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Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes.

MHC class I polymorphism improves the defense of vertebrate species against viruses and other intracellular pathogens. To see how polymorphism at the same class I genes can evolve in different species we compared the MHC-A, MHC-B, and MHC-C loci of common chimpanzees and humans. Diversity in 23 Patr-A, 32 Patr-B, and 18 Patr-C alleles obtained from study of 48 chimpanzees was compared to diversity in 66 HLA-A, 149 HLA-B, and 41 HLA-C alleles obtained from a study of over 1 million humans. At each locus, alleles group hierarchically into families and then lineages. No alleles or families are shared by the two species, commonality being seen only at the lineage level. The overall nucleotide sequence diversity of MHC class I is estimated to be greater for modern chimpanzees than humans. Considering the numbers of lineages, families, and alleles, Patr-B and Patr-C have greater diversity than the HLA-B and HLA-C, respectively. In contrast, Patr-A has less polymorphism than HLA-A, due to the absence of A2 lineage alleles. The results are consistent with ancestral humans having passed through a narrower population bottleneck than chimpanzees, and with pathogen-mediated selection having favored either preservation of A2 lineage alleles on the human line and/or their extinction on the chimpanzee line.

Alleles↗

Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4.

The centromeric regions of human and primate chromosomes are characterized by diverged subsets of tandemly repeated alpha-satellite DNA. Comparison of the alpha-satellites on known homologous chromosomes in human and chimpanzee provides insight into the very rapid evolution of satellite DNA sequences and the mechanisms that shape complex genomes. By using oligonucleotide primers specific for a conserved region of human alpha-satellite DNA, we have amplified a chromosome-specific alpha-satellite subset from the chimpanzee genome by the polymerase chain reaction. Fluorescence in situ hybridization showed that clones palphaPTR4N and palphaPTR4H are homologous to sequences at the centromere of the chimpanzee chromosome 4. This alpha-satellite subset is organized as a series of pentameric (higher-order) repeats, operationally defined by digestion of genomic DNA with HaeIII, MboI, RsaI, SstI, and XbaI. The lengths of four independent centromeric arrays measured by pulsed-field gel electrophoresis varied between 800 and 3,500 kb (mean = 1,850 kb, SD = 1,000 kb). Nucleotide sequence analysis demonstrated that chimpanzee chromosome 4 alpha-satellite is most closely related to the suprachromosomal subfamily II, which is evolutionarily different from the subfamily I to which the alpha-satellite on the homologous human chromosome 5 belongs. This implies that the human-chimpanzee sequence divergence has not arisen from a common ancestral alpha-satellite repeat(s) but instead represents concerted evolution of distinct repeats on homologous chromosomes.

Animals↗

Strategic navigation of two-dimensional alley mazes: comparing capuchin monkeys and chimpanzees.

Planning is an important component of cognition that contributes, for example, to efficient movement through space. In the current study we presented novel two-dimensional alley mazes to four chimpanzees and three capuchin monkeys to identify the nature and efficiency of planning in relation to varying task parameters. All the subjects solved more mazes without error than expected by chance, providing compelling evidence that both species planned their choices in some manner. The probability of making a correct choice on mazes designed to be more demanding and presented later in the testing series was higher than on earlier, simpler mazes (chimpanzees), or unchanged (capuchin monkeys), suggesting microdevelopment of strategic choice. Structural properties of the mazes affected both species' choices. Capuchin monkeys were less likely than chimpanzees to take a correct path that initially led away from the goal but that eventually led to the goal. Chimpanzees were more likely to make an error by passing a correct path than by turning onto a wrong path. Chimpanzees and one capuchin made more errors on choices farther in sequence from the goal. Each species corrected errors before running into the end of an alley in approximately 40% of cases. Together, these findings suggest nascent planning abilities in each species, and the prospect for significant development of strategic planning capabilities on tasks presenting multiple simultaneous or sequential spatial relations. The computerized maze paradigm appears well suited to investigate movement planning and spatial perception in human and nonhuman primates alike.

Animals↗

Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments.

