Pan Troglodytes Troglodytes Research Articles

Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon

Homo faber was once proposed as a label for humans specifically to highlight their unique propensity for tool use. However, new observations on complex tool use by the chimpanzees of Loango National Park, Gabon, expand our knowledge about tool-using abilities in Pan troglodytes. Chimpanzees in Loango, when using tools to extract honey from three types of bee nests, were observed to regularly use three- to five-element tool sets. In other words, different types of tools were used sequentially to access a single food source. Such tool sets included multi-function tools that present typical wear for two distinct uses. In addition, chimpanzees exploited underground bee nests and used ground-perforating tools to locate nest chambers that were not visible from the ground surface. These new observations concur with others from Central African chimpanzees to highlight the importance of honey extraction in arguments favoring the emergence of complex tool use in hominoids, including different tool types, expanded tool sets, multifunction tools, and the exploitation of underground resources. This last technique requires sophisticated cognitive abilities concerning unseen objects. A sequential analysis reveals a higher level of complexity in honey extraction than previously proposed for nut cracking or hunting tools, and compares with some technologies attributed to early hominins from the Early and Middle Stone Age. A better understanding of similarities in human and chimpanzee tool use will allow for a greater understanding of tool-using skills that are uniquely human.

Estimation of African apes’ body size from postcranial dimensions

We examine how African apes' postcranial skeletal dimensions and their combinations are related to body size, as represented by trunk volume, within sex-specific samples of a total of 39 central chimpanzees (Pan troglodytes troglodytes) and 34 western gorillas (Gorilla gorilla gorilla). We examine this relationship by determining the strength of the correlation between selected skeletal dimensions and trunk volume. The findings indicate that sex should be taken into account when possible. Most two-predictor models perform better than most single-predictor models. Interspecific regressions based on log-transformed variables and sex/species-specific regression based on raw variables perform about equally well.

Origin and biology of simian immunodeficiency virus in wild-living western gorillas.

Western lowland gorillas (Gorilla gorilla gorilla) are infected with a simian immunodeficiency virus (SIVgor) that is closely related to chimpanzee and human immunodeficiency viruses (SIVcpz and HIV-1, respectively) in west central Africa. Although existing data suggest a chimpanzee origin for SIVgor, a paucity of available sequences has precluded definitive conclusions. Here, we report the molecular characterization of one partial (BQ664) and three full-length (CP684, CP2135, and CP2139) SIVgor genomes amplified from fecal RNAs of wild-living gorillas at two field sites in Cameroon. Phylogenetic analyses showed that all SIVgor strains clustered together, forming a monophyletic lineage throughout their genomes. Interestingly, the closest relatives of SIVgor were not SIVcpzPtt strains from west central African chimpanzees (Pan troglodytes troglodytes) but human viruses belonging to HIV-1 group O. In trees derived from most genomic regions, SIVgor and HIV-1 group O formed a sister clade to the SIVcpzPtt lineage. However, in a tree derived from 5' pol sequences ( approximately 900 bp), SIVgor and HIV-1 group O fell within the SIVcpzPtt radiation. The latter was due to two SIVcpzPtt strains that contained mosaic pol sequences, pointing to the existence of a divergent SIVcpzPtt lineage that gave rise to SIVgor and HIV-1 group O. Gorillas appear to have acquired this lineage at least 100 to 200 years ago. To examine the biological properties of SIVgor, we synthesized a full-length provirus from fecal consensus sequences. Transfection of the resulting clone (CP2139.287) into 293T cells yielded infectious virus that replicated efficiently in both human and chimpanzee CD4(+) T cells and used CCR5 as the coreceptor for viral entry. Together, these results provide strong evidence that P. t. troglodytes apes were the source of SIVgor. These same apes may also have spawned the group O epidemic; however, the possibility that gorillas served as an intermediary host cannot be excluded.

Increased constraints on MC4R during primate and human evolution.

