Population history, biogeography, and taxonomy of orangutans (Genus: Pongo) based on a population genetic meta-analysis of multiple loci

This paper examines orangutan population history and evolution through a meta-analysis of seven loci collected from both Sumatran and Bornean orangutans. Within orangutans, most loci show that the Sumatran population is about twice as diverse as the Bornean population. Orangutans are more diverse than African apes and humans. Sumatran and Bornean populations show significant genetic differentiation from one another and their history does not differ significantly from an 'island model' (population splitting without gene flow). Two different methods support a divergence of Bornean and Sumatran orangutans at 2.7-5 million years ago. This suggests that Pleistocene events, such as the cyclical exposure of the Sunda shelf and the Toba volcanic eruption, did not have a major impact on the divergence of Bornean and Sumatran orangutans. Pairwise mismatch analyses, however, suggest that Bornean orangutans have undergone a recent population expansion (beginning 39,000-64,000 years ago), while Sumatran orangutan populations were stable. Pleistocene events may have contributed to these aspects of orangutan population history. These conclusions are applied to the debate on orangutan taxonomy.     

Factors Affecting Mortality,Fertility, and Well-being in Relation to Species Differences in Captive Orangutans

For the past 20 years, field biologists have recognized Sumatran and Bornean orangutans as belonging to 2 separate subspecies. Primatologists have recently suggested that they may be full species and that the Bornean species could be divided into 3–5 subspecies. Statistical analyses of factors affecting the mortality, fertility, and well-being of captive orangutans have revealed some important differences between Bornean, Sumatran, and hybrid orangutans that could support the suggestion. Hybrid orangutans appeared to be genetically weaker, with much lower survival rates than pure subspecific individuals. The weakness also may have contributed to their higher rate of infant rejection. In addition, infertility was 3 times higher in Bornean orangutans than in Sumatran and hybrid orangutans.     

The mitochondrial DNA molecule of sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan

The complete mitochondrial DNA (mtDNA) molecule of Sumatran orangutan, plus the complete mitochondrial control region of another Sumatran specimen and the control regions and five protein-coding genes of two specimens of Bornean orangutan were sequenced and compared with a previously reported complete mtDNA of Bornean orangutan. The two orangutans are presently separated at the subspecies level. Comparison with five different species pairs—namely, harbor seal/grey seal, horse/donkey, fin whale/blue whale, common chimpanzee/pygmy chimpanzee, and Homo/common chimpanzee—showed that the molecular difference between Sumatran and Bornean orangutan is much greater than that between the seals, and greater than that between the two chimpanzees, but similar to that between the horse and the donkey and the fin and blue whales. Considering their limited morphological distinction the comparison revealed unexpectedly great molecular difference between the two orangutans. The nucleotide difference between the orangutans is about 75% of that between Homo and the common chimpanzee, whereas the amino acid difference exceeds that between Homo and the common chimpanzee. On the basis of their molecular distinction we propose that the two orangutans should be recognized as different species, Pongo pygmaeus, Bornean orangutan, and P. abelii, Sumatran orangutan. Received: 15 May 1996 / Accepted: 21 June 1996     

Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus

Mitochondrial DNA control region sequences of orangutans (Pongo pygmaeus) from six different populations on the island of Borneo were determined and analyzed for evidence of regional diversity and were compared separately with orangutans from the island of Sumatra. Within the Bornean population, four distinct subpopulations were identified. Furthermore, the results of this study revealed marked divergence, supportive evidence of speciation between Sumatran and Bornean orangutans. This study demonstrates that, as an entire population, Bornean orangutans have not experienced a serious genetic bottleneck, which has been suggested as the cause of low diversity in humans and east African chimpanzees. Based on these new data, it is estimated that Bornean and Sumatran orangutans diverged approximately 1.1 MYA and that the four distinct Bornean populations diverged 860,000 years ago. These findings have important implications for management, breeding, and reintroduction practices in orangutan conservation efforts.     

Mitochondrial 16S rRNA sequence diversity of hominoids

We determined nucleotide sequences of the 16S rRNA gene of mitochondrial DNA (mtDNA) (about 1.6 kb) for 35 chimpanzee, 13 bonobo, 10 gorilla, 16 orangutan, and 23 gibbon individuals. We compared those data with published sequences and estimated nucleotide diversity for each species. All the ape species showed higher diversity than human. We also constructed phylogenetic trees and networks. The two orangutan subspecies were clearly separated from each other, and Sumatran orangutans showed much higher nucleotide diversity than Bornean orangutans. Some gibbon species did not form monophyletic clusters, and variation within species was not much different from that among species in the subgenus Hylobates.     

