A Chromosomal Inversion Unique to the Northern White- Cheeked Gibbon Lucia Carbone1*, Alan R. Mootnick2, Tilo Nadler3, Pierre Moisson 4 , Oliver Ryder5, Christian Roos6, Pieter J. de Jong1 1 BACPAC Resources, Children’s Hospital of Oakland Research Institute, Oakland, California, United States of America, 2 Gibbon Conservation Center (GCC), Santa Clarita, California, United States of America, 3 Endangered Primate Rescue Center, Cuc Phuong National Park, Ninh Binh Province, Vietnam, 4 Parc Zoologique et Botanique, Mulhouse, France, 5 Zoological Society of San Diego, San Diego, California, United States of America, 6 German Primate Center, Leibniz-Institut for Primate Research, Go¨ ttingen, Germany Abstract The gibbon family belongs to the superfamily Hominoidea and includes 15 species divided into four genera. Each genus possesses a distinct karyotype with chromosome numbers varying from 38 to 52. This diversity is the result of numerous chromosomal changes that have accumulated during the evolution of the gibbon lineage, a quite unique feature in comparison with other hominoids and most of the other primates. Some gibbon species and subspecies rank among the most endangered primates in the world. Breeding programs can be extremely challenging and hybridization plays an important role within the factors responsible for the decline of captive gibbons. With less than 500 individuals left in the wild, the northern white-cheeked gibbon (Nomascus leucogenys leucogenys, NLE) is the most endangered primate in a successful captive breeding program. We present here the analysis of an inversion that we show being specific for the northern white-cheeked gibbon and can be used as one of the criteria to distinguish this subspecies from other gibbon taxa. The availability of the sequence spanning for one of the breakpoints of the inversion allows detecting it by a simple PCR test also on low quality DNA. Our results demonstrate the important role of genomics in providing tools for conservation efforts. Citation: Carbone L, Mootnick AR, Nadler T, Moisson P, Ryder O, et al. (2009) A Chromosomal Inversion Unique to the Northern White-Cheeked Gibbon. PLoS ONE 4(3): e4999. doi:10.1371/journal.pone.0004999 Editor: Michael Hofreiter, Max Planck Institute for Evolutionary Anthropology, Germany Received May 13, 2008; Accepted February 16, 2009; Published March 25, 2009 Copyright: 2009 Carbone et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors have no support or funding to report. Competing Interests: The authors have declared that no competing interests exist. * E-mail: lcarbone@chori.org Introduction Gibbons (family Hylobatidae) are small arboreal apes, which belong, together with humans and great apes, to the superfamily of Hominoidea. They inhabit tropical and semi-deciduous forests of Southeast Asia and small parts of South- and East-Asia [1–4]. Gibbons were the first to branch off from the other hominoids and display a set of characteristics distinctly different from great apes and humans. While gibbons are widely considered to form a monophyletic clade (Hylobatidae), there is no consensus about the taxonomy, phylogeny and evolutionary history within the family. Some of the earlier taxonomic manuscripts described the small apes to have two genera: Symphalangus (including one species) and Hylobates (including all other species) [4]. Subsequently, the family has been divided into four major clades, which were recognized as four subgenera [5] and eventually elevated to four genera [3,6,7]. This division takes into account the fact that species within each of the four major clades share a number of characteristics, most importantly a distinctive diploid chromosome number [2,3,8]: Hoolock (2n = 38), Hylobates (2n = 44), Symphalangus (2n = 50) and Nomascus (2n = 52). The genus Hoolock (hoolock gibbon) contains two species, while Symphalangus (siamang) consists of only a single species [3,7]. The genera Hylobates (44 chromosome gibbons) and Nomascus (crested gibbons) comprise seven and five species, respectively [1,9] (Table 1). The phylogenetic relationships among the four genera and among species have been examined at the level of morphology, taxonomy, behavior, vocalization, protein electrophoresis, molecular genetics and karyotyping, but this has not yet resulted in an unambiguous phylogeny [6,10]. However, at least for crested gibbon taxa, a clear branching pattern following a north to south axis is depicted by mitochondrial sequence data [9]. Some gibbon species are critically endangered and subject to captive breeding as part of the Species Survival Plan (SSP), with the ultimate goal of releasing physically and mentally healthy captive gibbons into a secure area of their native habitat. At this stage, to avoid undesirable hybridization with other taxa, it is essential that the release occurs in a proper location corresponding with the habitat of the same taxon [3]. Hybridization is detrimental to captive breeding or rehabilitation programs and it is also critical that hybridization does not occur when the animal is released into secure native habitat. On the other hand, the classification of gibbon species can be confusing and in some cases ‘‘visual’’ identification of a gibbon can be complicated by several factors (existence of different colors for the two sexes, variable color shades at different ages of the same gibbon, etc). The use of comparative genomics may therefore become important to assist with the classification of gibbons. Comparisons between gibbon chromosomes and those of other primates soon revealed that gibbons present an extraordinary level of evolutionary chromosomal rearrangements, which obscured PLoS ONE | www.plosone.org 1 March 2009 | Volume 4 | Issue 3 | e4999