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Comparative primate genomics: the year of the chimpanzee.

This is the year of the chimpanzee genome. Chimpanzee chromosome 22 has been sequenced and soon will be followed by the whole genome, and thousands of chimpanzee cDNA sequences are available for comparative analysis. Not only does this genomic information allow us to identify human-specific changes in particular genes that are potentially under selection, but also to understand molecular evolutionary dynamics characterizing the two most closely related mammalian genomes sequenced so far. Studies comparing gene expression in chimpanzees and other closely related primates reveal significant species differences in brain, liver and fibroblasts. New empirical data, in combination with models of speciation, are giving insight into how humans and chimpanzees speciated.

Animals↗

Identification of novel chimpanzee MHC class I and II alleles using an improved sequence-based typing strategy.

The chimpanzee (Pan troglodytes) is a valuable model for the study of infection with hepatitis C virus and hepatitis B virus, to which only humans and chimpanzees are susceptible. Because the cellular immune response plays a crucial role in host defense against these viruses, the analysis of major histocompatibility complex (MHC) (Patr) class I and II allele diversity in chimpanzees is essential for immune response analysis and vaccine development. In the present study, we report a novel, rapid, and sensitive sequence-based typing strategy to identify polymorphisms of the principal Patr class I (Patr-A and Patr-B) and Patr class II (Patr-DQB1 and Patr-DRB1) alleles. Using this method we identified seven novel Patr alleles in 17 chimpanzees, one of them present in 3 chimpanzees. Furthermore, we detected heterozygosity more rapidly and with higher sensitivity than was done with previous techniques that were based on reverse transcription and amplification of messenger RNA followed by molecular cloning and sequencing.

Alleles↗

The potential significance of adaptive evolution and dimerization in chimpanzee intercellular cell adhesion molecules (ICAMs).

Cell adhesion molecules are involved in a diverse array of cellular processes. Recent data suggests that human immunodeficiency virus (HIV-1) co-opts their functions, in particular the properties of the intercellular cell adhesion molecules (ICAMs), to enhance viral infection and transmission. To investigate mechanisms that may underlie the non-progression that occurs in immunodeficiency virus-infected chimpanzees, we amplified the protein coding regions of multiple non-human primate ICAMs 1-5 and two ICAM ligands, leukocyte function-associated antigen-1 (LFA-1) and macrophage antigen 1 (Mac-1). We then employed a phylogenetic tree-based approach to comparative genomics, in order to screen for the presence of adaptive changes. Strong Darwinian positive selection in chimpanzee ICAMs 1, 2 and 3 was observed, most markedly in domains that are critical for the integrity and maintenance of ICAM-1 dimerization. As binding of ligands, including the attachment of virions, is influenced by the state of ICAM 1 dimerization, chimpanzee ICAMs may have evolved to modulate their own dimerization. In concert with previous evidence suggesting an ancient retroviral pandemic as a prominent selective force in chimpanzee evolution, adaptation of chimpanzee ICAMs may have effected a mechanism that explains the lack of immunosuppression observed following HIV-1 or simian immunodeficiency virus (SIVcpz) infection.

Amino Acid Sequence↗

Molecular evidence for the infection of zoo chimpanzees by pig Ascaris.

We here describe the transmission of the pig roundworm, Ascaris suum to chimpanzees maintained in the Copenhagen Zoo, Denmark. Using a technique for whole genome fingerprinting, amplified fragment length polymorphism (AFLP) and the technique PCR restricted fragment length polymorphism (PCR-RFLP) of the internal transcribed spacer region (ITS) of the nuclear ribosomal DNA, the worms from the chimpanzees were compared with Ascaris spp obtained from humans and pigs in order to identify the source of the infection. By the use of different distance and clustering based methods on the AFLP data set the worms from the chimpanzees were assigned to the same cluster as that of the worms from pigs. The PCR-RFLP analysis supported the AFLP results. Therefore, the zoo chimpanzees have required Ascaris infections by cross-infection from pigs. Pigs as a potential source of Ascaris infections for both captive and wild chimpanzees and other animals, therefore needs to be considered and appropriate steps taken to prevent such infection.

Animals↗

Taste in chimpanzee: I. The summated response to sweeteners and the effect of gymnemic acid.

