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

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Abstract

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.

Section snippets

Introduction and background

The extant Old World monkeys have been divided into two major groups—the cercopithecines and the colobines—which diverged from one another in the mid-Miocene (Delson, 1994, Sterner et al., 2006). The colobines are primarily distinguished from their cercopithecine relatives by several derived morphological traits, including a multi-chambered ruminant-like stomach, that are adaptations to a more folivorous diet (Strasser and Delson, 1987). While the cercopithecines (macaques, guenons, and

Samples

This study includes a representative from all but one of the commonly recognized colobine genera (sensu Brandon-Jones et al., 2004, Grubb et al., 2003) (Table 1). Only Simias, which is expected to cluster as the sister taxon of Nasalis based on morphological and mitochondrial data (Groves, 1970, Delson, 1975, Whittaker et al., 2006), is not included. All but two of the colobine individuals used (Procolobus, Rhinopithecus) were held constant in the X-chromosomal and mitochondrial datasets.

Mitochondrial data

Maximum likelihood and Bayesian analyses produced the same mitochondrial topology and both Bayesian runs showed identical results (Fig. 2A). These are congruent with those from Sterner et al. (2006) and show reciprocally monophyletic Asian and African colobine clades, a monophyletic odd-nosed clade, and a sister–taxon relationship between Presbytis and Trachypithecus. The SH test (Fig. 3) shows that trees possessing a Presbytis + Trachypithecus pair are significantly better at explaining the data

Discussion

The inferred X-chromosomal and mitochondrial trees differ mainly in the relationships between the langurs and leaf monkeys. The mitochondrial tree finds Presbytis and Trachypithecus as sister taxa, while the X-chromosomal tree groups Semnopithecus and Trachypithecus together. The relatively long X-chromosomal branch supporting this latter relationship suggests that the two taxa shared a common ancestry for a long period of time. The X-chromosomal tree also places Presbytis as sister to all

Future research in langur and leaf monkey molecular systematics

Semnopithecus sensu stricto (i.e., excluding Trachypithecus) has traditionally been comprised of one species, the Hanuman langur (S. entellus). Brandon-Jones et al. (2004) reclassified two other langur species (Nilgiri black langur [T. johnii], purple-faced langur [T. vetulus]) into Semnopithecus based primarily on mitochondrial relationships (Zhang and Ryder, 1998) despite their morphological similarity to other Trachypithecus species. If nuclear genes do not follow this pattern, then this

Acknowledgments

We thank Eric Delson, Kirstin Sterner, and two anonymous reviewers for helpful comments on drafts of this paper. This research was partially funded by a National Science Foundation East Asian and Pacific Studies Institute fellowship (0513148), a National Science Foundation Doctoral Dissertation Improvement Grant (0524990), and the National Natural Science Foundation of China.

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