The melanocortin 4 receptor (MC4R) is routinely investigated for the role it plays in human obesity, as mutations in MC4R are the most common dominantly inherited form of the disease. As little is known about the evolutionary history of this locus, we investigated patterns of variation at MC4R in a worldwide sample of 1,015 humans from 51 populations, and in 8 central chimpanzees. There is a significant paucity of diversity at MC4R in humans, but not in chimpanzees. The spectrum of mutations in humans, combined with the overall low level of diversity, suggests that most (if not all) of the observed non-synonymous polymorphisms are likely to be transient deleterious mutations. The MC4R coding region was resequenced in 12 primate species and sequences from an additional 29 vertebrates were included in molecular evolutionary analyses. MC4R is highly conserved throughout vertebrate evolution, and has apparently been subject to high levels of continuous purifying selection that increased approximately threefold during primate evolution. Furthermore, the strong selection extends to codon usage bias, where most silent mutations are expected to be either quickly fixed or removed from the population, which may help explain the unusually low levels of silent polymorphisms in humans. Finally, there is a significant tendency for non-synonymous mutations that impact MC4R function to occur preferentially at sites that are identified by evolutionary analyses as being subject to very strong purifying selection. The information from this study should help inform future epidemiological investigations of MC4R.

Analysis of Chimpanzee History Based on Genome Sequence Alignments

Population geneticists often study small numbers of carefully chosen loci, but it has become possible to obtain orders of magnitude for more data from overlaps of genome sequences. Here, we generate tens of millions of base pairs of multiple sequence alignments from combinations of three western chimpanzees, three central chimpanzees, an eastern chimpanzee, a bonobo, a human, an orangutan, and a macaque. Analysis provides a more precise understanding of demographic history than was previously available. We show that bonobos and common chimpanzees were separated ∼1,290,000 years ago, western and other common chimpanzees ∼510,000 years ago, and eastern and central chimpanzees at least 50,000 years ago. We infer that the central chimpanzee population size increased by at least a factor of 4 since its separation from western chimpanzees, while the western chimpanzee effective population size decreased. Surprisingly, in about one percent of the genome, the genetic relationships between humans, chimpanzees, and bonobos appear to be different from the species relationships. We used PCR-based resequencing to confirm 11 regions where chimpanzees and bonobos are not most closely related. Study of such loci should provide information about the period of time 5–7 million years ago when the ancestors of humans separated from those of the chimpanzees.

Comparing ape densities and habitats in northern Congo: surveys of sympatric gorillas and chimpanzees in the Odzala and Ndoki regions

The conservation status of western lowland gorillas and central chimpanzees in western equatorial Africa remains largely speculative because many remote areas have never been surveyed and the impact of emergent diseases in the region has not been well documented. In this study, we compared ape densities and habitats in the Lokoué study area in Odzala National Park and the Goualougo Triangle in Nouabalé-Ndoki National Park in northern Republic of Congo. Both of these sites have long been considered strongholds for the conservation of chimpanzees and gorillas, but supposedly differ in vegetative composition and relative ape abundance. We compared habitats between these sites using conventional ground surveys and classified Landsat-7 ETM+ satellite images. We present density estimates via both standing-crop and marked-nest methods for the first time for sympatric apes of the Congo Basin. The marked-nest method was effective in depicting chimpanzee densities, but underestimated gorilla densities at both sites. Marked-nest surveys also revealed a dramatic decline in the ape population of Lokoué which coincided with a local Ebola epidemic. Normal baseline fluctuations in ape nest encounter rates during the repeated passages of marked-nest surveys were clearly distinguishable from a 80% decline in ape nest encounter rates at Lokoué. Our results showed that ape densities, habitat composition, and population dynamics differed between these populations in northern Congo. We emphasize the importance of intensifying monitoring efforts and further refinement of ape survey methods, as our results indicated that even the largest remaining ape populations in intact and protected forests are susceptible to sudden and dramatic declines.

