Concordance between vocal and genetic diversity in crested gibbons

Background  

Gibbons or small apes are, next to great apes, our closest living relatives, and form the most diverse group of contemporary hominoids. A characteristic trait of gibbons is their species-specific song structure, which, however, exhibits a certain amount of inter- and intra-individual variation. Although differences in gibbon song structure are routinely applied as taxonomic tool to identify subspecies and species, it remains unclear to which degree acoustic and phylogenetic differences are correlated. To trace this issue, we comparatively analyse song recordings and mitochondrial cytochrome b gene sequence data from 22 gibbon populations representing six of the seven crested gibbon species (genus Nomascus). In addition, we address whether song similarity and geographic distribution can support a recent hypothesis about the biogeographic history of crested gibbons.     

The yellow-cheeked gibbon (Hylobates gabriellae) in nam bai cat tien (southern vietnam) revisited

Data concerning the status, habitat, and vocalizations of yellow-cheeked crested gibbons (Hylobates gabriellae) were collected during a short field trip to the Nam Bai Cat Tien National Park (southern Vietnam). Nam Bai Cat Tien may be the southernmost locality where crested gibbons (i.e. theHylobates concolor group) still survive. Fewer songs were heard at Nam Bai Cat Tien National Park than at other crested gibbon sites visited by the author. At least two gibbon groups appear to have been greatly reduced in number since previous surveys in the park. There is some evidence that both the gibbon population and the gibbon habitat in Nam Bai Cat Tien are disturbed. The first case of a great call solo song in wild gibbons of theconcolor group is reported. Great calls ofH. gabriellae are described and documented with sonagrams for the first time. They differ from those previously described forH. leucogenys.     

Crested gibbon (Hylobates [Nomascus]) identification using noninvasively obtained DNA

The development of captive breeding programs for the crested gibbons (Hylobates [Nomascus]) of Indochina is hindered by the difficulty of sorting individuals into their correct species and subspecies groups. We describe taxon-specific DNA sequence variation in a 252-base pair region of the mitochondrial cytochrome b gene, which can be used to identify individuals of the three taxa of crested gibbon commonly found in Western zoos. These molecular genetic markers can be amplified from plucked hair and will permit the identification of morphologically similar females and crested gibbons of either sex of unknown origin. Noninvasive genotyping of captive animals will facilitate the genetic management of these critically endangered primates. © 1994 Wiley-Liss, Inc.     

滇南、滇东南黑冠长臂猿分布与数量

滇南、滇东南曾是黑冠长臂猿广泛分布的地区之一。为掌握该地区近年黑冠长臂猿分布及种群数量现状,从2003年7月~2004年12月,采用访问调查及利用鸣声定位法进行了实地调查。调查结果显示,在近40000km2的范围内,东黑冠长臂猿(Nomascussp.cf.nasutus)在云南境内可能已消失;西黑冠长臂猿(N.concolor)亦仅发现4~7个种群,且孤立分布于3个地区(金平芭蕉河2群6只,金平西隆山1-2群,绿春黄连山1~3群,总计不超过25只),而在江城牛倮河自然保护区、马关古林箐自然保护区、麻栗坡老君山自然保护区及屏边大围山自然保护区可能已绝迹。滇南、滇东南黑冠长臂猿分布区缩小及种群数量剧减,主要与栖息地丧失及过度捕猎有关。     

Preliminary survey on the population and distribution of gibbons in yunnan province

Of the gibbons in China,Hylobates hoolock, H. lar, andH. concolor leucogenys are distributed only in Yunnan Province, whileH. c. concolor occurs limitedly in Yunnan Province and Hainan Island. During the periods from February to November 1984, and March to August 1985, the authors undertook surveys of the population and distribution of gibbons in 56 counties of 10 prefectures in Yunnan Province, and obtained the first reliable population and distribution data on the gibbons of this Province. The findings serve to fill an important blank in gibbon research in Yunnan and should pave the way for further research in the future.     

