Chromosome studies in the orangutan (Pongo pygmaeus): Practical applications for breeding and conservation

The unequivocal identification of Bornean, Sumatran, and first-generation hybrid orangutans can be carried out by chromosome analysis, a procedure that is more reliable than any other so far used to distinguish between orangutan subspecies. Chromosome differences between subspecies have been compared with protein and DNA studies, and these have shown that Bornean and Sumatran orangutans are more different from each other than we originally thought. Chromosome studies in the orangutan have shown variant chromosome types that are not subspecies-specific. One of these variant types is a product of a complex double inversion rearrangement and is a polymorphic trait in both subspecies. In view of our findings, specific guidelines have been recommended for evaluating the fertility of hybrid specimens and maintaining purebred orangutan stocks.     

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.     

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     

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.     

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.     

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.     

Demographic history and genetic differentiation in apes

Comparisons of genetic variation between humans and great apes are hampered by the fact that we still know little about the demographics and evolutionary history of the latter species. In addition, characterizing ape genetic variation is important because they are threatened with extinction, and knowledge about genetic differentiation among groups may guide conservation efforts. We sequenced multiple intergenic autosomal regions totaling 22,400 base pairs (bp) in ten individuals each from western, central, and eastern chimpanzee groups and in nine bonobos, and 16,000 bp in ten Bornean and six Sumatran orangutans. These regions are analyzed together with homologous information from three human populations and gorillas. We find that whereas orangutans have the highest diversity, western chimpanzees have the lowest, and that the demographic histories of most groups differ drastically. Special attention should therefore be paid to sampling strategies and the statistics chosen when comparing levels of variation within and among groups. Finally, we find that the extent of genetic differentiation among "subspecies" of chimpanzees and orangutans is comparable to that seen among human populations, calling the validity of the "subspecies" concept in apes into question.     

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.     

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.     

Inferring Pongo conservation units: a perspective based on microsatellite and mitochondrial DNA analyses

In order to define evolutionarily significant and management units (ESUs and MUs) among subpopulations of Sumatran (Pongo pygmaeus abelii) and Bornean (P. p. pygmaeus) orangutans we determined their genetic relationships. We analyzed partial sequences of four mitochondrial genes and nine autosomal microsatellite loci of 70 orangutans to test two hypotheses regarding the population structure within Borneo and the genetic distinction between Bornean and Sumatran orangutans. Our data show Bornean orangutans consist of two genetic clusters—the western and eastern clades. Each taxon exhibits relatively distinct mtDNA and nuclear genetic distributions that are likely attributable to genetic drift. These groups, however, do not warrant designations as separate conservation MUs because they demonstrate no demographic independence and only moderate genetic differentiation. Our findings also indicate relatively high levels of overall genetic diversity within Borneo, suggesting that observed habitat fragmentation and erosion during the last three decades had limited influence on genetic variability. Because the mtDNA of Bornean and Sumatran orangutans are not strictly reciprocally monophyletic, we recommend treating these populations as separate MUs and discontinuing inter-island translocation of animals unless absolutely necessary.     

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.     

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.     

Genetic variation of complete mitochondrial genome sequences of the Sumatran rhinoceros (<Emphasis Type="Italic">Dicerorhinus sumatrensis</Emphasis>)

The Sumatran rhinoceros (Dicerorhinus sumatrensis) is the smallest and one of the most endangered rhinoceros species, with less than 100 individuals estimated to live in the wild. It was originally divided into three subspecies but only two have survived, D. sumatrensis sumatrensis (Sumatran subspecies), and D. s. harrissoni (Bornean). Questions regarding whether populations of the Sumatran rhinoceros should be treated as different management units to preserve genetic diversity have been raised, particularly in light of its severe decline in the wild and low breeding success in captivity. This work aims to characterize genetic differentiation between Sumatran rhinoceros subspecies using complete mitochondrial genomes, in order to unravel their maternal evolutionary history and evaluate their status as separate management units. We identified three major phylogenetic groups with moderate genetic differentiation: two distinct haplogroups comprising individuals from both the Malay Peninsula and Sumatra, and a third group from Borneo. Estimates of divergence time indicate that the most recent common ancestor of the Sumatran rhinoceros occurred approximately 360,000 years ago. The three mitochondrial haplogroups showed a common divergence time about 80,000 years ago corresponding with a major biogeographic event in the Sundaland region. Patterns of mitochondrial genetic differentiation may suggest considering Sumatran rhinoceros subspecies as different conservation units. However, the management of subspecies as part of a metapopulation may appear as the last resource to save this species from extinction, imposing a conservation dilemma.     