Chimpanzees (Pan troglodytes) are the most proficient and versatile users of tools in the wild. How such skills become integrated into the behavioural repertoire of wild chimpanzee communities is investigated here by drawing together evidence from three complementary approaches in a group of oil-palm nut- ( Elaeis guineensis) cracking chimpanzees at Bossou, Guinea. First, extensive surveys of communities adjacent to Bossou have shown that population-specific details of tool use, such as the selection of species of nuts as targets for cracking, cannot be explained purely on the basis of ecological differences. Second, a 16-year longitudinal record tracing the development of nut-cracking in individual chimpanzees has highlighted the importance of a critical period for learning (3-5 years of age), while the similar learning contexts experienced by siblings have been found to result in near-perfect (13 out of 14 dyads) inter-sibling correspondence in laterality. Third, novel data from field experiments involving the introduction of unfamiliar species of nuts to the Bossou group illuminates key aspects of both cultural innovation and transmission. We show that responses of individuals toward the novel items differ markedly with age, with juveniles being the most likely to explore. Furthermore, subjects are highly specific in their selection of conspecifics as models for observation, attending to the nut-cracking activities of individuals in the same age group or older, but not younger than themselves. Together with the phenomenon of inter-community migration, these results demonstrate a mechanism for the emergence of culture in wild chimpanzees.

Animals↗

Matching vocalizations to vocalizing faces in a chimpanzee (Pan troglodytes).

Auditory-visual processing of species-specific vocalizations was investigated in a female chimpanzee named Pan. The basic task was auditory-visual matching-to-sample, where Pan was required to choose the vocalizer from two test movies in response to a chimpanzee's vocalization. In experiment 1, movies of vocalizing and silent faces were paired as the test movies. The results revealed that Pan recognized the status of other chimpanzees whether they vocalized or not. In experiment 2, two different types of vocalizing faces of an identical individual were prepared as the test movies. Pan recognized the correspondence between vocalization types and faces. These results suggested that chimpanzees possess crossmodal representations of their vocalizations, as do humans. Together with the ability of vocal individual recognition, this ability might reflect chimpanzees' profound understanding of the status of other individuals.

Acoustic Stimulation↗

Visual preference by chimpanzees (Pan troglodytes) for photos of primates measured by a free choice-order task: implication for influence of social experience.

With a free-choice task, visual preference was estimated in five adult chimpanzees (Pan troglodytes). The subjects were presented with digitized color photographs of various species of primates on a CRT screen. Their touching responses to the photographs were reinforced by food reward irrespective of which photographs they touched. The results revealed that all chimpanzees touched the photographs of humans significantly more than any other species, or phylogenetic families of primates. This tendency was consistent across different stimulus sets. The results suggest that the chimpanzees showed visual preference for the photographs of humans over those of their own species. The results also suggest that the degree of this visual preference was not in accordance with phylogenetic distance from the subjects' species, chimpanzees. The preference for humans was stronger in the case of the colored photographs than in monochromatic ones. All of the five chimpanzees had been in captivity for at least 16 years. They were reared by humans from just after their birth, or at least from 1.5 years old. Their preference might have developed through social experience, especially that during infanthood.

Animals↗

An experimental study of leaf swallowing in captive chimpanzees: insights into the origin of a self-medicative behavior and the role of social learning.

Chimpanzees in the wild swallow the rough hispid leaves of certain plant species as a means of physically expelling intestinal parasites. A plant with such a leaf texture was introduced in 36 trial sessions to a captive group of 11 healthy adult chimpanzees to investigate the possible origin and acquisition of leaf swallowing behavior. One male (housed separately from the group during testing) and one female, both captive born, spontaneously exhibited the behavior on their first trial without prior opportunity to observe others with this plant. Six other chimpanzees on their first trial displayed a phobic response to these leaves and rejected them entirely, while another two chewed and swallowed the leaves in a normal way. Four individuals eventually exhibited the behavior, after having approached and closely observed the leaf swallowing of the first female to exhibit the behavior in the group. Four of the six individuals that initially avoided the leaves never overcame their phobia toward this plant and were not in proximity to a chimpanzee performing leaf swallowing during test sessions. Individuals born to wild chimpanzee mothers were no more likely to perform the behavior than captive-reared group mates. These results suggest that the acquisition of this behavior is based in part on a propensity to fold and swallow rough, hispid leaves, but that the acquisition and spread of leaf swallowing within a group is likely to be socially influenced. This study provides support for the hypothesis that leaf swallowing originated in the wild from opportunistic feeding behavior and was later passed down in the form of a self-medicative behavioral tradition.