Call diversity of wild male orangutans: a phylogenetic approach

Over the past 20 years several studies have attempted to clarify orangutan systematics based on DNA sequences and karyological and morphological data; however, the systematic and phylogenetic relationships among orangutan taxa remain controversial. Surprisingly, few systematic studies have used data from wild-living orangutans of exactly known provenance. Furthermore, most of these studies pooled data from huge geographic areas in their analyses, thus ignoring possibly distinct subpopulations. This study represents a new approach to orangutan systematics that uses orangutan long calls. Long calls are species-specific vocalizations used by many nonhuman primates, and data on their acoustical and temporal structures have been used to assess the relationships among, and phylogenies of, several primate taxa. Altogether, 78 long calls from wild-living orangutans from five populations in Borneo and five in Sumatra were included in the analyses. Aside from the chiefly paraphyletic topology of cladistic results, which neither support nor reject a Borneo-Sumatra dichotomy, bootstrap values support three monophyletic clades (northwest Borneo, northeast-east Borneo, and Ketambe) that corroborate geographic groups. The shortest trees and multivariate analyses provide some support for a closer relationship between Sumatran and specific Bornean demes than between particular Bornean demes themselves, indicating that conservation management should be based on orangutans from different populations rather than on just the two island-specific groups.     

North American orangutan species survival plan: Current status and progress in the 1980s

The SSP program for orangutan (Pongo pygmaeus ssp.) was initiated in 1982. Since that time, the Propagation Group has dealt with issues related to improving captive management of the species. Prior to 1982, most orangutans in North America were managed as a single species, though a number of institutions did house their Bornean and Sumatran specimens separately. However, the determination of race at that time was made largely on the basis of physical appearance, a method subsequently proven imprecise. A major achievement of the SSP has been the refinement of orangutan subspecies determination; SSP-sponsored karotyping has determined, on a chromosomal level, the true subspecies of virtually every orangutan managed by the SSP. The validity of these results has been confirmed by recent fieldwork, also completed under the auspices of the SSP. Since 1985, as a result of these captive and field data, the SSP has held to the policy that subspecific hybrid orangutans should not be produced; to that end, there is a moratorium on the breeding of hybrid animals. Another significant step taken by the SSP group is the completion of the sophisticated demographic and genetic analyses, leading to the development of a Masterplan for this species and its captive management. Goals for the near future include refinement of the Masterplan analyses and publication of a new international studbook for the species.     

The phylogeography of orangutan foamy viruses supports the theory of ancient repopulation of Sumatra

Phylogenetic analysis of foamy virus sequences obtained from Bornean and Sumatran orangutans showed a distinct clustering pattern. One subcluster was represented by both Bornean and Sumatran orangutan simian foamy viruses (SFV). Combined analysis of host mitochondrial DNA and SFV phylogeny provided evidence for the hypothesis of the repopulation of Sumatra by orangutans from Borneo.     

Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo

Orangutans are amongst the most craniometrically variable of the extant great apes, yet there has been no attempt to explicitly link this morphological variation with observed differences in behavioral ecology. This study explores the relationship between feeding behavior, diet, and mandibular morphology in orangutans. All orangutans prefer ripe, pulpy fruit when available. However, some populations of Bornean orangutans (Pongo pygmaeus morio and P. p. wurmbii) rely more heavily on bark and relatively tough vegetation during periods of low fruit yield than do Sumatran orangutans (Pongo abelii). I tested the hypothesis that Bornean orangutans exhibit structural features of the mandible that provide greater load resistance abilities to masticatory and incisal forces. Compared to P. abelii, P. p. morio exhibits greater load resistance abilities as reflected in a relatively deeper mandibular corpus, deeper and wider mandibular symphysis, and relatively greater condylar area. P. p. wurmbii exhibits most of these same morphologies, and in all comparisons is either comparable in jaw proportions to P. p. morio, or intermediate between P. p. morio and P. abelii. These data indicate that P. p. morio and P. p. wurmbii are better suited to resisting large and/or frequent jaw loads than P. abelii. Using these results, I evaluated mandibular morphology in P. p. pygmaeus, a Bornean orangutan population whose behavioral ecology is poorly known. Pongo p. pygmaeus generally exhibits relatively greater load resistance capabilities than P. abelii, but less than P. p. morio. These results suggest that P. p. pygmaeus may consume greater amounts of tougher and/or more obdurate foods than P. abelii, and that consumption of such foods may intensify amongst Bornean orangutan populations. Finally, data from this study are used to evaluate variation in craniomandibular morphology in Khoratpithecus piriyai, possibly the earliest relative of Pongo from the late Miocene of Thailand, and the late Pleistocene Hoa Binh subfossil orangutan recovered from Vietnam. With the exception of a relatively thicker M(3) mandibular corpus, K. piriyai has jaw proportions that would be expected for an extant orangutan of comparable jaw size. Likewise, the Hoa Binh subfossil does not differ in skull proportions from extant Pongo, independent of the effects of increase in jaw size. These results indicate that differences in skull and mandibular proportions between these fossil and subfossil orangutans and extant Pongo are allometric. Furthermore, the ability of K. piriyai to resist jaw loads appears to have been comparable to that of extant orangutans. However, the similarity in jaw proportions between P. abelii and K. piriyai suggest the latter may have been dietarily more similar to Sumatran orangutans.     

