Sample Of Chimpanzees Research Articles

Blood cell telomere lengths and shortening rates of chimpanzee and human females

Slower rates of aging distinguish humans from our nearest living cousins. Chimpanzees rarely survive their forties while large fractions of women are postmenopausal even in high-mortality hunter-gatherer populations. Cellular and molecular mechanisms for these somatic aging differences remain to be identified, though telomeres might play a role. To find out, we compared telomere lengths across age-matched samples of female chimpanzees and women. We used a monochrome multiplex quantitative polymerase chain reaction to assay canonical telomere repeats in blood cells from captive female chimpanzees (65 individuals; age: 6.2-56.7 years) and compared them to the same measure in human females (43 individuals; age: 7.4-57.3 years). Our samples showed little difference in attrition rates between the species (~0.022 T/S per year for chimpanzees and ~0.012 T/S per year for humans with overlapping 95% confidence intervals), but telomeres were twice as long in chimpanzees as in humans (T/S ratios = 2.70 and 1.26, respectively). Based on the longevity differences, we initially hypothesized that telomere shortening rates would be faster in chimpanzees than in humans. Instead, it is shorter telomere length that appears to be the derived state in humans. This comparison indicates that better characterization of physiological aging in our closest living relatives will be indispensable for understanding the evolution of distinctive human longevity.

Poor receptive joint attention skills are associated with atypical gray matter asymmetry in the posterior superior temporal gyrus of chimpanzees (Pan troglodytes).

Clinical and experimental data have implicated the posterior superior temporal gyrus as an important cortical region in the processing of socially relevant stimuli such as gaze following, eye direction, and head orientation. Gaze following and responding to different socio-communicative signals is an important and highly adaptive skill in primates, including humans. Here, we examined whether individual differences in responding to socio-communicative cues was associated with variation in either gray matter (GM) volume and asymmetry in a sample of chimpanzees. Magnetic resonance image scans and behavioral data on receptive joint attention (RJA) was obtained from a sample of 191 chimpanzees. We found that chimpanzees that performed poorly on the RJA task had less GM in the right compared to left hemisphere in the posterior but not anterior superior temporal gyrus. We further found that middle-aged and elderly chimpanzee performed more poorly on the RJA task and had significantly less GM than young-adult and sub-adult chimpanzees. The results are consistent with previous studies implicating the posterior temporal gyrus in the processing of socially relevant information.

A Penile Spine/Vibrissa Enhancer Sequence Is Missing in Modern and Extinct Humans but Is Retained in Multiple Primates with Penile Spines and Sensory Vibrissae

Previous studies show that humans have a large genomic deletion downstream of the Androgen Receptor gene that eliminates an ancestral mammalian regulatory enhancer that drives expression in developing penile spines and sensory vibrissae. Here we use a combination of large-scale sequence analysis and PCR amplification to demonstrate that the penile spine/vibrissa enhancer is missing in all humans surveyed and in the Neandertal and Denisovan genomes, but is present in DNA samples of chimpanzees and bonobos, as well as in multiple other great apes and primates that maintain some form of penile integumentary appendage and facial vibrissae. These results further strengthen the association between the presence of the penile spine/vibrissa enhancer and the presence of penile spines and macro- or micro- vibrissae in non-human primates as well as show that loss of the enhancer is both a distinctive and characteristic feature of the human lineage.

Are Chimpanzees Really So Poor at Understanding Imperative Pointing? Some New Data and an Alternative View of Canine and Ape Social Cognition

There is considerable interest in comparative research on different species’ abilities to respond to human communicative cues such as gaze and pointing. It has been reported that some canines perform significantly better than monkeys and apes on tasks requiring the comprehension of either declarative or imperative pointing and these differences have been attributed to domestication in dogs. Here we tested a sample of chimpanzees on a task requiring comprehension of an imperative request and show that, though there are considerable individual differences, the performance by the apes rival those reported in pet dogs. We suggest that small differences in methodology can have a pronounced influence on performance on these types of tasks. We further suggest that basic differences in subject sampling, subject recruitment and rearing experiences have resulted in a skewed representation of canine abilities compared to those of monkeys and apes.