Animals↗

Muscle dimensions in the chimpanzee hand.

We dissected the forearms and hands of a female chimpanzee and systematically recorded mass, fiber length, and physiological cross-sectional area (PCSA) of all muscles including those of intrinsic muscles that have not been reported previously. The consistency of our measurements was confirmed by comparison with the published data on chimpanzees. Comparisons of the hand musculature of the measured chimpanzee with corresponding published human data indicated that the chimpanzee has relatively larger forearm flexors but smaller thenar eminence muscles, as observed in previous studies. The interosseous muscles were also confirmed to be relatively larger in the chimpanzee. However, a new finding was that relative PCSA, which reflects a muscle's capacity to generate force, might have increased slightly in humans as a result of relatively shorter muscle fiber length. This suggests that the human intrinsic muscle architecture is relatively more adapted to dexterous manipulative functions. Shortening of the metacarpals and the intervening interosseous muscles might accordingly be a prerequisite for the evolution of human precision-grip capabilities.

Animals↗

Comparison of behavioral sequence of copulation between chimpanzees and bonobos.

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.

Animals↗

Tool-use for drinking water by immature chimpanzees of Mahale: prevalence of an unessential behavior.

Use of leaves or sticks for drinking water has only rarely been observed during long-term study of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Recently, however, we observed 42 episodes of tool-use for drinking water (73 tools and two cases of using "tool-sets") between 1999 and 2004. Interestingly, all of the performers were immature chimpanzees aged from 2 to 10 years. Immature chimpanzees sometimes observed the tool-using performance of others and subsequently reproduced the behavior, while adults usually paid no attention to the performance. This tool-use did not seem to occur out of necessity: (1) chimpanzees often used tools along streams where they could drink water without tools, (2) they used tools for drinking water from tree holes during the wet season when they could easily obtain water from many streams, and (3) the tool-using performance sometimes contained playful aspects. Between-site comparisons revealed that chimpanzees at drier habitats used tools for drinking water more frequently and in a more "conventional" manner. However, some variations could not be explained by ecological conditions. Such variations and the increase in this tool-use in recent years at Mahale strongly suggest that social learning plays an important role in the process of acquiring the behavior. We should note here that such behaviors that lack obvious benefits or necessity can be prevalent in a group.

Aging↗

Visual search for orientation of faces by a chimpanzee (Pan troglodytes): face-specific upright superiority and the role of facial configural properties.

A previous experiment showed that a chimpanzee performed better in searching for a target human face that differed in orientation from distractors when the target had an upright orientation than when targets had inverted or horizontal orientation [Tomonaga (1999a) Primate Res 15:215-229]. This upright superiority effect was also seen when using chimpanzee faces as targets but not when using photographs of a house. The present study sought to extend these results and explore factors affecting the face-specific upright superiority effect. Upright superiority was shown in a visual search for orientation when caricaturized human faces and dog faces were used as stimuli for the chimpanzee but not when shapes of a hand and chairs were presented. Thus, the configural properties of facial features, which cause an inversion effect in face recognition in humans and chimpanzees, were thought to be a source of the upright superiority effect in the visual search process. To examine this possibility, various stimuli manipulations were introduced in subsequent experiments. The results clearly show that the configuration of facial features plays a critical role in the upright superiority effect, and strongly suggest similarity in face processing in humans and chimpanzees.

Animals↗

Selection of the chimpanzee over the baboon as a model for Helicobacter pylori infection.

Baboons (Papio sp.) and chimpanzees (Pan troglodytes) were screened for the presence of Helicobacter pylori. The gastric mucosae of the baboons were colonized by large spiral bacteria. However, a group of adult chimpanzees were identified that were free of spiral gastric bacteria, with five animals being recruited into an H. pylori challenge study. These animals were inoculated orogastrically with one of four strains of H. pylori and followed for up to 26 weeks. H. pylori was established in one of these animals during a primary challenge and in two other animals on secondary challenge. It was shown that the chimpanzee can be infected with H. pylori and that the inflammatory response in these animals mimics that seen in humans. Infection was marked by an antibody response to H. pylori-specific antigens in two animals. It was observed that H. pylori antibody-negative chimpanzees had no apparent infection by H. pylori or related bacteria. Thus serological screening of chimpanzees can be used to identify candidate animals for further evaluation.