Geographical variation in and evolutionary history of the Sunda clouded leopard (Neofelis diardi) (Mammalia: Carnivora: Felidae) with the description of a new subspecies from Borneo

Recent morphological and molecular studies led to the recognition of two extant species of clouded leopards; Neofelis nebulosa from mainland southeast Asia and Neofelis diardi from the Sunda Islands of Borneo and Sumatra, including the Batu Islands. In addition to these new species-level distinctions, preliminary molecular data suggested a genetic substructure that separates Bornean and Sumatran clouded leopards, indicating the possibility of two subspecies of N. diardi. This suggestion was based on an analysis of only three Sumatran and seven Bornean individuals. Accordingly, in this study we re-evaluated this proposed subspecies differentiation using additional molecular (mainly historical) samples of eight Bornean and 13 Sumatran clouded leopards; a craniometric analysis of 28 specimens; and examination of pelage morphology of 20 museum specimens and of photographs of 12 wild camera-trapped animals. Molecular (mtDNA and microsatellite loci), craniomandibular and dental analyses strongly support the differentiation of Bornean and Sumatran clouded leopards, but pelage characteristics fail to separate them completely, most probably owing to small sample sizes, but it may also reflect habitat similarities between the two islands and their recent divergence. However, some provisional discriminating pelage characters are presented that need further testing. According to our estimates both populations diverged from each other during the Middle to Late Pleistocene (between 400 and 120 kyr). We present a discussion on the evolutionary history of Neofelis diardi sspp. on the Sunda Shelf, a revised taxonomy for the Sunda clouded leopard, N. diardi, and formally describe the Bornean subspecies, Neofelis diardi borneensis, including the designation of a holotype (BM.3.4.9.2 from Baram, Sarawak) in accordance with the rules of the International Code of Zoological Nomenclature.     

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.     

Variation in perikymata counts between repetitive episodes of linear enamel hypoplasia among orangutans from Sumatra and Borneo

The goal of this study is to evaluate whether repetitive linear enamel hypoplasia (rLEH) in apes is ecologically informative. LEH, which appears as grooves of thinner enamel often caused by malnutrition and/or disease, is a permanent record of departures from developmental homeostasis in infant and juvenile apes. Orangutans were selected for the study as they are a threatened species, have a remarkably high prevalence of rLEH, and because Sumatra is deemed a better habitat for orangutans than is Borneo, facilitating an ecological comparison. Objectives are to determine: a) whether periodicity of rLEH in orangutans corresponds to monsoon‐mediated cycles in precipitation or food; and b) whether patterning of rLEH supports the view that Borneo is an inferior habitat. This study compares the counts of perikymata between adjacent LEH from 9 Sumatran and 26 Bornean orangutans to estimate the periodicity of rLEH. A total of 131 nonredundant inter‐LEH perikymata counts were transformed to natural log values to reveal clusters of counts in a multiplicative series. Using a value of 10 days to form one perikyma, rLEH tends to recur semiannually in both populations. However, Sumatran orangutans show significantly fewer semiannual intervals and more annually recurring episodes. Bornean orangutans show mostly semiannual intervals and are more variable in inter‐LEH perikymata counts. It is concluded that: a) developmental conditions for infant orangutans in Sumatra protect them somewhat from seasonal and environmental variation; b) temporal patterning of rLEH indicates that Borneo is the poorer habitat for orangutans; and c) the study of rLEH can be ecologically informative. Am J Phys Anthropol 154:125–139, 2014. © 2014 Wiley Periodicals, Inc.     

A model for the evolution of developmental arrest in male orangutans

Male Sumatran orangutans (Pongo abelii) may delay for many years the acquisition of the full array of secondary sexual traits, including their characteristic cheek flanges. Such flexible developmental arrest is unique among male primates. Among male Bornean orangutans (Pongo pygmaeus) such long delays appear less common. Here, we develop a simple model to identify the conditions under which developmental arrest can be adaptive. We show that the baseline strategy (i.e., males are not susceptible to arrest) cannot be invaded by the flexible strategy (i.e., males can arrest their development when the conditions are unfavorable) when the potential for high‐ranking unflanged or flanged males to monopolize sexual access to females is low. In contrast, at high monopolization potential, the flexible strategy is the evolutionarily stable strategy. We also derive the proportion of flanged males in the population for each combination of monopolization values. This model concurs with field data that found a different monopolization potential between Bornean and Sumatran flanged males and a lower proportion of flanged males in the population in Sumatran orangutans. Pronounced developmental arrest is linked to very low adult mortality, which explains why it is so limited in its taxonomic distribution. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

Slow loris (Nycticebus borneanus) consumption by a wild Bornean orangutan (Pongo pygmaeus wurmbii)

Primates - Vertebrate predation and consumption by wild Bornean orangutans (Pongo pygmaeus spp.) is rare. In contrast to recorded observations of slow loris consumption by Sumatran orangutans...     

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.     

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.