An Alu-Based Phylogeny of Gibbons (Hylobatidae)

Abstract

Gibbons (Hylobatidae) are small, arboreal apes indigenous to Southeast Asia that diverged from other apes 15-18 Ma. Extant lineages radiated rapidly 6-10 Ma and are organized into four genera (Hylobates, Hoolock, Symphalangus, and Nomascus) consisting of 12-19 species. The use of short interspersed elements (SINEs) as phylogenetic markers has seen recent popularity due to several desirable characteristics: the ancestral state of a locus is known to be the absence of an element, rare potentially homoplasious events are relatively easy to resolve, and samples can be quickly and inexpensively genotyped. During radiation of primates, one particular family of SINEs, the Alu family, has proliferated in primate genomes. Nomascus leucogenys (northern white-cheeked gibbon) sequences were analyzed for repetitive content with RepeatMasker using a custom library. The sequences containing Alu elements identified as members of a gibbon-specific subfamily were then compared with orthologous positions in other primate genomes. A primate phylogenetic panel consisting of 18 primate species, including 13 gibbon species representing all four extant genera, was assayed for all loci, and a total of 125 gibbon-specific Alu insertions were identified. The resulting amplification patterns were used to generate a phylogenetic tree. We demonstrate significant support for Symphalangus as the most basal lineage within the family. Our findings also place Nomascus as a derived lineage, sister to Hoolock, with the NomascusHoolock clade sister to Hylobates. Further, our analysis groups N. leucogenys and Nomascus siki as sister taxa to the exclusion of the other Nomascus species assayed. This study represents the first use of SINEs to determine the genus level phylogenetic relationships within the family Hylobatidae. These relationships have been resolved with robust support at most internal nodes, demonstrating the utility of SINE-based phylogenetic analysis. We postulate that hybridization and rapid radiation may have contributed to the complex and contradictory findings of the previous studies. Our findings will aid in the conservation of these threatened primates and inform future studies of the biogeographical history and distribution of modern gibbon species.

A Phylogeny Based on the Concatenated 9 Protein-coding Gene Sequences of Mt Genomes among Three Gibbon Genera

“…The family Hylobatidae is monophyletic with predominantly strongly supported (100% bootstrap support) and each of the three genera with multiple species also show monophyly with high support (98-100% bootstrap support). At this point, our result is consistent with all previous result, including numerous morphological and molecular studies on the phylogenetic relationships among Hylobatidae members (Hayashi et al, 1995;Müller et al, 2003;Brandon-Jones et al, 2004;Takacs et al, 2005;Monda et al, 2007;Whittaker et al, 2007;Matsudaira and Ishida, 2010;Kim et al, 2011;Chan et al, 2012;Meyer et al, 2012;Wall et al, 2013).…”

“…A number of molecular studies have been performed, including karyotypes (Müller et al, 2003), mitochondrial DNA (mtDNA) (Hayashi et al, 1995;Takacs et al, 2005;Monda et al, 2007;Whittaker et al, 2007;Chan et al, 2010;Matsudaira and Ishida, 2010), Y chromosomes (Chan et al, 2012), Arthrobacter luteus (ALU) repeats (Meyer et al, 2012), and short stretches of autosomal sequence (Kim et al, 2011;Wall et al, 2013), the phylogenetic relationships among the four gibbon genera are still confidently unresolved; phylogenetic relationships proposed in the studies using different data were inconsistent (reviewed in (Kim et al, 2011;Wall et al, 2013)). …”

Examining Phylogenetic Relationships Among Gibbon Genera Using Whole Genome Sequence Data Using an Approximate Bayesian Computation Approach

“…Primarily on the basis of their karyotypes, gibbons are now divided into four major genera, with Nomascus, Symphalangus, Hylobates, and Hoolock each possessing 52, 50, 44, and 38 diploid chromosomes, respectively. While many genetic studies have been performed, including a number based on karyotypes (Müller et al 2003), mitochondrial DNA (mtDNA) (Hayashi et al 1995;Takacs et al 2005;Monda et al 2007;Whittaker et al 2007;Matsudaira and Ishida 2010;Van Ngoc et al 2010), Y chromosomes (Chan et al 2012), Arthrobacter luteus (ALU) repeats (Meyer et al 2012), and short stretches of autosomal sequence Wall et al 2013), the phylogenetic relationships among the four gibbon genera remain unresolved, with at least seven different topologies being supported by different data. A recent study examined 1.5 Mb of orthologous autosomal sequence generated by second-generation sequencing from one individual representing each of the four genera .…”

“…mitochondrial DNA (mtDNA) (Hayashi et al 1995;Takacs et al 2005;Monda et al 2007;Whittaker et al 2007;Matsudaira and Ishida 2010;Van Ngoc et al 2010), Y chromosomes (Chan et al 2012), Arthrobacter luteus (ALU) repeats (Meyer et al 2012), and short stretches of autosomal sequence Wall et al 2013), the phylogenetic relationships among the four gibbon genera remain unresolved, with at least seven different topologies being supported by different data.…”

The phylogenetic species concept and its role in Southeast Asian mammal conservation

“…These four subgenera were subsequently raised to generic status (Brandon-Jones et al, 2004;Geissmann, 2002), and are now commonly recognised (e.g. Meyer et al, 2012;Takacs et al, 2005). Groves, therefore played a fundamental role in development of the currently understood systematics of the Hylobatidae at the generic level.…”