Animals↗

Evaluation of thrombogenicity of beta-propiolactone/ultraviolet (beta-PL/UV) treated PPSB in chimpanzees.

The thrombogenicity of beta-PL/UV-treated PPSB (factor IX concentrate) was evaluated in chimpanzees. PPSB isolated from beta-propiolactone-treated and UV-irradiated plasma was injected into chimpanzees at a dose of approximately 100 units/kg body weight. An FDA licensed PPSB preparation served as the negative control, and a preparation containing activated as well as precursor clotting factors served as the positive control. 15 minutes, 1 h, 4 h, and 24 h after the PPSB application the following parameters were determined in the chimpanzee blood: factors II, VII, IX, X, VIII, fibrinogen, AT III, thrombin coagulase, Quick value, APTT and platelet count. Neither the untreated control preparation, nor the PPSB isolated from beta-propiolactone-treated and UV-irradiated plasma, showed signs of thrombogenicity in the chimpanzee model. The positive control indicated that the chimpanzee is a suitable model for the thrombogenicity testing of activated clotting factors.

Animals↗

Characterization of the variable regions of a chimpanzee monoclonal antibody with potent neutralizing activity against HIV-1.

The variable (V) regions of C108G, a potent neutralizing chimpanzee mAb against a glycan-dependent epitope in the V2 region of HIV-1 gp120, have been characterized for reactivity with human VH and VK family-specific antisera, and their nucleotide sequences have been determined and analysed. To our knowledge, this is the first study characterizing expressed chimpanzee VH and VK genes. Results show that C108G expresses members of the VH3 and VK1 families, the largest VH and VK families in humans, respectively. Nucleotide and amino acid sequence analyses reveal that C108G VH is most homologous to the human VH3 germline gene, hsigdp33 or V3-43, and the human JH4 minigene. The human germline VK1 gene that is most homologous to C108G VK, hsigk1012, was previously observed in unmutated form in a human autoantibody with anti-i red blood cell antigen specificity and in seven human Fabs and a mAb directed against epitopes overlapping the CD4-binding site of HIV-1 gp120. This germline gene was unmutated in three of the human Fabs and was somatically mutated in the other four Fabs and the mAb. In addition, the JK minigene was used in C108G VK, JK2, is apparently over-represented in anti-HIV-1 mAbs/Fabs; this minigene was used in 61% of the anti-gp120 human Fabs recently described and in three other anti-CD4-binding site human mAbs derived by EBV transformation. While the significance of these findings is unclear, they may suggest a bias in VK/JK gene usage and/or network regulation involving an hsigk1012/JK2 idiotope(s) in the antibody response to HIV-1. Both the C108G VH and VK genes showed evidence of somatic mutation and antigen selection that apparently occurred in vivo during chronic exposure to HIV-1 and its antigens. Surprisingly, this somatic mutation was most profound in the CDR3 region of C108G VK; this region shared only 48% nucleotide homology with hsigk1012 contrasted with a homology of 94% over the remainder of these two V gene sequences. Perhaps the most significant finding of this study is that the expressed VH and VK genes of chimpanzee mAb C108G are no more divergent from their most homologous human germline genes than are the expressed V genes of several recently characterized human anti-HIV-1 mAbs/Fabs from their apparent human germline genes. This suggests that chimpanzee mAbs are no more likely to elicit deleterious anti-immunoglobulin responses in humans than are human mAbs and emphasizes the potential for development of chimpanzee mAbs as immunotherapeutic agents.

Amino Acid Sequence↗

Polymorphonuclear leukocyte function in HIV-1-infected chimpanzees.

