Patterns of Genetic Variation Within and Between Gibbon Species Open
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Patterns of Genetic Variation Within and Between Gibbon Species Sung K. Kim, ,1 Lucia Carbone, ,2,3 Celine Becquet,1 Alan R. Mootnick,4 David Jiang Li,2 Pieter J. de Jong,2 and Jeffrey D. Wall*,1,5 1Institute for Human Genetics, University of California San Francisco 2Children’s Hospital of Oakland Research Institute 3Department of Behavioral Neuroscience, Oregon Health and Science University 4Gibbon Conservation Center 5Department of Epidemiology and Biostatistics, University of California San Francisco These authors contributed equally to the work. *Corresponding author: E-mail: [email protected]. Research article Associate editor: Anne Stone Abstract Gibbons are small, arboreal, highly endangered apes that are understudied compared with other hominoids. At present, there are four recognized genera and approximately 17 species, all likely to have diverged from each other within the last 5–6 My. Although the gibbon phylogeny has been investigated using various approaches (i.e., vocalization, morphology, mitochondrial DNA, karyotype, etc.), the precise taxonomic relationships are still highly debated. Here, we present the first survey of nuclear sequence variation within and between gibbon species with the goal of estimating basic population genetic parameters. We gathered ;60 kb of sequence data from a panel of 19 gibbons representing nine species and all four genera. We observe high levels of nucleotide diversity within species, indicative of large historical population sizes. In addition, we find low levels of genetic differentiation between species within a genus comparable to what has been estimated for human populations. This is likely due to ongoing or episodic gene flow between species, and we estimate a migration rate between Nomascus leucogenys and N. gabriellae of roughly one migrant every two generations. Together, our findings suggest that gibbons have had a complex demographic history involving hybridization or mixing between diverged populations. Key words: population history, chromosomal rearrangements, genetic diversity, gibbon, population genetics. Introduction species have been identified; however, the global taxonomy for gibbons remains very controversial (Mootnick 2006; Mis- Gibbons are small apes native to the forests of Southeast, ceo et al. 2008; Van Ngoc, Mootnick, Geissmann et al. 2010; South, and East Asia. They belong to the same superfamily Van Ngoc, Mootnick Li et al. 2010). Gibbons are known for as humans and other great apes (Hominoidea), and their common ancestor was the first to branch off from the other their high rates of chromosomal rearrangements, estimated hominoids roughly 16–20 Ma (e.g., Matsudaira and Ishida to be roughly 10–20 times faster than the standard mam- 2010; Van Ngoc, Mootnick, Li et al. 2010). Most gibbon spe- malian rate (Misceo et al. 2008). This accelerated rate can cies are considered ‘‘endangered’’ or ‘‘critically endangered’’ be seen in the large number of rearrangements separating (IUCN 2009), and the Hainan gibbon (Nomascus hainanus), the Hylobatidae common ancestor from other hominoids with approximately 20 extant individuals, is the rarest pri- (Muller et al. 2003; Carbone et al. 2006), the numerous re- mate in the world (Mootnick et al. 2007). Despite their arrangements that separate different gibbon species, as well conservation importance and despite their distinct charac- as the rearrangements that are polymorphic within a species teristics such as accelerated karyotype evolution (cf. Muller (van Tuinen et al. 1999; Carbone, Mootnick, et al. 2009). et al. 2003; Carbone et al. 2006; Misceo et al. 2008)andhigh In contrast, humans and the other great apes are separated species diversity (Mootnick 2006; IUCN 2009; Van Ngoc, by just two interchromosomal rearrangements—a fusion Mootnick, Li et al. 2010), gibbons have mostly been ne- of two chromosomes that formed human chromosome glected by population genetic studies. We do not have even 2 and a reciprocal translocation that occurred on the gorilla basic data on levels of nuclear sequence diversity within or lineage (Dutrillaux et al. 1973). This makes gibbons a very divergence between gibbon species. good model to study factors responsible for chromosomal There are four currently recognized gibbon genera (Hy- instability in primate genomes. lobates, Nomascus, Symphalangus, and Hoolock), which are Previous phylogenetic and taxonomic studies have been defined by their different karyotypes: Their diploid chromo- conducted for gibbon species using different traits (i.e., vo- some counts vary from 2n 5 38–52. Overall, 17 gibbon calization, morphology, mitochondrial DNA [mtDNA], © The Author(s) 2011. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Open Access Mol. Biol. Evol. 28(8):2211–2218. 