for Conservation of Biodiversity, Cambodia) and Tilo Nadler (Endangered Primate Rescue Center, Vietnam) for samples. Finally, we thank Christiane Schwarz for her excellent technical assistance in the laboratory. The work was financially supported by the German Primate Center (DPZ).
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