Differences in the early cognitive development of children and great apes

There is very little research comparing great ape and human cognition developmentally. In the current studies we compared a cross-sectional sample of 2- to 4-year-old human children (n=48) with a large sample of chimpanzees and bonobos in the same age range (n=42, hereafter: apes) on a broad array of cognitive tasks. We then followed a group of juvenile apes (n=44) longitudinally over 3 years to track their cognitive development in greater detail. In skills of physical cognition (space, causality, quantities), children and apes performed comparably at 2 years of age, but by 4 years of age children were more advanced (whereas apes stayed at their 2-year-old performance levels). In skills of social cognition (communication, social learning, theory of mind), children out-performed apes already at 2 years, and increased this difference even more by 4 years. Patterns of development differed more between children and apes in the social domain than the physical domain, with support for these patterns present in both the cross-sectional and longitudinal ape data sets. These results indicate key differences in the pattern and pace of cognitive development between humans and other apes, particularly in the early emergence of specific social cognitive capacities in humans.

A comparison of antemortem tooth loss in human hunter‐gatherers and non‐human catarrhines: Implications for the identification of behavioral evolution in the human fossil record

Middle and Late Pleistocene fossil hominin specimens with severe antemortem tooth loss are often regarded as evidence for the precocious evolution of human-like behaviors, such as conspecific care or cooking, in ancient hominin species. The goal of this project was to ask whether the theoretical association between antemortem tooth loss and uniquely human behaviors is supported empirically in a large skeletal sample of human hunter-gatherers, chimpanzees, orangutans, and baboons. Binomial regression modeling in a Bayesian framework allows for the investigation of the effects of tooth class, genus, age, and sex on the likelihood of tooth loss. The results strongly suggest that modern humans experience more antemortem tooth loss than non-human primates and identify age in years as an important predictor. Once age is accounted for, the difference between the humans and the closest non-human genus (chimpanzees) is less pronounced; humans are still more likely on average to experience antemortem tooth loss though 95% uncertainty envelopes around the average prediction for each genus show some overlap. These analyses support theoretical links between antemortem tooth loss and modern human characteristics; humans' significantly longer life history and a positive correlation between age and antemortem tooth loss explain, in part, the reason why humans are more likely to experience tooth loss than non-human primates, but the results do not exclude behavioral differences as a contributing factor.

Understanding geographic origins and history of admixture among chimpanzees in European zoos, with implications for future breeding programmes

Despite ample focus on this endangered species, conservation planning for chimpanzees residing outside Africa has proven a challenge because of the lack of ancestry information. Here, we analysed the largest number of chimpanzee samples to date, examining microsatellites in >100 chimpanzees from the range of the species in Africa, and 20% of the European zoo population. We applied the knowledge about subspecies differentiation throughout equatorial Africa to assign origin to chimpanzees in the largest conservation management programme globally. A total of 63% of the genotyped chimpanzees from the European zoos could be assigned to one of the recognized subspecies. The majority being of West African origin (40%) will help consolidate the current breeding programme for this subspecies and the identification of individuals belonging to the two other subspecies so far found in European zoos can form the basis for breeding programmes for these. Individuals of various degree of mixed ancestry made up 37% of the genotyped European zoo population and thus highlight the need for appropriate management programmes guided by genetic analysis to preserve maximum genetic diversity and reduce hybridization among subspecies.

The Frequency of CD127 + Hepatitis C Virus (HCV)-Specific T Cells but Not the Expression of Exhaustion Markers Predicts the Outcome of Acute HCV Infection

T cells are exhausted and overexpress inhibitory molecules in chronic hepatitis C virus (HCV) infection. It is unclear whether this is the cause or consequence of HCV persistence. By studying serial blood and liver samples of chimpanzees during acute infection, we demonstrate that the early expression of the memory precursor marker CD127 on HCV-specific T cells, but not the expression of inhibitory molecules on those T cells or their ligands in the liver, predicts the outcome of acute infection.