The purpose of this study was to investigate further with electrophysiological and behavioral techniques the similarity between the sense of taste of humans and chimpanzees, especially with regard to the effects of gymnemic acid. Gymnemic acid (GA) is a powerful suppressor of sweet taste in humans but lacks this ability in nonprimates and lower primates. The summated taste responses from the chorda tympani nerve were recorded in nine adult chimpanzees, Pan troglodytes. The results show that all tested compounds that taste to humans elicited nerve responses in chimpanzees. GA suppressed or abolished the response to all sweeteners, but had no effects on the responses to the nonsweet compounds. The suppression varied from complete abolishment (aspartame, saccharin), to about 50% reduction (xylitol). When the effect of GA was tested on concentration series, 20% remained of the response to sucrose, whereas the responses to aspartame and saccharin were basically abolished. Higher concentrations of GA suppressed more. The effects of GA developed also in the presence of saccharin, but seemed less pronounced. The behavioral results were obtained with a one-bottle preference technique before and after GA. The results demonstrated that after exposure of the tongue to GA, the animals' liking for sweet diminished. These results parallel psychophysical and electrophysiological findings in humans. The way GA suppressed sweet taste in chimpanzees added one more characteristic to those that set chimpanzees apart from monkeys and close to humans.

Animals↗

Transmission of non-A, non-B hepatitis from man to chimpanzee.

Non-A, non-B hepatitis was transmitted to four colony-born chimpanzees by intravenous inoculation of human sera. Two chimpanzees were inoculated with serum from a patient with a clinical and serological diagnosis of chronic non-A, non-B hepatitis whose blood appeared to transmit this disease to a nurse following accidental needle-stick, and the other two chimpanzees were inoculated with serum from either of two former blood-donors whose HBsAg-negative blood appeared to transmit clinically recognisable hepatitis, and who were found to have raised serum-aminotransferase levels 1 1/2 and 5 years later. Serum-aminotransferase levels rose in all four chimpanzees, beginning 2--4 weeks after inoculation: peak alanine-aminotransferase values were 210 to 328 I.U./l. Evidence of hepatitis was present in liver biopsy specimens from all four chimpanzees, beginning 8--10 weeks after inoculation. None showed serological evidence of infection with hepatitis A virus, hepatitis B virus, cytomegalovirus, or Epstein-Barr virus.

Alanine Transaminase↗

Comparison of amino acid sequences in hypervariable region-1 of hepatitis C virus clones between human inocula and the infected chimpanzee sera.

We analyzed nucleic and amino acid sequences of the hypervariable region (HVR)-1 of the hepatitis C virus (HCV) from inocula and the infected chimpanzee sera. One milliliter each of 10(-5), 10(-3) and 10(-2) dilutions of serum no. 4, and those of 10(-4), 10(-5) and 10(-6) dilutions of serum no. 6 were inoculated to six different chimpanzees. Both inocula nos. 4 and 6 contained 10(7) copies of HCV RNA/ml. The two chimpanzees inoculated with 10(-4) and 10(-5) dilutions of no. 6 were infective, while none of the dilutions from inoculum no. 4 were infective. Our results indicated that HCV RNA titer in sera did not correlate with in vivo infectivity. RNA from both inocula and the infected chimpanzee sera were extracted and transcribed to cDNA. The PCR products amplifying the HCV HVR-1 were incorporated into a vector, followed by transformation. Twenty colonies were picked up randomly from each sample. DNA was extracted and the DNA and amino acid sequences were determined. Genetic variations of 20 clones from inoculum no. 6 were divided into six groups, whereas, 40 clones from infected chimpanzees were completely identical to the major quasispecies of inoculum no. 6 in amino acid sequences. The study suggested that the major quasispecies in the diluted inocula were transmitted and replicated.

Amino Acid Sequence↗

The live attenuated subgroup B respiratory syncytial virus vaccine candidate RSV 2B33F is attenuated and immunogenic in chimpanzees, but exhibits partial loss of the ts phenotype following replication in vivo.

The cold-adapted (ca), temperature-sensitive (ts) respiratory syncytial virus (RSV) subgroup B vaccine candidate, designated RSV 2B33F, was found previously to be restricted in replication, immunogenic, and protective against wild-type (wt) virus challenge in rodents and African green monkeys. We sought to investigate the level of attenuation, immunogenicity and genetic stability of this vaccine candidate in seronegative chimpanzees. The 2B33F vaccine candidate was attenuated in chimpanzees and manifested a ten- and 1000-fold restriction in replication in the upper and lower respiratory tracts respectively, compared with its wt RSV 2B parent virus. Despite this attenuation, chimpanzees immunized with RSV 2B33F were completely resistant to respiratory tract disease and virus replication upon challenge with wt virus. The ts phenotype of the RSV 2B33F mutant exhibited some alteration during replication in vivo in three of four chimpanzees tested. Virus present in nasopharyngeal swab or tracheal lavage secretions of these three chimpanzees was biologically cloned by plaque passage in Vero cells at permissive temperature. The plaque progeny retained the ts phenotype, but uniformly produced plaques at 39 and 40 degrees C to a level intermediate between that of the 2B33F input virus and the 2B wt parent virus, indicating that partial loss of the level of temperature sensitivity occurred following replication in vivo. The implications of these findings for RSV vaccine development are discussed.