Anatomical Contributions to Hylobatid Taxonomy and Adaptation

Compared with the great apes, the small-bodied hylobatids were treated historically as a relatively uniform group with 2 genera, Hylobates and the larger-bodied Symphalangus. Four genera are now recognized, each with a different chromosome number: Hoolock (hoolock) (38), Hylobates (44), Nomascus (crested gibbon) (52), and Symphalangus (siamang) (50). Previous morphological studies based on relative bone lengths, e.g., intermembral indices; molar tooth sizes; and body masses did not distinguish the 4 genera from each other. We applied quantitative anatomical methods to test the hypothesis that each genus can be differentiated from the others using the relative distribution of body mass to the forelimbs and hind limbs. Based on dissections of 13 hylobatids from captive facilities, our findings demonstrate that each of the 4 genera has a distinct pattern of body mass distribution. For example, the adult Hoolock has limb proportions of nearly equal mass, a pattern that differentiates it from species in the genus Hylobates, e.g., H. lar (lar gibbon), H. moloch (Javan gibbon), H. pileatus (pileated gibbon), Nomascus, and Symphalangus. Hylobates is distinct in having heavy hind limbs. Although Symphalangus has been treated as a scaled up version of Hylobates, its forelimb exceeds its hind limb mass, an unusual primate pattern otherwise found only in orangutans. This research provides new information on whole body anatomy and adds to the genetic, ecological, and behavioral evidence for clarifying the taxonomy of the hylobatids. The research also underscores the important contribution of studies on rare species in captivity.     

Allelic variation of the dopamine receptor D4 gene polymorphic region in gibbons

We examined the tandem repeat sequence of the dopamine receptor D4 (DRD4) gene in 73 individuals derived from 8 species of gibbons (genusHylobates) in an attempt to assess the variability of this gene in gibbon species.H. syndactylus (subgenusSymphalangus) andH. concolor (subgenusNomascus), which were inferred to have diverged at an early time within the family Hylobatidae, shared only long repeat (7–8) alleles. On the other hand, DRD4 was highly polymorphic in gibbons of the subgenusHylobates, with 4-, 5-, 6-, 7-, and 8-repeat alleles being recognized. In this subgenus, 4- and 5-repeat alleles were found in the species distributed mainly in the southern islands such as Sumatra, Java, and Borneo but not in the species inhabiting the Asian continent. Sequence analysis indicated that the repeat structure of the gibbon DRD4 gene was quite complex but most of the 48-bp units could be classified into several groups across the species based on sequence similarities. However, the sequence of the 7-repeat allele ofH. muelleri was unique, since the repeat units had low similarities to other units of gibbons.     

Taxonomy,distribution, and status of gibbons (Hylobates) in Southern China and adjacent areas

Gibbons are small and arboreal apes restricted to southeastern tropical and southern subtropical regions in Asia. They are distributed from Assam in the northwest, eastward to south China and Vietnam, south through the Malay Peninsula to Sumatra, Borneo, Java, and the Mentawai Islands. Twenty-two genetically distinct populations of gibbons are generally recognized. Gibbons were once widely distributed in China; however, they are now primarily restricted to southern and southwestern Yunnan and Hainan Island. Their widest distribution and greatest species diversity is in Yunnan Province. Gibbons are rare in China and are now listed as a first class endangered species. Four gibbon species inhabit Yunnan Province in southern China. They areH. hoolock, H. lar, H. leucogenys, andH. concolor. There are three subspecies ofH. leucogenys: H. l. leucogenys, H. l. siki, andH. l. gabriellae. OnlyH. l. leucogenys inhabits China. Four subspecies ofH. concolor inhabit China. These areH. c. concolor, H. c. jingdongensis, H. c. furvogaster, andH. c. hainanus. The first three subspecies inhabit Yunnan andH. c. hainanus is found only on Hainan Island.H. lar yunnanensis is the subspecies ofH. lar in southern China.H. hoolock leucogenys is the subspecies ofH. hoolock in southern China.H. concolor jingdongensis, H. concolor furvogaster, andH. lar yunnanensis are all newly proposed subspecies byMa andWang (1986). The data on southern China gibbons presented here is based on an analysis of the skeletons and skins of 49 specimens held at the Kunming Institute of Zoology, Kunming, Yunnan.     

Phylogenetic Separation in Limb Use in Captive Gibbons (Hylobatidae): A Comparison Across the Primate Order

Although there have been few studies of self‐scratching in primates, some have reported distinct differences in whether hands or feet are used, and these variations seem to reflect the evolutionary history of the Order. Monkeys and prosimians use both hands and feet to self‐scratch while African great apes use hands almost exclusively. Gibbons represent an evolutionary divergence between monkeys and great apes and incidental observations at the Gibbon Conservation Center pointed to a difference in self‐scratching among the four extant gibbon genera (Hoolock, Nomascus, Symphalangus, and Hylobates). To validate and further explore these preliminary observations, we collected systematic data on self‐scratching from 32 gibbons, including nine species and all four genera. To supplement gibbon data, we also collected self‐scratching information from 18 great apes (four species), five prosimians (two species), 26 New World Monkeys (nine species) and 20 Old World Monkeys (seven species). All monkeys and some prosimians used both hands and feet to self‐scratch, whereas one prosimian species used only feet. All African great apes used hands exclusively (orangutans were an exception displaying occasional foot‐use). This appears to represent a fundamental difference between monkeys and great apes in limb use. Interestingly, there was a clear difference in self‐scratching between the four gibbon genera. Hylobates and Symphalangus self‐scratched only with hands (like all African great apes), while Hoolock and Nomascus self‐scratched with both hands and feet (like monkeys and prosimians). This difference in gibbon behavior may reflect the evolutionary history of gibbons as Hoolock and Nomascus are thought to have evolved before both Hylobates and Symphalangus. What evolutionary pressures led to this divergent pattern is currently opaque; however, this shift in limb preference may result from niche separation across the order facilitating differences in the behavioral repertoire associated with hind and forelimbs. Am. J. Primatol. 74:1035‐1043, 2012. © 2012 Wiley Periodicals, Inc.     

Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China

Predation on vertebrates is infrequent in gibbons. In a 14-month field study of the central Yunnan black crested gibbon (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed gibbons attacking, killing and eating giant flying squirrels (Petaurista philippensis). During 845 h of observation on one study group, the gibbons attacked giant flying squirrels 11 times, and succeeded in 4 cases. Although all members of the group attempted to attack the squirrels, all four successful attacks were made by the same adult female. The victims were infants in three cases and a juvenile or sub-adult in one case. Black crested gibbons also attacked adult giant flying squirrels by grabbing their long tails and throwing them from the canopy, but they failed to catch or kill the prey in three cases observed. Passive meat sharing occurred in three out of four successful cases. Besides hunting giant flying squirrels, the black crested gibbons also ate eggs or chicks in two birds’ nests and one lizard.     

Population and distribution of western black crested gibbon (Nomascus concolor) at Ailao Mountain, Xinping, Yunnan

The western black crested gibbon (Nomascus concolor) is mainly distributed in Yunnan, China. Ailao Mountain is located in central Yunnan and divided into three prefectures and six counties. This mountain forms the principle distribution range for western black crested gibbon; however, there are no published data on the gibbon population inhabiting the Xinping administrative. Take the interview results conducted in 2007 and 2009 with local people as the reference, this study conducted an extensive field survey covering all possible habitats from November 2009 to January 2010 using call surveys. Among the one hundred and twenty-four gibbon groups which were confirmed across the Ailao Mountain, the largest known population of western black crested gibbons yet, 85 groups inhabit the national nature reserve and adjacent national forest, 30 groups inhabit the provincial nature reserve and nine groups inhabit the collective forest located outside the reserve and national forest. We found that the western black crested gibbons here have a patchy distribution pattern and occur at higher densities in certain areas. Moreover, the population distribution density and elevation gradient distribution decline from north to south. The results also demonstrated the importance of Ailao Mountain in the western black crested gibbon protection.     

Taxonomic note: Bunopithecus: A genus-level taxon for the hoolock gibbon (Hylobates hoolock)

The recent discovery that the hoolock gibbon (Hylobates hoolock [Harlan, 1834]) has a karyotype distinct from all other hylobatids provides a new and strong motive for revising gibbon taxonomy and establishing hoolocks in a separate, higher taxon. Revising Groves's taxonomy of 1972, we propose that hoolock, along with the fossil species sericus, occupy a subgenus, Bunopithecus. With the newly added taxon, the genus Hylobates would thus contain four subgenera: Bunopithecus, Hylobates, Nomascus, and Symphalangus.     

Mitochondrial genome sequences effectively reveal the phylogeny of Hylobates gibbons

Background

Uniquely among hominoids, gibbons exist as multiple geographically contiguous taxa exhibiting distinctive behavioral, morphological, and karyotypic characteristics. However, our understanding of the evolutionary relationships of the various gibbons, especially among Hylobates species, is still limited because previous studies used limited taxon sampling or short mitochondrial DNA (mtDNA) sequences. Here we use mtDNA genome sequences to reconstruct gibbon phylogenetic relationships and reveal the pattern and timing of divergence events in gibbon evolutionary history.

Methodology/Principal Findings

We sequenced the mitochondrial genomes of 51 individuals representing 11 species belonging to three genera (Hylobates, Nomascus and Symphalangus) using the high-throughput 454 sequencing system with the parallel tagged sequencing approach. Three phylogenetic analyses (maximum likelihood, Bayesian analysis and neighbor-joining) depicted the gibbon phylogenetic relationships congruently and with strong support values. Most notably, we recover a well-supported phylogeny of the Hylobates gibbons. The estimation of divergence times using Bayesian analysis with relaxed clock model suggests a much more rapid speciation process in Hylobates than in Nomascus.