2011 doi:10.1093/molbev/msr033 Advance Access publication March 2, 2011 2211 Kim et al. · doi:10.1093/molbev/msr033 MBE Table 1. Specimen Information. Symbol Scientific name Common name ISIS# Institution Distribution NLE1 N. leucogenys northern white-cheeked gibbon NL605 GCC S Yunnan, N Lao PDR, NW Vietnam NLE2 N. leucogenys northern white-cheeked gibbon 982103 Columbus Zoo S Yunnan, N Lao PDR, NW Vietnam NLE3 N. leucogenys northern white-cheeked gibbon NL600 GCC S Yunnan, N Lao PDR, NW Vietnam NLE4 N. leucogenys northern white-cheeked gibbon 92 Gladys Porter Zoo S Yunnan, N Lao PDR, NW Vietnam NLE5 N. leucogenys northern white-cheeked gibbon NL607 GCC S Yunnan, N Lao PDR, NW Vietnam NLE6 N leucogenys northern white-cheeked gibbon NL606 GCC S Yunnan, N Lao PDR, NW Vietnam NLE7 N. leucogenys northern white-cheeked gibbon UNK Kunming Institute S Yunnan, N Lao PDR, NW Vietnam NGA1 N. gabriellae southern buff-cheeked gibbon 96070 Los Angeles Zoo S Vietnam, S Lao PDR, NE Cambodia NGA2 N. gabriellae southern buff-cheeked gibbon 96075 Los Angeles Zoo S Vietnam, S Lao PDR, NE Cambodia Hoolock HLE leucodenys eastern hoolock gibbon HL305 GCC E Myanmar, SW Yunnan, NE India SSY S. syndactylus siamang SS901 GCC NW & C Malay Peninsula, Sumatra HPI1 H. pileatus pileated gibbon HP103 GCC W Cambodia, SE Thailand, SW Lao PDR HPI2 H. pileatus pileated gibbon 8097 Gladys Porter Zoo W Cambodia, SE Thailand, SW Lao PDR HAGI1 H. agilis agile gibbon 94135 Fort Wayne Zoo Sumatra, Malay Peninsula HAGI2 H. agilis agile gibbon 94137 Fort Wayne Zoo Sumatra, Malay Peninsula HAGI3 H. agilis agile gibbon 15353 Henry Doorly Zoo Sumatra, Malay Peninsula HMO H. moloch Javan gibbon HMO894 GCC W and C Java HMU H. muelleri Mueller’s gibbon 86 Gladys Porter Zoo Borneo, except for the southwest SW Yunnan, N, C, & S Thailand, SE Myanmar, C & HLA Hylobates lar lar gibbon 9087 Gladys Porter Zoo S Malay Peninsula, N Sumatra NOTE.—List of the species, individuals, institution from which each sample was received and distribution of the species. Each gibbon species is abbreviated by the first letter of its genus and the two first letters of its species. karyotype, etc.) but with conflicting results. Initial genetic New York; British Museum (Natural History), London; Field variation studies in gibbons have focused on mtDNA (e.g., Museum of Natural History, Chicago; Institute of Ecology Hayashi et al. 1995; Takacs et al. 2005; Monda et al. 2007; and Biological Resources, Hanoi; Harvard Museum of Whittaker et al. 2007; Matsudaira and Ishida 2010; Van Comparative Zoology, Cambridge; Muse´um National d’His- Ngoc, Mootnick, Li et al. 2010), in part due to the difficulty toire Naturelle, Paris; Museum Zoologicum Borgoriense, in obtaining high-quality DNA samples from rare and en- Bogor; National Museum of Natural History, Washington, dangered gibbon species. However, the mitochondrion DC; Zoological Museum, Vietnam National University, makes up a very small fraction of the genome. A fuller pic- Hanoi; and Zoological Reference Collection, National Univer- ture of genetic diversity within and between gibbon species sity of Singapore, Singapore. Additional criteria for determin- and the evolutionary relationships among gibbon species ing taxonomic identification followed (Groves 1972; 2001; can only be achieved by a comprehensive study of nuclear Marshall and Sugardjito 1986; Geissmann 1995; Mootnick sequence variation. 2006; Van Ngoc, Mootnick, Geissmann, 2010; Mootnick In this study, we investigate levels of nuclear genetic di- and Fan 2011). Vocalizations of live specimens were com- versity in a panel of 19 unrelated individuals from nine dif- pared with Marshall et al. (1984), Marshall JT and Marshall ferent gibbon species, including representatives from all ER (1976, 1978),andMarshall and Sugardjito (1986). four genera. Because interspecific hybridization has been The Hylobatidae in this study that were housed at the linked both to speciation and to genome reshuffling GCC, Fort Wayne Children’s Zoo, Gladys Porter Zoo, Henry (O’Neil et al. 1998; Fontdevila 2005), we are interested in Doorly Zoo, and Los Angeles Zoo were observed in person the possibility of detecting gene flow between gibbon spe- to confirm their identification. The northern white- cies. Our study generated the largest autosomal genetic cheeked gibbon at the Columbus Zoo was identified by data set in gibbons, which was made possible, thanks to photographs of his sire and dam housed at the Columbus a unique sample collection of high-quality genomic DNA Zoo. The cell line from the Kunming Institute of Zoology from captive individuals. was a wild-born N. leucogenys, and this specimen’s species identification was also confirmed by Christian Roos. Materials and Methods Sequencing Specimen Identification Genomic DNA was extracted from gibbon whole blood us- The species identification of the Hylobatidae in this study ing Gentra Puregene DNA extraction kit (distributed by (table 1) was based on visual and auditorial examination Qiagen). We used about 100 ng of DNA for each long-range by Alan Mootnick of the gibbons housed at the Gibbon Con- polymerase chain reaction (PCR) reaction.