Reconstructing the demographic history of orang‐utans using Approximate Bayesian Computation

Investigating how different evolutionary forces have shaped patterns of DNA variation within and among species requires detailed knowledge of their demographic history. Orang‐utans, whose distribution is currently restricted to the South‐East Asian islands of Borneo (Pongo pygmaeus) and Sumatra (Pongo abelii), have likely experienced a complex demographic history, influenced by recurrent changes in climate and sea levels, volcanic activities and anthropogenic pressures. Using the most extensive sample set of wild orang‐utans to date, we employed an Approximate Bayesian Computation (ABC) approach to test the fit of 12 different demographic scenarios to the observed patterns of variation in autosomal, X‐chromosomal, mitochondrial and Y‐chromosomal markers. In the best‐fitting model, Sumatran orang‐utans exhibit a deep split of populations north and south of Lake Toba, probably caused by multiple eruptions of the Toba volcano. In addition, we found signals for a strong decline in all Sumatran populations ~24 ka, probably associated with hunting by human colonizers. In contrast, Bornean orang‐utans experienced a severe bottleneck ~135 ka, followed by a population expansion and substructuring starting ~82 ka, which we link to an expansion from a glacial refugium. We showed that orang‐utans went through drastic changes in population size and connectedness, caused by recurrent contraction and expansion of rainforest habitat during Pleistocene glaciations and probably hunting by early humans. Our findings emphasize the fact that important aspects of the evolutionary past of species with complex demographic histories might remain obscured when applying overly simplified models.     

Molecular genetic divergence of orang utan (Pongo pygmaeus) subspecies based on isozyme and two-dimensional gel electrophoresis

The orang utan (Pongo pygmaeus), as currently recognized, includes two geographically separated subspecies: Pongo pygmaeus pygmaeus, which resides on Borneo, and P. p. abelii, which inhabits Sumatra. At present, there is no known route of gene flow between the two populations except through captive individuals which have been released back into the wild over the last several decades. The two subspecies are differentiated by morphological and behavioral characters, and they can be distinguished by a subspecies specific pericentric chromosomal inversion. Nei-genetic distances were estimated between orang utan subspecies, gorilla, chimpanzee and humans using 44 isozyme loci and using 458 soluble fibroblast proteins which were resolved by two-dimensional gel electrophoresis. Phenetic analysis of both data sets supports the following conclusions: the orang utan subspecies distances are approximately 10 times closer to each other than they are to the African apes, and the orang utan subspecies are approximately as divergent as are the two chimpanzee species. Comparison of the genetic distances to genetic distance estimates done in the same laboratory under identical conditions reveals that the distance between Bornean vs. Sumatran orang utans is 5-10 times the distance measured between several pairs of subspecies including lions, cheetahs, and tigers. Near species level molecular genetic distances between orang utan subspecies would support the separate management of Bornean and Sumatran orang utans as evolutionary significant units (Ryder 1987). Evolutionary topologies were constructed from the distance data using both cladistic and phenetic methods. The majority of resulting trees affirmed previous molecular evolutionary studies that indicated that man and chimpanzee diverged from a common ancestor subsequent to the divergence of gorilla from the common ancestor.     

Electrophoretic polymorphism of proteins and the genetic divergence of primates

The hypothesis suggesting that genetic distances between primate taxa are smaller than characteristic genetic distances between non-primate taxa having the similar level of phylogenetic affinity, due to the specific features of primate protein evolution, has been probed. To this end, genetic distances between green and rhesus monkeys representing different genera of one subfamily, and between humans and chimpanzees representing related families, have been calculated and compared. It has been shown that the former are 2-2,5 times smaller than the latter. It is pointed out in this connection that genetic distances reflect adequately the hierarchy of the above taxa, and the existing interpretation of the "paradox of genetic similarity" of man and apes needs to be corrected. To calculate genetic distances, we used both literature data and the results of comparative analysis of 9 electrophoretic gene markers of green and rhesus monkeys represented in this work. Differences in genetic variability of these species were detected.     

Meat-eating behaviour in wild orang utans,Pongo pygmaeus

Meat-eating was observed for the first time among a population of wild orang utans at Gunung Leuser National Park, Sumatra. An adult female who was consorting with an adult male consumed a gibbon (Hylobates lar) carcass. There was no food sharing between the consort pair. The absence of food sharing is interpreted as indicative of the anti-social attitude of adult orang utans.     