Dietary and Energetic Responses of Pongo abelii to Fruit Availability Fluctuations

Like many primates, orangutans face fluctuations in fruit availability. We show that in Ketambe (Sumatra), fruit availability fluctuations have very little influence on orangutan diet. Most importantly, the percentages of fruits including figs, fruits excluding figs, and figs in their diet do not differ significantly between periods of varying fruit availability. In addition, there is no trace of ketones in orangutan urine samples during periods of varying fruit availability. Unlike 1 orangutan population in Borneo, orangutans in Sumatra experience no prolonged negative energy budget because of fluctuations in fruit availability. Dietary data from other Sumatran and Bornean orangutan populations indicate that the pattern might be representative for a more general difference between Sumatra and Borneo, and we discuss how this might have affected orangutan reproduction and life history for the 2 species.     

Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant Orangutans (genus: Pongo)

The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.     

Enamel thickness in Bornean and Sumatran orangutan dentitions

Dental enamel thickness has received considerable attention in ecological models of the adaptive significance of primate morphology. Several authors have theorized that the degree of enamel thickness may reflect selective pressures related to the consumption of fallback foods (dietary items that may require complex processing and/or have low nutritional value) during times of preferred food scarcity. Others have speculated that enamel thickness reflects selection during mastication of foods with particular material properties (i.e., toughness and hardness). Orangutans prefer ripe fruit when available, but show interspecific and sex differences in the consumption of fallback foods (bark, leaves, and figs) and other preferred foods (certain seeds). Bornean orangutans (Pongo pygmaeus) have also been reported to masticate more mechanically demanding foods than Sumatran orangutans (Pongo abelii). To test these ecological models, we assessed two-dimensional enamel thickness in orangutan full dentitions using established histological and virtual quantification methods. No significant differences in average enamel thickness (AET) were found between species. We found significant differences in the components of enamel thickness indices between sexes, with males showing greater enamel-dentine junction lengths and dentine core areas, and thus relatively thinner enamel than females. Comparisons of individuals of known sex and species revealed a dentition-wide trend for Bornean females to show greater AET than Sumatran females. Differences between small samples of males were less evident. These data provide only limited support for ecological explanations of enamel thickness patterns within great ape genera. Future studies of dietary ecology and enamel thickness should consider sex differences more systematically.     

Life history of wild Sumatran orangutans (Pongo abelii)

We present life history data on wild Sumatran orangutans gleaned from a 32-year and a 5.5-year study. Estimated age at first reproduction was 15.4 years. At 9.3 years, the average interbirth interval for this population is the longest ever recorded for any great ape population, significantly longer than that of a Bornean orangutan population. We find that age-specific mortality of Sumatran orangutans does not differ between sexes and is significantly lower than that of wild chimpanzees. We conclude that orangutan life history is the slowest among extant great apes. In accordance with their slow life history, longevity in the wild is estimated to be at least 58 years for males and at least 53 for females. We find no evidence for menopause. These data suggest that compared to the ancestral state, humans have undergone less of an increase in longevity than commonly assumed, and have experienced selection on earlier cessation of reproduction.     