Evidence for a midlife crisis in great apes consistent with the U-shape in human well-being

Recently, economists and behavioral scientists have studied the pattern of human well-being over the lifespan. In dozens of countries, and for a large range of well-being measures, including happiness and mental health, well-being is high in youth, falls to a nadir in midlife, and rises again in old age. The reasons for this U-shape are still unclear. Present theories emphasize sociological and economic forces. In this study we show that a similar U-shape exists in 508 great apes (two samples of chimpanzees and one sample of orangutans) whose well-being was assessed by raters familiar with the individual apes. This U-shaped pattern or "midlife crisis" emerges with or without use of parametric methods. Our results imply that human well-being's curved shape is not uniquely human and that, although it may be partly explained by aspects of human life and society, its origins may lie partly in the biology we share with great apes. These findings have implications across scientific and social-scientific disciplines, and may help to identify ways of enhancing human and ape well-being.

Quantifying lateral femoral condyle ellipticalness in chimpanzees, gorillas, and humans

Articular surfaces of limb bones provide information for understanding animal locomotion because their size and shape are a reflection of habitual postures and movements. Here we present a novel method for quantifying the ellipticalness (i.e., departure from perfectly circular) of the lateral femoral condyle (LFC), applying this technique to hominid femora. Three-dimensional surface models were created for 49 Homo sapiens, 34 Pan troglodytes and 25 Gorilla gorilla femora. Software was developed that fit separate cylinders to each of the femoral condyles. These cylinders were constrained to have a single axis, but could have different radii. The cylinder fit to the LFC was allowed to assume an elliptical cross-section, while the cylinder fit to the medial condyle was constrained to remain circular. The shape of the elliptical cylinder (ratio of the major and minor axes of the ellipse) was recorded, and the orientation of the elliptical cylinder quantified as angles between the major axis of the ellipse and the anatomical and mechanical axes of the femur. Species were compared using analysis of variance and post hoc multiple comparisons tests. Confirming qualitative descriptions, human LFCs are more elliptical than those of chimpanzees and gorillas. Human femora exhibit a narrow range for the angle between the major axis of the elliptical cylinder and femoral axes. Conversely, the chimpanzee sample is bimodal for these angles, exhibiting two ellipse orientations, while Gorilla shows no preferred angle. Our results suggest that like modern human femora, chimpanzee femoral condyles have preferentially used regions.

High Diversity at PRDM9 in Chimpanzees and Bonobos

BackgroundThe PRDM9 locus in mammals has increasingly attracted research attention due to its role in mediating chromosomal recombination and possible involvement in hybrid sterility and hence speciation processes. The aim of this study was to characterize sequence variation at the PRDM9 locus in a sample of our closest living relatives, the chimpanzees and bonobos.Methodology/Principal FindingsPRDM9 contains a highly variable and repetitive zinc finger array. We amplified this domain using long-range PCR and determined the DNA sequences using conventional Sanger sequencing. From 17 chimpanzees representing three subspecies and five bonobos we obtained a total of 12 alleles differing at the nucleotide level. Based on a data set consisting of our data and recently published Pan PRDM9 sequences, we found that at the subspecies level, diversity levels did not differ among chimpanzee subspecies or between chimpanzee subspecies and bonobos. In contrast, the sample of chimpanzees harbors significantly more diversity at PRDM9 than samples of humans. Pan PRDM9 shows signs of rapid evolution including no alleles or ZnFs in common with humans as well as signals of positive selection in the residues responsible for DNA binding.Conclusions and SignificanceThe high number of alleles specific to the genus Pan, signs of positive selection in the DNA binding residues, and reported lack of conservation of recombination hotspots between chimpanzees and humans suggest that PRDM9 could be active in hotspot recruitment in the genus Pan. Chimpanzees and bonobos are considered separate species and do not have overlapping ranges in the wild, making the presence of shared alleles at the amino acid level between the chimpanzee and bonobo species interesting in view of the hypothesis that PRDM9 plays a universal role in interspecific hybrid sterility.