Conclusions/Significance

Use of more than 15 kb sequences of the mitochondrial genome provided more informative and robust data than previous studies of short mitochondrial segments (e.g., control region or cytochrome b) as shown by the reliable reconstruction of divergence patterns among Hylobates gibbons. Moreover, molecular dating of the mitogenomic divergence times implied that biogeographic change during the last five million years may be a factor promoting the speciation of Sundaland animals, including Hylobates species.     

Population differences and acoustic stability in male songs of wild western black crested gibbons (Nomascus concolor) in Mt. Wuliang, Yunnan

Population differences and acoustic stability in male songs of the western black crested gibbon (Nomascus concolor) at Mt. Wuliang, Yunnan, were investigated using data collected over 4 years. Detectable vocal differences were found between the western and eastern populations within Mt. Wuliang. Discriminant functions calculated using the phrases recorded in 2007-2008 correctly classified phrases recorded in 2009, and discriminant functions produced from phrases recorded in 2007-2009 could correctly classify phrases recorded in 2010 for 4 of 5 males. Results showed that the male songs of western black crested gibbons remain relatively stable over years. In light of the acoustic individuality in male songs of this gibbon species, which has recently been proved, and the acoustic stability shown in this research, we suggest that the song of male individuals may be useful in monitoring individuals or family groups of this species.     

Seasonal variation of diet and time budget of Eastern hoolock gibbons (Hoolock leuconedys) living in a northern montane forest

Most gibbons dwell in the tropical forests of Southeastern Asia, but eastern hoolock gibbons (Hoolock leuconedys) survive in high montane forest ranging from 1,600 to 2,700 m a.s.l. in Gaoligongshan (>24°30′N), Yunnan, China. To assess the behavioral adaptations of hoolock gibbons to the montane forest, we related temperature and food availability within the habitat to the seasonal behavioral patterns of a family group and a solitary female between August 2010 and September 2011 in Nankang, Gaoligongshan National Nature Reserve. The maximum temperature was 29.2 °C and the minimum temperature was ?0.3 °C during the period. The monthly mean temperature was <10 °C between December and February, making Nankang the coldest gibbon habitat reported so far. Nonfig fruit and fig availability declined to nearly zero in cold months. The family group increased resting and decreased travel and social behaviors when the monthly mean temperature was low. Compared with other gibbon populations, the hoolock gibbons spent proportionally less time feeding on figs and other fruit than other gibbon populations except Nomascus concolor and Symphalangus syndactylus. Only 36 species of plants provided nonfig fruit or figs, which is less than the number of fruit species consumed by any other gibbon population observed during a similar period of time (about 1 year). Hoolock gibbons shifted their diet to leaves and increased feeding time when fruit was not available. We conclude that diet flexibility and an energy-conserving strategy during the cold season when fruit is scarce have enabled the hoolock gibbons to survive in a northern montane forest.     

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

Gibbons are believed to have diverged from the larger great apes ∼16.8 MYA and today reside in the rainforests of Southeast Asia. Based on their diploid chromosome number, the family Hylobatidae is divided into four genera, Nomascus, Symphalangus, Hoolock, and Hylobates. Genetic studies attempting to elucidate the phylogenetic relationships among gibbons using karyotypes, mitochondrial DNA (mtDNA), the Y chromosome, and short autosomal sequences have been inconclusive . To examine the relationships among gibbon genera in more depth, we performed second-generation whole genome sequencing (WGS) to a mean of ∼15× coverage in two individuals from each genus. We developed a coalescent-based approximate Bayesian computation (ABC) method incorporating a model of sequencing error generated by high coverage exome validation to infer the branching order, divergence times, and effective population sizes of gibbon taxa. Although Hoolock and Symphalangus are likely sister taxa, we could not confidently resolve a single bifurcating tree despite the large amount of data analyzed. Instead, our results support the hypothesis that all four gibbon genera diverged at approximately the same time. Assuming an autosomal mutation rate of 1 × 10⁻⁹/site/year this speciation process occurred ∼5 MYA during a period in the Early Pliocene characterized by climatic shifts and fragmentation of the Sunda shelf forests. Whole genome sequencing of additional individuals will be vital for inferring the extent of gene flow among species after the separation of the gibbon genera.     