Plasticity of human chromosome 3 during primate evolution

Comparative mapping of more than 100 region-specific clones from human chromosome 3 in Bornean and Sumatran orangutans, siamang gibbon, and Old and New World monkeys allowed us to reconstruct ancestral simian and hominoid chromosomes. A single paracentric inversion derives chromosome 1 of the Old World monkey Presbytis cristata from the simian ancestor. In the New World monkey Callithrix geoffroyi and siamang, the ancestor diverged on multiple chromosomes, through utilizing different breakpoints. One shared and two independent inversions derive Bornean orangutan 2 and human 3, implying that neither Bornean orangutans nor humans have conserved the ancestral chromosome form. The inversions, fissions, and translocations in the five species analyzed involve at least 14 different evolutionary breakpoints along the entire length of human 3; however, particular regions appear to be more susceptible to chromosome reshuffling. The ancestral pericentromeric region has promoted both large-scale and micro-rearrangements. Small segments homologous to human 3q11.2 and 3q21.2 were repositioned intrachromosomally independent of the surrounding markers in the orangutan lineage. Breakage and rearrangement of the human 3p12.3 region were associated with extensive intragenomic duplications at multiple orangutan and gibbon subtelomeric sites. We propose that new chromosomes and genomes arise through large-scale rearrangements of evolutionarily conserved genomic building blocks and additional duplication, amplification, and/or repositioning of inherently unstable smaller DNA segments contained within them.     

The Population Genetics of the α-2 Globin Locus of Orangutans (Pongo pygmaeus)

In this study, the molecular population genetics of the orangutans -2 globin (HBA2) gene were investigated in order to test for the action of natural selection. Haplotypes from 28 orangutan chromosomes were collected from a 1.46-kilobase region of the -2 globin locus. While many aspects of the data were consistent with neutrality, the observed heterogeneous distribution of polymorphisms was inconsistent with neutral expectations. Furthermore, a single amino acid variant, found in both the Bornean and the Sumatran orangutan subspecies, was associated with different alternative synonymous variants in each subspecies, suggesting that the allele may have spread separately through the two subspecies after two distinct origination events. This variant is not in Hardy–Weinberg equilibrium (HWE). These observations are consistent with neutral models that incorporate population structure and models that invoke selection. The orangutan Plasmodium parasite is a plausible selective agent that may underlie the variation at -2 globin in orangutans.This article contains electronic supplementary material.[Reviewing Editor: Dr. Deborah Charlesworth]Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession numbers AY372078–AY372110.     

Genetic Divergence of Orangutan Subspecies (Pongo pygmaeus)

Microsatellites and mitochondrial DNA sequences were studied for the two subspecies of orangutans (Pongo pygmaeus), which are located in Borneo (P. p. pygmaeus) and Sumatra (P. p. abelii), respectively. Both subspecies possess marked genetic diversity. Genetic subdivision was identified within the Sumatran orangutans. The genetic differentiation between the two subspecies is highly significant for ND5 region but not significant for 16s rRNA or microsatellite data by exact tests, although F _ST estimates are highly significant for these markers. Divergence time between the two subspecies is approximately 2.3 ± 0.5 million years ago (MYA) estimated from our data, much earlier than the isolation of their geological distribution. Neither subspecies underwent a recent bottleneck, though the Sumatran subspecies might have experienced expansion approximately 82,000 years ago. The estimated effective population sizes for both subspecies are on the order of 10⁴. Our results contribute additional information that may be interpreted in the context of orangutan conservation efforts. Received: 13 June 2000 / Accepted: 30 January 2000     

mtDNA Sequence Diversity of Orangutans from the Islands of Borneo and Sumatra

A comparison of mitochondrial DNA sequences was undertaken for two genes among orangutans from Borneo and Sumatra. The distribution of haplotypes among 42 individuals for NADH dehydrogenease subunit 3 and 39 individuals for cytochrome B was used to infer population structure. The haplotypes among all Bornean orangutans form a cluster of closely related individuals for both genes, with two distinct haplotypes occupying different regions of the island. Sumatran haplotypes fall into three distinct, and highly diverged, groups. Strikingly, one of the Sumatran haplotypes shares sequence identity with the most widespread Bornean haplotype. This haplotype distribution is considered in the context of the highly complex geological history for the area around the Malay Archipelago. Alternating periods of geographic isolation and reunion, resulting from glacially induced land bridge formation, presented substantial opportunity for population dispersal between periodically isolated demes. We present a paleodispersal model that is consistent with genetic, geological, paleoecological, and fossil data. The disparity of sequences present in orangutan populations argues against a simple Sumatra–Borneo dichotomy. Our evidence, and that of others, suggests that the Sumatran population alone contains the remnants of at least three separate lineages. Received: 3 February 1999 / Accepted: 2 August 2000     

Fertility and mortality patterns of captive Bornean and Sumatran orangutans: is there a species difference in life history?