An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci

Rhesus macaques (Macaca mulatta) are the most widely used nonhuman primate species in biomedical research. To create new opportunities for genetic and genomic studies using rhesus monkeys, we constructed a genetic linkage map of the rhesus genome. This map consists of 241 microsatellite loci, all previously mapped in the human genome. These polymorphisms were genotyped in five pedigrees of rhesus monkeys totaling 865 animals. The resulting linkage map covers 2048 cM including all 20 rhesus autosomes, with average spacing between markers of 9.3 cM. Average heterozygosity among those markers is 0.73. This linkage map provides new comparative information concerning locus order and interlocus distances in humans and rhesus monkeys. The map will facilitate whole-genome linkage screens to locate quantitative trait loci (QTLs) that influence individual variation in phenotypic traits related to basic primate anatomy, physiology, and behavior, as well as QTLs relevant to risk factors for human disease.     

Classical genetic markers and DNA markers: A commensal marriage

In this paper, we present an overview of classical genetic markers in nonhuman primates and then contrast the discriminatory powers of these markers with DNA markers. We have restricted the scope of our discussion to genetic markers found in blood, since they have been studied most extensively over the past 30 years. For example, immunoglobulin allotypes, complement markers, transferrins, and other protein markers can be identified using serum or plasma. Lymphocytes carry the major histocompatibility complex (MHC) markers, which are very polymorphic in most nonhuman primates. Lymphocytes are also used as a source of DNA. Finally, red blood cells carry an enormous array of blood group as well as isozyme markers. Our discussion will be limited to three species: rhesus monkeys (Macaca mulatta), baboons (Papio hamadryas), and chimpanzees (Pan troglodytes), although the principles are applicable to all nonhuman primates.     

Video-task acquisition in rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes): A comparative analysis

This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.     

非人灵长类动物种质冷冻保存研究进展和展望

非人灵长类动物是生物多样性的重要组成部分,也是生物医学研究的珍贵实验动物,然而,由于人类活动、栖息地破坏、狩猎和遗传隔离等原因,许多非人灵长类动物的野生种群数量急剧下降,甚至处于灭绝的边缘。种质冷冻保存对拯救非人灵长类动物和保存遗传物质资源具有重要意义。本文综述了新大陆猴、旧大陆猴和巨猿等类群动物精子、卵子、胚胎和性腺组织等种质冷冻保存的研究进展,介绍了狨猴、松鼠猴、恒河猴、食蟹猴和黑猩猩等种质冷冻保存的主要方法,并对未来种质冷冻保存的研究方向进行了讨论。     

The timing of spheno‐occipital fusion in hominoids

The degree of spheno‐occipital fusion has been used to assign a relative age to dentally mature hominoid cranial specimens. However, a recent study of captive individuals (Poe: Am J Phys Anthropol 144 (2011) 162–165) concluded that fusion of the spheno‐occipital suture in great ape taxa is of little utility for aging dentally mature individuals. In this contribution, I use dentally mature samples of extant hominoid taxa (Homo sapiens, Pan troglodytes schweinfurthii, Gorilla gorilla gorilla, Pongo pygmaeus pygmaeus and Hylobates lar) to investigate a) the temporal relationship between spheno‐occipital fusion and dental maturity, b) whether there is an association between the degree of spheno‐occipital fusion and relative age, c) whether there are differences in relative timing of spheno‐occipital fusion between taxa, and d) whether there are sex differences in the relative timing of spheno‐occipital fusion. Results suggest that a) a substantial proportion of dentally mature wild‐shot chimpanzee, gorilla and orang‐utans have unfused or partially fused spheno‐occipital synchondoses, b) there is an association between the degree of spheno‐occipital fusion and age, c) there are interspecific differences in the timing of spheno‐occipital fusion, and d) there are significant sex differences in spheno‐occipital fusion in chimpanzees, orang‐utans and gibbons. Thus, contrary to previous work, degree of spheno‐occipital fusion is a potentially useful indicator of relative maturity, especially in great ape taxa. Am J Phys Anthropol 156:135–140, 2015. © 2014 Wiley Periodicals, Inc.     

Dynamics of DNA Methylation in Recent Human and Great Ape Evolution

DNA methylation is an epigenetic modification involved in regulatory processes such as cell differentiation during development, X-chromosome inactivation, genomic imprinting and susceptibility to complex disease. However, the dynamics of DNA methylation changes between humans and their closest relatives are still poorly understood. We performed a comparative analysis of CpG methylation patterns between 9 humans and 23 primate samples including all species of great apes (chimpanzee, bonobo, gorilla and orangutan) using Illumina Methylation450 bead arrays. Our analysis identified ∼800 genes with significantly altered methylation patterns among the great apes, including ∼170 genes with a methylation pattern unique to human. Some of these are known to be involved in developmental and neurological features, suggesting that epigenetic changes have been frequent during recent human and primate evolution. We identified a significant positive relationship between the rate of coding variation and alterations of methylation at the promoter level, indicative of co-occurrence between evolution of protein sequence and gene regulation. In contrast, and supporting the idea that many phenotypic differences between humans and great apes are not due to amino acid differences, our analysis also identified 184 genes that are perfectly conserved at protein level between human and chimpanzee, yet show significant epigenetic differences between these two species. We conclude that epigenetic alterations are an important force during primate evolution and have been under-explored in evolutionary comparative genomics.     

Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda

We present census data for eight primate species spanning 32.9 years along the same transect at Ngogo, Kibale National Park, Uganda, demonstrating major changes in the composition of the primate community. Correlated with an estimated decline of ～89% in the red colobus population was an increase in encounter rates with chimpanzee parties. Our data, along with the unusually high rates of predation by chimpanzees on red colobus at Ngogo and the fact that the chimpanzee community at Ngogo is the largest ever recorded, support the conclusion that the red colobus decline was caused primarily by chimpanzee predation. This seems to be the first documented case of predation by one nonhuman primate causing the population decline in another. We evaluated disease and interspecific competition as other possible causes of the red colobus decline, but judged them to be relatively insignificant compared with predation by chimpanzees. Notable changes in encounter rates with other primate species may have resulted from forest expansion. Those for mangabeys, redtails, and black and white colobus increased significantly. Encounter rates increased for l'Hoest's monkeys too, but the increased sightings may have been an artifact of increased habituation. Sightings of blue monkey and baboon groups declined. There was no significant change in encounter rates for all species combined. The Ngogo primate community seemed to be in a nonequilibrium state, changing from one dominated by two species, a folivore (red colobus) and a frugivorous omnivore (redtails), to one dominated by three species of frugivorous omnivores (redtails, mangabeys, and chimpanzees). This study demonstrates the importance of long-term monitoring in understanding population dynamics and the role of intrinsic variables in shaping the species composition of a community.     

Copy Number Variation of CCL3-like Genes Affects Rate of Progression to Simian-AIDS in Rhesus Macaques (Macaca mulatta)

Variation in genes underlying host immunity can lead to marked differences in susceptibility to HIV infection among humans. Despite heavy reliance on non-human primates as models for HIV/AIDS, little is known about which host factors are shared and which are unique to a given primate lineage. Here, we investigate whether copy number variation (CNV) at CCL3-like genes (CCL3L), a key genetic host factor for HIV/AIDS susceptibility and cell-mediated immune response in humans, is also a determinant of time until onset of simian-AIDS in rhesus macaques. Using a retrospective study of 57 rhesus macaques experimentally infected with SIVmac, we find that CCL3L CNV explains approximately 18% of the variance in time to simian-AIDS (p<0.001) with lower CCL3L copy number associating with more rapid disease course. We also find that CCL3L copy number varies significantly (p<10⁻⁶) among rhesus subpopulations, with Indian-origin macaques having, on average, half as many CCL3L gene copies as Chinese-origin macaques. Lastly, we confirm that CCL3L shows variable copy number in humans and chimpanzees and report on CCL3L CNV within and among three additional primate species. On the basis of our findings we suggest that (1) the difference in population level copy number may explain previously reported observations of longer post-infection survivorship of Chinese-origin rhesus macaques, (2) stratification by CCL3L copy number in rhesus SIV vaccine trials will increase power and reduce noise due to non-vaccine-related differences in survival, and (3) CCL3L CNV is an ancestral component of the primate immune response and, therefore, copy number variation has not been driven by HIV or SIV per se.     

Evolution of alpha 2-fucosyltransferase genes in primates: relation between an intronic Alu-Y element and red cell expression of ABH antigens

Coding sequences of the paralogous FUT1 (H), FUT2 (Se), and Sec1 alpha 2-fucosyltransferase genes were obtained from different primate species. Analysis of the primate FUT1-like and FUT2-like sequences revealed the absence of the known human inactivating mutations giving rise to the h null alleles of FUT1 and the se null alleles of FUT2. Therefore, most primate FUT1-like and FUT2-like genes potentially code for functional enzymes. The Sec1-like gene encodes for a potentially functional alpha 2-fucosyltransferase enzyme in nonprimate mammals, New World monkeys, and Old World monkeys, but it has been inactivated by a nonsense mutation at codon 325 in the ancestor of humans and African apes (gorillas, chimpanzees). Human and gorilla Sec1's have, in addition, two deletions and one insertion, respectively, 5' of the nonsense mutation leading to proteins shorter than chimpanzee Sec1. Phylogenetic analysis of the available H, Se, and Sec1 mammalian protein sequences demonstrates the existence of three clusters which correspond to the three genes. This suggests that the differentiation of the three genes is rather old and predates the great mammalian radiation. The phylogenetic analysis also suggests that Sec1 has a higher evolutionary rate than FUT2 and FUT1. Finally, we show that an Alu-Y element was inserted in intron 1 of the FUT1 ancestor of humans and apes (chimpanzees, gorillas, orangutans, and gibbons); this Alu-Y element has not been found in monkeys or nonprimate mammals, which lack ABH antigens on red cells. A potential mechanism leading to the red cell expression of the H enzyme in primates, related to the insertion of this Alu-Y sequence, is proposed.     