Endocranial volume of Australopithecus africanus: New CT-based estimates and the effects of missing data and small sample size

Estimation of endocranial volume in Australopithecus africanus is important in interpreting early hominin brain evolution. However, the number of individuals available for investigation is limited and most of these fossils are, to some degree, incomplete and/or distorted. Uncertainties of the required reconstruction (‘missing data uncertainty’) and the small sample size (‘small sample uncertainty’) both potentially bias estimates of the average and within-group variation of endocranial volume in A. africanus.We used CT scans, electronic preparation (segmentation), mirror-imaging and semilandmark-based geometric morphometrics to generate and reconstruct complete endocasts for Sts 5, Sts 60, Sts 71, StW 505, MLD 37/38, and Taung, and measured their endocranial volumes (EV). To get a sense of the reliability of these new EV estimates, we then used simulations based on samples of chimpanzees and humans to: (a) test the accuracy of our approach, (b) assess missing data uncertainty, and (c) appraise small sample uncertainty.Incorporating missing data uncertainty of the five adult individuals, A. africanus was found to have an average adult endocranial volume of 454–461 ml with a standard deviation of 66–75 ml. EV estimates for the juvenile Taung individual range from 402 to 407 ml. Our simulations show that missing data uncertainty is small given the missing portions of the investigated fossils, but that small sample sizes are problematic for estimating species average EV. It is important to take these uncertainties into account when different fossil groups are being compared.

Brief communication: Endocranial volumes in an ontogenetic sample of chimpanzees from the taï forest national park, ivory coast

Ontogenetic samples of endocranial volumes (EVs) from great apes and humans are critical for understanding the evolution of the brain growth pattern in the hominin lineage. However, high quality ontogenetic data are scarce, especially for nonhuman primates. Here, we provide original data derived from an osteological collection of a wild population of Pan troglodytes verus from the Taï Forest National Park, Ivory Coast. This sample is unique, because age, sex, and pedigree information are available for many specimens from behavioral observations in the wild. We scanned crania of all 30 immature specimens and 13 adult individuals using high-resolution computed tomography. We then created virtual casts of the bony braincase (endocasts) to measure EVs. We also measured cranial length, width, and height and attempted to relate cranial distances to EV via regression analysis. Our data are consistent with previous studies. The only neonate in the sample has an EV of 127 cm(3) or 34% of the adult mean. EV increases rapidly during early ontogeny. The average adult EV in this sample is 378.7 ± 30.1 cm(3) . We found sexual dimorphism in adults; males seem to be already larger than females before adult EV is attained. Regressions on cranial width and multiple regression provide better estimates for EV than regressions on cranial length or height. Increasing the sample size and compiling more high quality ontogenetic data of EV will help to reconcile ongoing discussions about the evolution of hominin brain growth.

Detection and Genetic Characterization of Enteroviruses Circulating among Wild Populations of Chimpanzees in Cameroon: Relationship with Human and Simian Enteroviruses

Enteroviruses (EVs), members of the family Picornaviridae, are a genetically and antigenically diverse range of viruses causing acute infections in humans and several Old World monkey (OWM) species. Despite their known wide distribution in primates, nothing is currently known about the occurrence, frequency, and genetic diversity of enteroviruses infecting apes. To investigate this, 27 chimpanzee and 27 gorilla fecal samples collected from undisturbed jungle areas with minimal human contact in Cameroon were screened for EVs. Four chimpanzee samples were positive, but none of the gorilla samples were positive. Genetic characterization of the VP1, VP4, and partial VP2 genes, the 5' untranslated region, and partial 3Dpol sequences enabled chimpanzee-derived EVs to be identified as (i) the species A type, EV76, (ii) a new species D type assigned as EV111, along with a human isolate from the Democratic Republic of Congo previously described by the International Committee on the Taxonomy of Viruses, and (iii) a new species B type (assigned as EV110) most closely related to, although a distinct type from, the SA5 isolate recovered from a vervet monkey. The identification of EVs infecting chimpanzees related to those circulating in human and OWM populations provides evidence for cross-species transmission of EVs between primates. However, the direction of transfer and the existence of primate sources of zoonotic enterovirus infections in humans require further investigation of population exposure and more extensive characterization of EVs circulating in wild ape populations.

