A complete species-level phylogeny of the Hylobatidae based on mitochondrial ND3–ND4 gene sequences

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Abstract

The Hylobatidae (gibbons) are among the most endangered primates and their evolutionary history and systematics remain largely unresolved. We have investigated the species-level phylogenetic relationships among hylobatids using 1257 bases representing all species and an expanded data set of up to 2243 bases for select species from the mitochondrial ND3–ND4 region. Sequences were obtained from 34 individuals originating from all 12 recognized extant gibbon species. These data strongly support each of the four previously recognized clades or genera of gibbons, Nomascus, Bunopithecus, Symphalangus, and Hylobates, as monophyletic groups. Among these clades, there is some support for either Bunopithecus or Nomascus as the most basal, while in all analyses Hylobates appears to be the most recently derived. Within Nomascus, Nomascus sp. cf. nasutus is the most basal, followed by N. concolor, and then a clade of N. leucogenys and N. gabriellae. Within Hylobates, H. pileatus is the most basal, while H. moloch and H. klossii clearly, and H. agilis and H. muelleri likely form two more derived monophyletic clades. The segregation of H. klossii from other Hylobates species is not supported by this study. The present data are (1) consistent with the division of Hylobatidae into four distinct clades, (2) provide the first genetic evidence for all the species relationships within Nomascus, and (3) call for a revision of the current relationships among the species within Hylobates. We propose a phylogenetic tree as a working hypothesis against which intergeneric and interspecific relationships can be tested with additional genetic, morphological, and behavioral data.

Introduction

Gibbons or small apes (family Hylobatidae) are a relatively small and morphologically homogeneous group of primate species inhabiting closed canopy rain forests throughout Southeast Asia. The range of the Hylobatidae family is delineated by eastern India, southern China, Borneo, and Java. A distribution map of the genera is presented in Fig. 1 (for distribution maps of the species see Geissmann, 1995 and Geissmann et al., 2000). Habitat loss and fragmentation, habitat degradation, hunting (food, medicine, and sport), and illegal trade (pets, medicine) are the top four threats which have seriously threatened gibbons throughout their range (Geissmann, 2003b).

While gibbons represent one of the three major adaptive radiations of anthropoid primates in Southeast Asia, and despite several revisions of gibbon systematics (e.g. Geissmann, 1995, Groves, 1972, Marshall and Sugardjito, 1986, Pocock, 1927) and various scenarios proposed to explain the radiation of this group (e.g., Chivers, 1977, Groves, 1993, Haimoff et al., 1982), their evolutionary history and systematics remain largely unresolved. Phylogenetic relationships, even among the main divisions of the Hylobatidae family are unclear, and the total number of species is contested. Most published gibbon phylogenies are summarized in Fig. 2. The lack of resolution regarding hylobatid evolutionary history and systematics has been attributed to a lack of adequate sampling, inconsistencies among results obtained using different characters, and the effect of a presumed short time period during which gibbons have differentiated.

Fossil evidence applicable to gibbon evolution is very limited and its interpretation is considered problematic (Fleagle, 1984, Fleagle, 1999). Earlier studies applying morphological, behavioral or vocal characters to address the evolutionary relationships among gibbons have produced inconsistent results (Creel and Preuschoft, 1984, Geissmann, 1993, Geissmann, 2002a, Groves, 1972, Haimoff et al., 1982).

Genetic approaches to reconstructing the phylogeny of hylobatids have included cytogenetic studies and the sequencing of mitochondrial and nuclear genes. Cytogenetic studies based on unique karyotypes and diploid numbers divided the Hylobatidae into four groups often referred to as subgenera (Prouty et al., 1983), or more recently as genera (Brandon-Jones et al., 2004, Roos and Geissmann, 2001), namely Hylobates, Bunopithecus, Symphalangus, and Nomascus. The cytogenetic differentiation of these four groups is also supported by morphological (Marshall and Sugardjito, 1986, Prouty et al., 1983), and vocal data (Geissmann, 1995, Geissmann, 2002a). The classification and the genus assignments used in the present study are based on the most recent consensus taxonomy for gibbons (Brandon-Jones et al., 2004, Geissmann, 2002b, Geissmann, 2003a, Geissmann et al., 2000) (Table 1).

DNA sequence analysis of various segments of the mitochondrial and nuclear genome was used to resolve the relationships among and within the four main divisions of Hylobatidae. The cytochrome b region of the mitochondrial genome that has been subject to separate studies (Garza and Woodruff, 1992, Hall et al., 1998) produced incomplete or inconsistent results regarding the phylogenetic relationship of the main gibbon groups and the species within those groups. Partial sequences of ND4 and ND5 regions using limited species representation also did not allow the complete reconstruction of species groups or subgenus relationships (Hayashi et al., 1995). A consensus tree based on both previously published and new sequences of mitochondrial and nuclear DNA favored Bunopithecus as the first genus to diverge, with the next branch leading to Symphalangus and Nomascus as sister taxa (Zehr, 1999). Most recently, a study based on the fast evolving mitochondrial control region supported Nomascus as the most basal clade, followed by Symphalangus, with Bunopithecus and Hylobates as the last to diverge (Roos and Geissmann, 2001). In none of these studies, however, were all 12 recognized gibbon species across all four genera represented. In addition, these studies, were constrained by a lack of samples representing species from all four gibbon groups and a lack of enough variability in the relatively short segments of DNA analyzed.

In the present study, we investigated the phylogenetic relationships of the Hylobatidae at the tentative genus and species level. We sequenced the mitochondrial ND3, ND4L, and ND4 region from 34 individuals representing all 12 recognized species of living Hylobatidae. We performed several analyses to reconstruct the phylogenetic relationships among and within the major clades of gibbons.

Section snippets

Specimen information

A total of 34 specimens representing all 12 currently recognized species of Hylobatidae were genotyped and included in the present study (Table 2). Species identification was based on pelage, vocalization, morphology and geographical origin, and photographs were taken of most individuals. We did not include specimens where the identification of the species was questionable. Samples were collected from wild individuals or captive specimens maintained in zoos, rehabilitation centers, or as house

Sequence variation

Thirty-four specimens representing all extant species of hylobatids were sequenced for the mitochondrial ND3, ND4L, and ND4 region corresponding to base pairs from 9424 to 11,667 in Hylobates lar (GenBank X99256). Comparison of the aligned sequences with tRNAs removed from the ingroup taxa revealed 683 variable sites including 515 phylogenetically informative sites (903 variable with 682 phylogenetically informative sites including the outgroups) of the total 2016 bases sequenced (variable

Relationship among the genera

In the present study, we analyzed the phylogenetic relationship of all 12 currently recognized extant gibbon species using the mitochondrial ND3–ND4 region. Based on morphological, vocal, biochemical, and karyotypic evidence, it has been long recognized that the family Hylobatidae is composed of two (Schultz, 1933; Simonetta, 1957; Napier and Napier, 1967), and more recently, four distinct clades, often referred to as subgenera (Geissmann, 1995, Groves, 2001, Hayashi et al., 1995, Marshall and

Acknowledgments

We thank our colleagues, Drs. Jatna Supriatna and Noviar Andayani, and the Indonesian government for assistance in obtaining gibbon samples from Indonesia. All samples were properly permitted by the CITES authorities of Indonesia and the USA. We thank Prithiviraj Fernando and Ben Evans (Columbia University, New York, NY) for various comments and advice during this study. Michael Forstner and Jennifer Pastorini (Columbia University) generated some of the sequence data. We are grateful to

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