Avoiding Predators: Expectations and Evidence in Primate Antipredator Behavior

Predation and antipredator behavior are important but poorly studied influences on the evolution of primate societies. I review recent evidence of predation and antipredator strategies among primates. I describe patterns of antipredator behavior and attempt to explain the variation among primate taxa and among antipredator strategies. I use predation by chimpanzees on red colobus and antipredator strategies by the colobus as a case study of how a primate prey species may respond to the threat of predation.     

Alpha1,4-fucosyltransferase activity: a significant function in the primate lineage has appeared twice independently

In the animal kingdom the enzymes that catalyze the formation of alpha1,4 fucosylated-glycoconjugates are known only in apes (chimpanzee) and humans. They are encoded by FUT3 and FUT5 genes, two members of the Lewis FUT5-FUT3-FUT6 gene cluster, which had originated by duplications of an alpha3 ancestor gene. In order to explore more precisely the emergence of the alpha1,4 fucosylation, new Lewis-like fucosyltransferase genes were studied in species belonging to the three main primate groups. Two Lewis-like genes were found in brown and ruffed lemurs (prosimians) as well as in squirrel monkey (New World monkey). In the latter, one gene encodes an enzyme which transfers fucose only in alpha1,3 linkage, whereas the other is a pseudogene. Three genes homologous to chimpanzee and human Lewis genes were identified in rhesus macaque (Old World monkey), and only one encodes an alpha3/4-fucosyltransferase. The ability of new primate enzymes to transfer fucose in alpha1,3 or alpha1,3/4 linkage confirms that the amino acid R or W in the acceptor-binding motif "HH(R/W)(D/E)" is required for the type 1/type 2 acceptor specificity. Expression of rhesus macaque genes proved that fucose transfer in alpha1,4 linkage is not restricted to the hominoid family and may be extended to other Old World monkeys. Moreover, the presence of only one enzyme supporting the alpha1,4 fucosylation in rhesus macaque versus two enzymes in hominoids suggests that this function occurred twice independently during primate evolution.     

Flow cytometric analysis on reactivity of human T lymphocyte-specific and cytokine-receptor-specific antibodies with peripheral blood mononuclear cells of chimpanzee (Pan troglodytes), rhesus macaque (Macaca mulatta), and squirrel monkey (Saimiri sciureus)

Abstract: There are relatively few monoclonal antibodies (mAb) that have been characterized for their applicability in studies on the immune system of various nonhuman primates. In the present study, we identified a large number of mAb that can be used in future immunological studies in three different nonhuman primates, i.e., chimpanzees, rhesus macaques, and squirrel monkeys. The reactivity of 161 anti-human mAb to T-cell antigens and cytokine receptors were tested on peripheral blood mononuclear cells (PBMC) from the three primate species by flow cytometric analysis. A total of 105 (65%), 73 (45%), and 68 (42%) antibodies reacted with PBMC from chimpanzees, rhesus macaques, and squirrel monkeys, respectively. Out of the 161 mAb, 38 reacted with all three species and 112 reacted with one or two of the species. No specific reaction was observed with mAb to receptors to GM-CSF, 4–1BB, FLT3, FLX2, common β-chain, IL-1 (type I receptor), and IL-8.     

Densities of Bornean orang‐utans (Pongo pygmaeus morio) in heavily degraded forest and oil palm plantations in Sabah,Borneo

The conversion of forest to agriculture continues to contribute to the loss and fragmentation of remaining orang‐utan habitat. There are still few published estimates of orang‐utan densities in these heavily modified agricultural areas to inform range‐wide population assessments and conservation strategies. In addition, little is known about what landscape features promote orang‐utan habitat use. Using indirect nest count methods, we implemented surveys and estimated population densities of the Northeast Bornean orang‐utan (Pongo pygmaeus morio) across the continuous logged forest and forest remnants in a recently salvage‐logged area and oil palm plantations in Sabah, Malaysian Borneo. We then assessed the influence of landscape features and forest structural metrics obtained from LiDAR data on estimates of orang‐utan density. Recent salvage logging appeared to have a little short‐term effect on orang‐utan density (2.35 ind/km ²), which remained similar to recovering logged forest nearby (2.32 ind/km ²). Orang‐utans were also present in remnant forest patches in oil palm plantations, but at significantly lower numbers (0.82 ind/km ²) than nearby logged forest and salvage‐logged areas. Densities were strongly influenced by variation in canopy height but were not associated with other potential covariates. Our findings suggest that orang‐utans currently exist, at least in the short‐term, within human‐modified landscapes, providing that remnant forest patches remain. We urge greater recognition of the role that these degraded habitats can have in supporting orang‐utan populations, and that future range‐wide analyses and conservation strategies better incorporate data from human‐modified landscapes.