Expanding whole exome resequencing into non-human primates

BackgroundComplete exome resequencing has the power to greatly expand our understanding of non-human primate genomes. This includes both a better appreciation of the variation that exists in non-human primate model species, but also an improved annotation of their genomes. By developing an understanding of the variation between individuals, non-human primate models of human disease can be better developed. This effort is hindered largely by the lack of comprehensive information on specific non-human primate genetic variation and the costs of generating these data. If the tools that have been developed in humans for complete exome resequencing can be applied to closely related non-human primate species, then these difficulties can be circumvented.ResultsUsing a human whole exome enrichment technique, chimpanzee and rhesus macaque samples were captured alongside a human sample and sequenced using standard next-generation methodologies. The results from the three species were then compared for efficacy. The chimpanzee sample showed similar coverage levels and distributions following exome capture based on the human genome as the human sample. The rhesus macaque sample showed significant coverage in protein-coding sequence but significantly less in untranslated regions. Both chimpanzee and rhesus macaque showed significant numbers of frameshift mutations compared to self-genomes and suggest a need for further annotation.ConclusionsCurrent whole exome resequencing technologies can successfully be used to identify coding-region variation in non-human primates extending into old world monkeys. In addition to identifying variation, whole exome resequencing can aid in better annotation of non-human primate genomes.

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000

The 3.5-Myr-old hominin cranium KNM-WT 40000 from Lomekwi, west of Lake Turkana, has been assigned to a new hominin genus and species, Kenyanthropus platyops, on the basis of a unique combination of derived facial and primitive neurocranial features. Central to the diagnosis of K. platyops is the morphology of the maxilla, characterized by a flat and relatively orthognathic subnasal region, anteriorly placed zygomatic processes and small molars. To study this morphology in more detail, we compare the maxillae of African Plio-Pleistocene hominin fossils and samples of modern humans, chimpanzees and gorillas, using conventional and geometric morphometric methods. Computed tomography scans and detailed preparation of the KNM-WT 40000 maxilla enable comprehensive assessment of post-mortem changes, so that landmark data characterizing the morphology can be corrected for distortion. Based on a substantially larger comparative sample than previously available, the results of statistical analyses show that KNM-WT 40000 is indeed significantly different from and falls outside the known range of variation of species of Australopithecus and Paranthropus, contemporary Australopithecus afarensis in particular. These results support the attribution of KNM-WT 40000 to a separate species and the notion that hominin taxonomic diversity in Africa extends back well into the Middle Pliocene.

Navigating the unknown: model selection in phylogeography

Despite the widespread use and obvious strengths of model-based methods for phylogeographic study, a persistent concern for such analyses is related to the definition of the model itself. The study by Peter et al. (2010) in this issue of Molecular Ecology demonstrates an approach for overcoming such hurdles. The authors were motivated by a deceptively simple goal; they sought to infer whether a population has remained at a low and stable size or has undergone a decline, and certainly there is no shortage of software packages for such a task (e.g., see list of programs in Excoffier & Heckel 2006). However, each of these software packages makes basic assumptions about the underling population (e.g., is the population subdivided or panmictic); these assumptions are explicit to any model-based approach but can bias parameter estimates and produce misleading inferences if the model does not approximate the actual demographic history in a reasonable manner. Rather than guessing which model might be best for analyzing the data (microsatellite data from samples of chimpanzees), Peter et al. (2010) quantify the relative fit of competing models for estimating the population genetic parameters of interest. Complemented by a revealing simulation study, the authors highlight the peril inherent to model-based inferences that lack a statistical evaluation of the fit of a model to the data, while also demonstrating an approach for model selection with broad applicability to phylogeographic analysis.