A new approach to estimate parameters of speciation models with application to apes

How populations diverge and give rise to distinct species remains a fundamental question in evolutionary biology, with important implications for a wide range of fields, from conservation genetics to human evolution. A promising approach is to estimate parameters of simple speciation models using polymorphism data from multiple loci. Existing methods, however, make a number of assumptions that severely limit their applicability, notably, no gene flow after the populations split and no intralocus recombination. To overcome these limitations, we developed a new Markov chain Monte Carlo method to estimate parameters of an isolation-migration model. The approach uses summaries of polymorphism data at multiple loci surveyed in a pair of diverging populations or closely related species and, importantly, allows for intralocus recombination. To illustrate its potential, we applied it to extensive polymorphism data from populations and species of apes, whose demographic histories are largely unknown. The isolation-migration model appears to provide a reasonable fit to the data. It suggests that the two chimpanzee species became reproductively isolated in allopatry approximately 850 Kya, while Western and Central chimpanzee populations split approximately 440 Kya but continued to exchange migrants. Similarly, Eastern and Western gorillas and Sumatran and Bornean orangutans appear to have experienced gene flow since their splits approximately 90 and over 250 Kya, respectively.

Genetic diversity and phylogeographic clustering of SIVcpz Ptt in wild chimpanzees in Cameroon

It is now well established that the clade of simian immunodeficiency viruses (SIVs) infecting west central African chimpanzees ( Pan troglodytes troglodytes) and western gorillas ( Gorilla gorilla gorilla) comprises the progenitors of human immunodeficiency virus type 1 (HIV-1). In this study, we have greatly expanded our previous molecular epidemiological survey of SIVcpz in wild chimpanzees in Cameroon. The new results confirm a wide but uneven distribution of SIVcpz Ptt in P. t. troglodytes throughout southern Cameroon and indicate the absence of SIVcpz infection in Pan troglodytes vellerosus. Analyzing 725 fecal samples from 15 field sites, we obtained partial nucleotide sequences from 16 new SIVcpz Ptt strains and determined full-length sequences for two of these. Phylogenetic analyses of these new viruses confirmed the previously reported phylogeographic clustering of SIVcpz Ptt lineages, with viruses related to the ancestors of HIV-1 groups M and N circulating exclusively in southeastern and south central P. t. troglodytes communities, respectively. Importantly, the SIVcpz Ptt strains from the southeastern corner of Cameroon represent a relatively isolated clade indicating a defined geographic origin of the chimpanzee precursor of HIV-1 group M. Since contacts between humans and apes continue, the possibility of ongoing transmissions of SIV from chimpanzees (or gorillas) to humans has to be considered. In this context, our finding of distinct SIVcpz Ptt envelope V3 sequence clades suggests that these peptides may be useful for the serological differentiation of SIVcpz Ptt and HIV-1 infections, and thus the diagnosis of new cross-species transmissions if they occurred.

Snapshots for July 2007

Snapshots for July 2007

Archaeological Analysis Does Not Support Intentionality in the Production of Brushed Ends on Chimpanzee Termiting Tools

Some chimpanzees use 2 types of tools to extract underground termites for consumption. Chimpanzees insert thin, flexible probes into tunnels or holes in termite mounds (fishing), and sometimes use stouter, rigid sticks to first puncture the holes and also possibly to fish. Many puncturing sticks have distinctive “brushed” ends. Researchers have hypothesized that chimpanzees create the brushed ends intentionally to increase their affixibility to biting termites (Sugiyama, 1985). The results of our archaeological analysis of a large collection of puncturing sticks used by Central African chimpanzees falsifies this hypothesis, and instead agrees with the recent behavioral observations of Sanz et al. (2004; cf. Bermejo and Illera, 1999) that brushing is a coincidental result of procuring sticks from vegetation sources. The results highlight the positive contribution of an archaeological approach to problems in chimpanzee material culture and emphasize to primatologists the value of curating artifacts.

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.

