Orangutan Species Research Articles

A New Isolation with Migration Model along Complete Genomes Infers Very Different Divergence Processes among Closely Related Great Ape Species

We present a hidden Markov model (HMM) for inferring gradual isolation between two populations during speciation, modelled as a time interval with restricted gene flow. The HMM describes the history of adjacent nucleotides in two genomic sequences, such that the nucleotides can be separated by recombination, can migrate between populations, or can coalesce at variable time points, all dependent on the parameters of the model, which are the effective population sizes, splitting times, recombination rate, and migration rate. We show by extensive simulations that the HMM can accurately infer all parameters except the recombination rate, which is biased downwards. Inference is robust to variation in the mutation rate and the recombination rate over the sequence and also robust to unknown phase of genomes unless they are very closely related. We provide a test for whether divergence is gradual or instantaneous, and we apply the model to three key divergence processes in great apes: (a) the bonobo and common chimpanzee, (b) the eastern and western gorilla, and (c) the Sumatran and Bornean orang-utan. We find that the bonobo and chimpanzee appear to have undergone a clear split, whereas the divergence processes of the gorilla and orang-utan species occurred over several hundred thousands years with gene flow stopping quite recently. We also apply the model to the Homo/Pan speciation event and find that the most likely scenario involves an extended period of gene flow during speciation.

Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.)

In contrast to most primate species, including the other great apes, orangutans maintain a fission–fusion social system in the wild without being part of a stable community. In zoos, however, they are kept in permanent groups, usually consisting of one adult male and several females. In zoo orangutans, we predict higher levels of glucocorticoids and androgens in the Bornean species compared to its congener from Sumatra, due to the much more solitary lifestyle of Bornean orangutans and the apparent higher frequency of male aggression directed towards females in this species in the wild. To compare hormone levels of the two orangutan species, we validated a fecal glucocorticoid and a fecal androgen assay. Subsequently, fecal samples from a total of 73 female and 38 male orangutans housed in 29 European zoos were analyzed to investigate the effect of species, social group size, age and (for female glucocorticoid levels) reproductive state and the presence of adult males on fecal hormone metabolite concentrations. The results of linear mixed effect models indicate that both male and female Bornean orangutans show a steeper increase in glucocorticoid levels with increasing group size than Sumatran orangutans. We therefore conclude that Sumatran zoo orangutans are better able to adjust to social housing conditions than their Bornean congeners. In addition, our analyses reveal higher glucocorticoid levels in lactating females of both species compared to non-lactating and juvenile females. Concerning androgen levels in males, our analyses revealed significantly higher concentrations in Bornean than Sumatran orangutans. These differences in both glucocorticoid and androgen output between the two species of orangutan are presumably linked to ecological and behavioral differences and could possibly be attributed to phenotypic plasticity. However, given that we found interspecific differences in hormone excretion in captivity, where both species live under very similar conditions, we conclude that this variation has a genetic basis.

Estimating Divergence Time and Ancestral Effective Population Size of Bornean and Sumatran Orangutan Subspecies Using a Coalescent Hidden Markov Model

Due to genetic variation in the ancestor of two populations or two species, the divergence time for DNA sequences from two populations is variable along the genome. Within genomic segments all bases will share the same divergence—because they share a most recent common ancestor—when no recombination event has occurred to split them apart. The size of these segments of constant divergence depends on the recombination rate, but also on the speciation time, the effective population size of the ancestral population, as well as demographic effects and selection. Thus, inference of these parameters may be possible if we can decode the divergence times along a genomic alignment. Here, we present a new hidden Markov model that infers the changing divergence (coalescence) times along the genome alignment using a coalescent framework, in order to estimate the speciation time, the recombination rate, and the ancestral effective population size. The model is efficient enough to allow inference on whole-genome data sets. We first investigate the power and consistency of the model with coalescent simulations and then apply it to the whole-genome sequences of the two orangutan sub-species, Bornean (P. p. pygmaeus) and Sumatran (P. p. abelii) orangutans from the Orangutan Genome Project. We estimate the speciation time between the two sub-species to be thousand years ago and the effective population size of the ancestral orangutan species to be , consistent with recent results based on smaller data sets. We also report a negative correlation between chromosome size and ancestral effective population size, which we interpret as a signature of recombination increasing the efficacy of selection.

Comparative and demographic analysis of orang-utan genomes

“Orangutan” is derived from the Malay term “man of the forest” and aptly describes the Southeast Asian great apes native to Sumatra and Borneo. The orangutan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orangutan draft genome assembly and short read sequence data from five Sumatran and five Bornean orangutan genomes. Our analyses reveal that, compared to other primates, the orangutan genome has many unique features. Structural evolution of the orangutan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe the first primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orangutan genome structure. Orangutans have extremely low energy usage for a eutherian mammal1, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400k years ago (ya), is more recent than most previous studies and underscores the complexity of the orangutan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (Ne) expanded exponentially relative to the ancestral Ne after the split, while Bornean Ne declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.

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

AbstractThe 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.

Methods for computing the standard errors of branching points in an evolutionary tree and their application to molecular data from humans and apes.

Statistical methods for computing the standard errors of the branching points of an evolutionary tree are developed. These methods are for the unweighted pair-group method-determined (UPGMA) trees reconstructed from molecular data such as amino acid sequences, nucleotide sequences, restriction-sites data, and electrophoretic distances. They were applied to data for the human, chimpanzee, gorilla, orangutan, and gibbon species. Among the four different sets of data used, DNA sequences for an 895-nucleotide segment of mitochondrial DNA (Brown et al. 1982) gave the most reliable tree, whereas electrophoretic data (Bruce and Ayala 1979) gave the least reliable one. The DNA sequence data suggested that the chimpanzee is the closest and that the gorilla is the next closest to the human species. The orangutan and gibbon are more distantly related to man than is the gorilla. This topology of the tree is in agreement with that for the tree obtained from chromosomal studies and DNA-hybridization experiments. However, the difference between the branching point for the human and the chimpanzee species and that for the gorilla species and the human-chimpanzee group is not statistically significant. In addition to this analysis, various factors that affect the accuracy of an estimated tree are discussed.

Phylogeny of NK cell reactivity against human and nonhuman primate lymphoblastoid cell lines: evolving and conserved target antigens.

Both human and nonhuman primate natural killer (NK) cells display little or no killing against allogeneic B lymphoblastoid cell lines. However, the same B cell lines are killed in baboon-human (B alpha H) or human-baboon (H alpha B) xenogeneic combinations. Competition-inhibition experiments indicate that the xenogeneic determinants recognized by NK cells are found principally if not exclusively on B rather than T target cells. Cell lines from closely related chimpanzee or orang-utan species can block some killing of human target cells, but lines from more distantly related species including gibbon, macaque, baboon, and marmoset do not inhibit cytotoxicity. This suggests that some NK target structures are susceptible to evolutionary change. Gibbon or marmoset lines infected with Epstein Barr virus (EBV) do not block killing, suggesting that host rather than viral determinants are being recognized. In contrast to the foregoing pattern, 2 cell lines derived from the same baboon differed in susceptibility to NK lysis irrespective of the effector cell species. The viral producer line 13CB-1 was more susceptible to lysis than its viral nonproducer partner 26CB-1. Thus, some NK target antigens may be highly conserved whereas others evolve with the species.