Animals↗

Gene diversity of chimpanzee ABO blood group genes elucidated from exon 7 sequences.

Human and non-human primate ABO blood group genes show relatively large numbers of nucleotide differences. In this study, we determined exon 7 sequences for 10 individuals of common chimpanzee and for four individuals of bonobo to estimate nucleotide diversities among them. Sequence data showed the existence of chimpanzee specific 9-base deletion in the beginning of the exon 7 coding region. From a phylogenetic network of exon 7 sequences of ABO blood group genes for human, common chimpanzee, bonobo and gorilla, effects of parallel substitutions and/or some kinds of convergent events are inferred in the chimpanzee lineage. We also estimated nucleotide diversities for common chimpanzee and bonobo ABO blood group genes, and these values were 0.4% and 0.2%, respectively. These values are higher than that of most human genes.

ABO Blood-Group System↗

Comparative ontogeny in humans and chimpanzees: similarities, differences and paradoxes in postnatal growth and development of the skull.

The hypothesis of retarded development is a classic and controversial issue in human evolution. It depends directly on the understanding of ontogenetic trajectories and their basic constituents: timing, rate and associated patterns of maturation. In the present study, we applied geometric morphometrics to investigate postnatal ontogeny in human and chimpanzee skulls (N = 302). We evaluated postnatal ontogenetic rates, based on comparisons of properties of size and shape in adults. At different dental ages the percentage of the adult mean size (growth) and adult mean shape (development) was used to quantify patterns of maturation. We found significantly higher levels of ontogenetic maturity in humans than chimpanzees during pre-M1 and M1 eruption. However, during this ontogenetic period the human increments were lower than those of chimpanzees suggesting lower rates. During and after M2-eruption species did not differ in their ontogenetic trajectories. The results indicate that higher prenatal and lower peri- and postnatal maturation rates characterize human ontogeny when compared with chimpanzees. If mandibular ontogeny is considered alone, a paradox was found. Whereas growth maturation proceeded in an expected trajectory continuously approximating 100% adult mean size, developmental maturity was different. After M1-eruption in both species the morphological distance, which had increased before, became reduced again, and reached adult mean shape in a second developmental peak. Such a tendency was found in humans and chimpanzees. This indicates that both size and shape maturation must be considered to understand the complexity of postnatal mandibular ontogeny.

Adolescent↗

Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures.

This study describes the use of referential gestures with concomitant gaze orienting behavior to both distal food objects and communicative interactants by 115 chimpanzees, ranging from 3 to 56 years of age. Gaze alternation between a banana and an experimenter was significantly associated with vocal and gestural communication. Pointing was the most common gesture elicited; 47 subjects pointed with the whole hand, whereas 6 subjects pointed with index fingers. Thus, communicative pointing is commonly used by laboratory chimpanzees, without explicit training to point, language training, or home rearing. Juveniles exhibited striking decrements in their propensity to communicate with adult male experimenters compared with older chimpanzees. Significantly fewer mother-reared chimpanzees exhibited gaze alternation compared with nursery-reared chimpanzees.

Animal Communication↗

Conspecific recognition in the chimpanzee (Pan troglodytes): cardiac responses to significant others.

The ability of a chimpanzee (Pan troglodytes) to recognize photographs of conspecifics was evaluated with heart-rate measures. Heart rate was recorded before, during, and after viewing photographs of an aggressive chimpanzee, a friendly companion animal, and an unfamiliar chimpanzee. The subject displayed a differential pattern of heart-rate response to the stimulus animals, without prior experience with the photographs. Responses to the aggressive animal were acceleratory, which suggests a defensive response. Respiratory sinus arrhythmia suggested that this response was associated with sympathetic activation. In contrast, responses to the familiar animal were minimal, whereas cardiac deceleration was observed in response to the strange chimp, which likely reflects an orienting response. Results suggest the chimpanzee is able to recognize photographs of individual conspecifics and that heart-rate change can reflect the nature of established social relationships between chimpanzees.

Animals↗

Lateral bias in infant chimpanzees (Pan troglodytes).

This study documents the presence, strength, and direction of lateralization in chimpanzees (Pan troglodytes) over the first 3 months of life. Nursery-reared chimpanzees (7 males and 5 females) were repeatedly assessed on a behavioral scale. Lateral bias was measured for 4 behaviors: hand-to-mouth, hand-to-hand, defensive grasp, and first step. Hand-to-mouth was significantly lateralized for the sample. Eight of the 10 chimpanzees that showed hand-to-mouth used the right hand. Lateral bias for defensive grasp was positively related to lateral bias both of first step and of hand-to-mouth. Lateral bias in hand-to-mouth was inversely related to lateral bias in hand-to-hand. Strength of lateralization increased as chimpanzees matured. These laterality effects in infant chimpanzees were expressed under conditions of emotional arousal. Moreover, degree of laterality may be a predictor of responsivity to stress.