Detection and molecular characterization of foamy viruses in Central African chimpanzees of the Pan troglodytes troglodytes and Pan troglodytes vellerosus subspecies

Foamy viruses are exogenous retroviruses that are highly endemic in non-human primates (NHPs). Recent studies, mainly performed in North America, indicated frequent simian foamy virus (SFV) infection in persons occupationally exposed to NHPs. This zoonotic infection was demonstrated mainly after bites by chimpanzees [Pan troglodytes (P. t.)] of the West African P. t. verus subspecies in primatology centers or zoos in the USA. We studied 32 chimpanzees from the Central African subspecies P. t. troglodytes and P. t. vellerosus, originating from Cameroon (29 cases) or Gabon (3 cases). We screened first plasma or sera of the animals with a Western blot detecting the SFVs Gag doublet proteins. Then, we performed two nested polymerase chain reactions (PCRs) amplifying a fragment of the integrase and LTR regions and, finally, we made phylogenetical analyses on the sequences obtained from the integrase PCR products. By serological and/or molecular assays, we detected foamy viruses (FVs) infection in 14 chimpanzees. Sequence comparison and phylogenetic analyses of a 425 bp fragment of the integrase gene obtained for 10 of the 14 positive apes, demonstrated a wide diversity of new FVs strains that belong phylogenetically either to the P. t. troglodytes or P. t. vellerosus foamy viral clade. This study shows that chimpanzees living in these areas of Central Africa are infected by several specific foamy viruses. This raises, in such regions, the potential risk of a human retroviral infection of zoonotic origin linked to chimpanzees contacts, as already exemplified for STLV-1 and SIV infections.

Fine-scale recombination patterns differ between chimpanzees and humans

Recombination rates seem to vary extensively along the human genome. Pedigree analysis suggests that rates vary by an order of magnitude when measured at the megabase scale, and at a finer scale, sperm typing studies point to the existence of recombination hotspots. These are short regions (1-2 kb) in which recombination rates are 10-1,000 times higher than the background rate. Less is known about how recombination rates change over time. Here we determined to what degree recombination rates are conserved among closely related species by estimating recombination rates from 14 Mb of linkage disequilibrium data in central chimpanzee and human populations. The results suggest that recombination hotspots are not conserved between the two species and that recombination rates in larger (50 kb) genomic regions are only weakly conserved. Therefore, the recombination landscape has changed markedly between the two species.

Simian Immunodeficiency Virus Infection in Wild-Caught Chimpanzees from Cameroon

Simian immunodeficiency viruses (SIVcpz) infecting chimpanzees (Pan troglodytes) in west central Africa are the closest relatives to all major variants of human immunodeficiency virus type 1 ([HIV-1]; groups M, N and O), and have thus been implicated as the source of the human infections; however, information concerning the prevalence, geographic distribution, and subspecies association of SIVcpz still remains limited. In this study, we tested 71 wild-caught chimpanzees from Cameroon for evidence of SIVcpz infection. Thirty-nine of these were of the central subspecies (Pan troglodytes troglodytes), and 32 were of the Nigerian subspecies (Pan troglodytes vellerosus), as determined by mitochondrial DNA analysis. Serological analysis determined that one P. t. troglodytes ape (CAM13) harbored serum antibodies that cross-reacted strongly with HIV-1 antigens; all other apes were seronegative. To characterize the newly identified virus, 14 partially overlapping viral fragments were amplified from fecal virion RNA and concatenated to yield a complete SIVcpz genome (9,284 bp). Phylogenetic analyses revealed that SIVcpzCAM13 fell well within the radiation of the SIVcpzPtt group of viruses, as part of a clade including all other SIVcpzPtt strains as well as HIV-1 groups M and N. However, SIVcpzCAM13 clustered most closely with SIVcpzGAB1 from Gabon rather than with SIVcpzCAM3 and SIVcpzCAM5 from Cameroon, indicating the existence of divergent SIVcpzPtt lineages within the same geographic region. These data, together with evidence of recombination among ancestral SIVcpzPtt lineages, indicate long-standing endemic infection of central chimpanzees and reaffirm a west central African origin of HIV-1. Whether P. t. vellerosus apes are naturally infected with SIVcpz requires further study.

Evidence for a complex demographic history of chimpanzees.