Articular to diaphyseal proportions of human and great ape metatarsals

This study proposes a new way to use metatarsals to identify locomotor behavior of fossil hominins. Metatarsal head articular dimensions and diaphyseal strength in a sample of chimpanzees, gorillas, orangutans, and humans (n = 76) are used to explore the relationships of these parameters with different locomotor modes. Results show that ratios between metatarsal head articular proportions and diaphyseal strength of the hallucal and fifth metatarsal discriminate among extant great apes and humans based on their different locomotor modes. In particular, the hallucal and fifth metatarsal characteristics of humans are functionally related to the different ranges of motion and load patterns during stance phase in the forefoot of humans in bipedal locomotion. This method may be applicable to isolated fossil hominin metatarsals to provide new information relevant to debates regarding the evolution of human bipedal locomotion. The second to fourth metatarsals are not useful in distinguishing among hominoids. Further studies should concentrate on measuring other important qualitative and quantitative differences in the shape of the metatarsal head of hominoids that are not reflected in simple geometric reconstructions of the articulation, and gathering more forefoot kinematic data on great apes to better understand differences in range of motion and loading patterns of the metatarsals.

A Pipeline to Determine RT-QPCR Control Genes for Evolutionary Studies: Application to Primate Gene Expression across Multiple Tissues

Because many species-specific phenotypic differences are assumed to be caused by differential regulation of gene expression, many recent investigations have focused on measuring transcript abundance. Despite the availability of high-throughput platforms, quantitative real-time polymerase chain reaction (RT-QPCR) is often the method of choice because of its low cost and wider dynamic range. However, the accuracy of this technique heavily relies on the use of multiple valid control genes for normalization. We created a pipeline for choosing genes potentially useful as RT-QPCR control genes for measuring expression between human and chimpanzee samples across multiple tissues, using published microarrays and a measure of tissue-specificity. We identified 13 genes from the pipeline and from commonly used control genes: ACTB, USP49, ARGHGEF2, GSK3A, TBP, SDHA, EIF2B2, GPDH, YWHAZ, HPTR1, RPL13A, HMBS, and EEF2. We then tested these candidate genes and validated their expression stability across species. We established the rank order of the most preferable set of genes for single and combined tissues. Our results suggest that for at least three tissues (cerebral cortex, liver, and skeletal muscle), EIF2B2, EEF2, HMBS, and SDHA are useful genes for normalizing human and chimpanzee expression using RT-QPCR. Interestingly, other commonly used control genes, including TBP, GAPDH, and, especially ACTB do not perform as well. This pipeline could be easily adapted to other species for which expression data exist, providing taxonomically appropriate control genes for comparisons of gene expression among species.

Pathogenesis of Hepatitis E Virus and Hepatitis C Virus in Chimpanzees: Similarities and Differences

The chimpanzee is the only animal model for investigating the pathogenesis of viral hepatitis types A through E in humans. Studies of the host response, including microarray analyses, have relied on the close relationship between these two primate species: chimpanzee samples are commonly tested with human-based reagents. In this study, the host responses to two dissimilar viruses, hepatitis E virus (HEV) and hepatitis C virus (HCV), were compared in multiple experimentally infected chimpanzees. Affymetrix U133+2.0 human microarray chips were used to assess the entire transcriptome in serial liver biopsies obtained over the course of the infections. Respecting the limitations of microarray probes designed for human target transcripts to effectively assay chimpanzee transcripts, we conducted probe-level analysis of the microarray data in conjunction with a custom mapping of the probe sequences to the most recent human and chimpanzee genome sequences. Time points for statistical comparison were chosen based on independently measured viremia levels. Regardless of the viral infection, the alignment of differentially expressed genes to the human genome sequence resulted in a larger number of genes being identified when compared with alignment to the chimpanzee genome sequence. This probably reflects the lesser refinement of gene annotation for chimpanzees. In general, the two viruses demonstrated very distinct temporal changes in host response genes, although both RNA viruses induced genes that were involved in many of the same biological systems, including interferon-induced genes. The host response to HCV infection was more robust in the magnitude and number of differentially expressed genes compared to HEV infection.