Animals↗

Development of self-recognition in chimpanzees (Pan troglodytes).

Chimpanzees (Pan troglodytes) demonstrate the ability to recognize themselves in mirrors, yet investigations of the development of self-recognition in chimpanzees are sparse. Twelve young chimpanzees, grouped by age, were given mirror exposure and tested for self-recognition and contingent movement. All 6 juveniles, 4 and 5 years old, exhibited mirror-guided, mark-directed behavior and clear evidence of self-recognition. In contrast, among the infants, only the oldest group of 2 1/2-year-olds exhibited clear evidence of self-recognition. All chimpanzees exhibited both self-directed behaviors and contingent movements. These results suggest that self-recognition occurs at a slightly older age in chimpanzees than in human infants. In humans, self-recognition is linked with other cognitive abilities. The results conform to the general pattern that great apes exhibit many cognitive skills comparable to those of 2-year-old humans.

Affect↗

Absence of knowledge attribution and self-recognition in young chimpanzees (Pan troglodytes).

Mirror self-recognition in chimpanzees (Pan troglodytes) is typically delayed until 4 1/2-8 years of age. Also, species capable of mirror self-recognition may be capable of some forms of mental state attribution related to intentions and knowledge. Previous investigations of knowledge attribution by chimpanzees used adolescents and adults but did not explicitly test for self-recognition. We report an investigation of knowledge attribution in 6 young chimpanzees previously tested for self-recognition. Subjects were required to discriminate between a person who had seen where food was hidden and another person who had not. The results are consistent with the proposition that most chimpanzees younger than 4 1/2 years of age show neither mirror self-recognition nor knowledge attribution. The results are also consistent with the idea that, just as in humans, development of self-recognition in chimpanzees may precede development of knowledge attribution.

Aging↗

Spontaneous classification in action by a human-enculturated and language-reared bonobo (Pan paniscus) and common chimpanzees (Pan troglodytes).

The authors investigated the formal features of spontaneous manipulations used by 1 bonobo (Pan paniscus) and 2 common chimpanzees (Pan troglodytes) to classify objects in action. Chimpanzees' manipulations were evenly split between serial, one-at-a-time acts on 1 object and parallel, two-at-a-time acts on 2 or 3 objects. Chimpanzees systematically combined their manipulations into routines to generate class-consistent categories of objects. Their routines featured much reproduction of the same manipulations, planful acts that anticipated follow-up manipulations, and manipulations that were reciprocal to each other to accomplish an end. In all these respects, chimpanzees' manipulations were similar to those of 2-year-old human infants. In others they differed. Chimpanzees' routines were mainly based on a linear integration of manipulations. Classifying in action was only infrequently produced by hierarchically integrated routines.

Acculturation↗

Scale-model comprehension by chimpanzees (Pan troglodytes).

The ability of chimpanzees (Pan troglodytes) to recognize the correspondence between a scale model and its real-world referent was examined. In Experiments 1 and 2, an adult female and a young adult male watched as an experimenter hid a miniature model food in 1 of 4 sites in a scale model. Then, the chimpanzees were given the opportunity to find the real food item that had been hidden in the analogous location in the real room. The female performed significantly above chance, whereas the male performed at chance level. Experiments 3 and 4 tested 5 adult and 2 adolescent chimpanzees in a similar paradigm, using a scale model of the chimpanzees' outdoor area. Results indicate that some adult chimpanzees were able to reliably demonstrate an understanding of the relationship between a scale model and the larger space it represented, whereas other subjects were constrained by inefficient and unsuccessful search patterns.

Animals↗

Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta).

Faces are one of the most salient classes of stimuli involved in social communication. Three experiments compared face-recognition abilities in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). In the face-matching task, the chimpanzees matched identical photographs of conspecifics' faces on Trial 1, and the rhesus monkeys did the same after 4 generalization trials. In the individual-recognition task, the chimpanzees matched 2 different photographs of the same individual after 2 trials, and the rhesus monkeys generalized in fewer than 6 trials. The feature-masking task showed that the eyes were the most important cue for individual recognition. Thus, chimpanzees and rhesus monkeys are able to use facial cues to discriminate unfamiliar conspecifics. Although the rhesus monkeys required many trials to learn the tasks, this is not evidence that faces are not as important social stimuli for them as for the chimpanzees.

Animals↗