Vocal Diversity and Taxonomy of Nomascus in Cambodia

It is usually thought that Nomascus gabriellae is the only Nomascus sp. in Cambodia. We studied vocal diversity among different wild populations of Nomascus in Cambodia to assess their taxonomic relationships and to examine whether their vocal patterns correspond to forms previously described for Nomascus leucogenys siki and Nomascus gabriellae. We tape-recorded crested gibbon songs in southern Mondulkiri Province, in central Rattanakiri Province, and in 2 different districts of the Virachey National Park in northern Rattanakiri. We also tape-recorded typical songs of Nomascus leucogenys siki near the type locality of the taxon in the Bach Ma National Park in central Vietnam. We analyzed 40 song bouts from different gibbon groups, including 151 phrases of 33 females and 235 phrases of 39 males. Discriminant analyses revealed marked separation of the most southern songs (Mondulkiri) from those of all other localities. Vocal differences among the 3 gibbon populations in northeast Cambodia (Rattanakiri) are less pronounced; they do not differ more among each other than each of them differs from the northernmost sample from Bach Ma (Vietnam). Vocal characteristics of the study populations revealed no cline, and populations do not differ significantly in vocal variability. We conclude that Cambodian crested gibbons represent 2 distinct taxa: Those from southern Mondulkiri are Nomascus gabriellae, those from northeast Cambodia (Rattanakiri) closely correspond to the sample from Bach Ma (Vietnam) and, together with the latter, represent a different taxon. We provisionally assign them to Nomascus leucogenys siki because of the close geographic distance between Bach Ma and the type locality of the taxon. We postulate that a taxonal boundary exists between southern Mondulkiri and central Rattanakiri and discuss the possible factors that may have acted as distribution barriers.     

Preliminary observations of wild black-crested gibbons (Hylobates concolor concolor) in Yunnan province,people's republic of China

Black-crested gibbons (Hylobates concolor concolor), which inhabit the subtropical forests of southern China and northern Vietnam, have until now never been the subject of any systematic behavioral or ecological field study. This report presents the findings of a three-month field study of wild black-crested gibbons in the Wuliang and Ailao Mountain Game Reserves in Yunnan Province, People's Republic of China. The sites visited consisted of temperate, subtropical, broadleaf evergreen forests, with trees belonging to the families Elaeocarpaceae, Fagaceae, Lauraceae, Magnoliaceae, and Theaceae. Black-crested gibbons were documented from four sites visited and were found to be polygynous, with an average group size of seven to eight animals. The family groups were observed to comprise one adult male, from one to four adult females, and numerous offspring of various ages. Both sexes of this species emit interactive songs, and various features of this loud vocal behavior were analyzed and are discussed here. Since all other gibbon species were found to inhabit only tropical rain forests and live in strictly monogamous family groups, some of the ecological and evolutionary implications of these findings are also presented.     

Ecology and behavior of wild black-crested gibbons (Hylobates concolor) in China with a reconsideration of evidence for polygyny

The black-crested gibbon,Hylobates concolor, is one of the few species of gibbons that has not yet been the subject of a long term field study. Field observations in the Ai Lao and Wu Liang Mountains of Yunnan Province, China indicate that in this area the habitat and ecology of this species differ markedly from those of other gibbons that have been studied to date. These differences are correlated with some behavioral differences. In particular, these gibbons apparently have greater day ranges than other gibbons. It has also been suggested that this species lives in polygynous groups. To demonstrate this requires observation of groups with two or more females with young. Our own observations and those from other recent studies suggest that there are alternative explanations consistent with available data.     

Vocal Diversity and Taxonomy of <Emphasis Type="Italic">Nomascus</Emphasis> in Central Vietnam and Southern Laos

Previous researchers suggested that gibbon song repertoire is genetically determined and song characteristics are useful for assessing systematic relationships. The southern white-cheeked crested gibbon is regarded as either a subspecies of Nomascus leucogenys or its own species (Nomascus siki). I studied vocal diversity among different wild populations of Nomascus in central Vietnam and southern Laos to assess their taxonomic relationships and to examine whether their vocal patterns correspond to forms previously described for Nomascus siki. I examined the songs of 7 Nomascus populations in Vietnam and Laos. I analyzed 192 song bouts from different gibbon groups including 173 phrases of 42 females and 192 phrases of 42 males. Linear discriminant analysis, classification trees, and multidimensional scaling revealed marked separation of groups in the northern and southern populations. Within the 2 geographic populations, there is little variability and the vocal characteristics exhibited no apparent cline. I conclude that the northern and southern geographic populations may represent 2 distinct taxa. I postulate that a taxonal boundary such as large rivers existing between southern Quang Binh province and northern Thua-Thien Hue province in Vietnam and northern Phou Xang He NBCA and southern Dong Phou Vieng NBCA in Laos has limited gene flow between the populations. Differing topographic features could also serve as a selective force for improved sound transmission in a highly territorial species, driving the divergence between the 2 populations.