Across broad taxonomic groups, life history models predict that increased ecological predictability will lead to conservative investment in reproductive effort. Within species, however, organisms are predicted to have increased reproductive rates under improved environmental conditions. It is not clear how these models apply to closely-related species. In this paper, we examine predictions from these models as applied to variability in reproductive rates between the two species of orangutans, Pongo pygmaeus (Bornean) and Pongo abelii (Sumatran). Orangutans exhibit characteristics of a "slow" life history strategy with large bodies, late age at maturity, low reproductive rates, and long lifespan. Recently, researchers proposed that Sumatran orangutans may have an even slower life history than Bornean orangutans as a result of ecological and genetic differences (Wich et al., 2004). We examined this hypothesis by studying important aspects of life history of both species under conditions of relative ecological stability, in captivity. In this large dataset, there were no significant species differences in age of first or last reproduction, completed fertility, perinatal and postnatal mortality, or female longevity. Bornean orangutans in captivity did have significantly longer interbirth intervals, and male Bornean orangutans had higher survival past maturity. Our results do not support the hypothesis that selection has led to decreased reproductive effort under conditions of increased habitat quality in Sumatra (Wich et al., 2004), and instead suggest that phenotypic flexibility may be particularly important in explaining differences between closely related species.     

Apes in space: saving an imperilled orangutan population in Sumatra

Deforestation rates in Sumatra are amongst the highest in the tropics. Lowland forests, which support the highest densities of orangutans, are particularly vulnerable to clearance and fragmentation because they are highly accessible. Consequently, many orangutans will, in the future, live in strictly or partially isolated populations. Whilst orangutans have been extensively studied in primary forests, their response to living in human-dominated landscapes remains poorly known, despite it being essential for their future management. Here, we focus on an isolated group of critically endangered Sumatran orangutans (Pongo abelii) that co-exist with farmers in a mixed agroforest system consisting of degraded natural forest, smallholder (predominantly rubber) farms and oil palm plantations. Over 24 months we conducted the first ever spatial assessment of orangutan habitat use in the human-transformed landscape of Batang Serangan, North Sumatra. From 1,204 independent crop-raiding incidents recorded, orangutans showed strong foraging preference for mixed farmland/degraded forest habitat over oil palm patches. The core home range areas of the eight adult orangutans encompassed only 14% of the available study area. Monthly home range sizes averaged 423 ha (±139, SD) for males, and 131 ± 46 ha for females, and were positively influenced by wild and cultivated fruit presence, and by crop consumption. The average daily distance travelled was similar for both adult males (868 m ± 350, SD) and females (866 m ± 195), but increased when orangutans raided crops. These findings show that orangutans can survive, demographically, in certain types of degraded landscapes, foraging on a mixture of crops and wild fruits. However, the poor quality habitat offered to orangutans by oil palm plantations, in terms of low food availability and as a barrier to female movements, is cause for concern since this is the land use type that is most rapidly replacing the preferred forest habitat across both Sumatran and Bornean orangutan ranges.     

A polymorphic structural rearrangement in the chromosomes of two populations of orangutan

A rearranged chromosome 9 was found in 12 of 23 specimens of orangutan, 4 of Bornean and 8 of Sumatran origin. Nine animals were heterozygous, and 3 were homozygous carriers for the variant chromosome, which was also traced in 4 other animals not studied by us. This type of chromosome rearrangement has been previously described (Seuánez et al., 1976) and is probably the same chromosome shown by Lucas et al. (1973) and reported by Turleau et al. (1975) in other specimens. There is obviously a very high incidence of this variant chromosome 9 in Pongo pygmaeus, and it is unlikely that it could result from independent rearrangements occurring in unrelated specimens from two geographically isolated populations (Sumatran and Bornean). It is concluded that the rearrangement is of ancient origin and that it has been maintained in the populations of Pongo as a balanced polymorphism. This type of complex rearrangement resulting from two pericentric inversions, one inside the other, is compared with certain sporadic pericentric inversions in the human complement, with pericentric inversions which are polymorphic in other mammals, and with pericentric inversions involved in chromosome evolution in the Hominoidea.