To characterize patterns of genomic variation in central chimpanzees (Pan troglodytes troglodytes) and gain insight into their evolution, we sequenced nine unlinked, intergenic regions, representing a total of 19,000 base pairs, in 14 individuals. When these DNA sequences are compared with homologous sequences previously collected in humans and in western chimpanzees (Pan troglodytes verus), nucleotide diversity is higher in central chimpanzees than in western chimpanzees or in humans. Consistent with a larger effective population size of central chimpanzees, levels of linkage disequilibrium are lower than in humans. Patterns of linkage disequilibrium further suggest that homologous gene conversion may be an important contributor to genetic exchange at short distances, in agreement with a previous study of the same DNA sequences in humans. In central chimpanzees, but not in western chimpanzees, the allele frequency spectrum is significantly skewed towards rare alleles, pointing to population size changes or fine-scale population structure. Strikingly, the extent of genetic differentiation between western and central chimpanzees is much stronger than what is seen between human populations. This suggests that careful attention should be paid to geographic sampling in studies of chimpanzee genetic variation.

Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii).

Simian immunodeficiency virus of chimpanzees (SIVcpz) is the immediate precursor to human immunodeficiency virus type 1 (HIV-1), yet remarkably, the distribution and prevalence of SIVcpz in wild ape populations are unknown. Studies of SIVcpz infection rates in wild chimpanzees are complicated by the species' endangered status and by its geographic location in remote areas of sub-Saharan Africa. We have developed sensitive and specific urine and fecal tests for SIVcpz antibody and virion RNA (vRNA) detection and describe herein the first comprehensive prevalence study of SIVcpz infection in five wild Pan troglodytes schweinfurthii communities in east Africa. In Kibale National Park in Uganda, 31 (of 52) members of the Kanyawara community and 39 (of approximately 145) members of the Ngogo community were studied; none were found to be positive for SIVcpz infection. In Gombe National Park in Tanzania, 15 (of 20) members of the Mitumba community, 51 (of 55) members of the Kasekela community, and at least 10 (of approximately 20) members of the Kalande community were studied. Seven individuals were SIVcpz antibody and/or vRNA positive, and two others had indeterminate antibody results. Based on assay sensitivities and the numbers and types of specimens analyzed, we estimated the prevalence of SIVcpz infection to be 17% in Mitumba (95% confidence interval, 10 to 40%), 5% in Kasekela (95% confidence interval, 4 to 7%), and 30% in Kalande (95% confidence interval, 15 to 60%). For Gombe as a whole, the SIVcpz prevalence was estimated to be 13% (95% confidence interval, 7 to 25%). SIVcpz infection was confirmed in five chimpanzees by PCR amplification of partial pol and gp41/nef sequences which revealed a diverse group of viruses that formed a monophyletic lineage within the SIVcpzPts radiation. Although none of the 70 Kibale chimpanzees tested SIVcpz positive, we estimated the likelihood that a 10% or higher prevalence existed but went undetected because of sampling and assay limitations; this possibility was ruled out with 95% certainty. These results indicate that SIVcpz is unevenly distributed among P. t. schweinfurthii in east Africa, with foci or "hot spots" of SIVcpz endemicity in some communities and rare or absent infection in others. This situation contrasts with that for smaller monkey species, in which infection rates by related SIVs are generally much higher and more uniform among different groups and populations. The basis for the wide variability in SIVcpz infection rates in east African apes and the important question of SIVcpz prevalence in west central African chimpanzees (Pan troglodytes troglodytes) remain to be elucidated.

Experimental oral polio vaccines and acquired immune deficiency syndrome.

The simian immunodeficiency virus (SIV) of the common chimpanzee is widely acknowledged as the direct ancestor of HIV-1. There is increasing historical evidence that during the late 1950s, kidneys were routinely excised from central African chimpanzees by scientists who were collaborating with the polio vaccine research of Dr Hilary Koprowski, and sent - inter alia - to vaccine-making laboratories in the USA and Africa, and to unspecified destinations in Belgium. While there is no direct evidence that cells from these kidneys were used as a substrate for growing Dr Koprowski's oral polio vaccines, there is a startling coincidence between places in Africa where his CHAT vaccine was fed, and the first appearances in the world of HIV-1 group M and group-M-related AIDS. Because of the enormous implications of the hypothesis that AIDS may be an unintended iatrogenic (physician-caused) disease, it is almost inevitable that this theory will engender heated opposition from many of those in the scientific establishment, and those with vested interests.