The chemiluminescent characteristics of enriched populations of neutrophils from control and HIV-infected chimpanzees were assessed. Neutrophils from HIV-infected chimpanzees were suppressed in their ability to generate a normal response to particulate and soluble stimuli when compared to normal and hepatitis non-A, non B-infected controls. Particulate (latex beads) stimulation of neutrophils resulted in an aberrant response when contrasted with controls. Normal control responses were characteristically biphasic while the response from hepatitis NANB HIV-infected chimpanzees was not biphasic. Neutrophils challenged with a soluble (phorbol ester) stimulant also demonstrated a suppressed response. These data suggest that HIV infection has an additive suppressive effect on neutrophil function in chimpanzees previously infected with hepatitis NANB. The suppression of chimpanzee neutrophil function following HIV infection is similar to that seen in other non-primate viral and retroviral infections.

Acquired Immunodeficiency Syndrome↗

A comparison in chimpanzees of the immunogenicity and efficacy of live attenuated respiratory syncytial virus (RSV) temperature-sensitive mutant vaccines and vaccinia virus recombinants that express the surface glycoproteins of RSV.

Respiratory syncytial virus (RSV) is the most common cause of viral bronchiolitis and pneumonia in children. The present study compares the level of attenuation, genetic stability and efficacy of three conditional-lethal temperature-sensitive (ts) mutants of the RSV A2 wild-type virus, designated ts-1, ts-1-NG1, and ts-4, in seronegative chimpanzees and also compares their efficacy with that of vaccinia virus recombinants that express the surface glycoproteins of RSV. Each of the ts mutants was highly attenuated in the lower respiratory tract, but still retained the capacity to induce significant rhinorrhoea. Each of the three ts mutants underwent partial reversion to a non-ts (ts+) phenotype during replication in a minority of the chimpanzees. The ts+ virus present in the upper respiratory tract of the chimpanzees did not spread to the lower respiratory tract and represented only a minority fraction of the virus present in the nasopharyngeal swab specimens. The ts mutants were highly immunogenic and provided resistance that effectively restricted RSV replication following virus challenge. In contrast, the vaccinia-RSV recombinants were less immunogenic. They protected the lungs of two of four chimpanzees challenged with RSV, but failed to protect the upper respiratory tract. The chimpanzee can serve as a model for the rapid evaluation of further attenuated live RSV vaccines.

Animals↗

A further attenuated derivative of a cold-passaged temperature-sensitive mutant of human respiratory syncytial virus retains immunogenicity and protective efficacy against wild-type challenge in seronegative chimpanzees.

A cold-passage (cp), temperature-sensitive (ts) RSV mutant designated RSV cpts-248 (shut-off temperature 38 degrees C), which possesses host-range mutations acquired during 52 passages at low temperature in bovine tissue culture and a ts phenotype introduced by subsequent chemical mutagenesis, was found previously to be attenuated, immunogenic, and protective against wild-type challenge in seronegative chimpanzees. We sought to introduce additional attenuating mutations such as small-plaque (sp) and ts mutations into RSV cpts-248 by chemical mutagenesis with 5-fluorouracil with the intent of obtaining cpts-248 derivatives that are more attenuated in mice or chimpanzees and that are more genetically stable following replication in vivo. Ten mutants of RSV cpts-248 which had acquired a sp phenotype or a second ts mutation were generated by chemical mutagenesis. Five cpts-248 derivatives which had acquired mutations that specified a 36 degrees C shut-off temperature for plaque formation and one which had acquired only a sp phenotype were more restricted in replication in Balb/c mice than the cpts-248 parental strain. One mutant, designated RSV cpts-248/404 (shut-off temperature 36 degrees C), was 100 times more restricted in replication in the nasal turbinates of mice and 100 times more restricted in the nasopharynx of seronegative chimpanzees than its cpts-248 parent. The cpts-248/404 mutant was completely restricted in replication in the lower respiratory tract of chimpanzees even following direct intratracheal administration. The ts phenotype of the cpts-248/404 mutant was stable during replication in vivo in mice and chimpanzees.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Male chimpanzees prefer mating with old females.

Cross-cultural studies indicate that women's sexual attractiveness generally peaks before motherhood and declines with age. Cues of female youth are thought to be attractive because humans maintain long-term pair bonds, making reproductive value (i.e. future reproductive potential) particularly important to males. Menopause is believed to exaggerate this preference for youth by limiting women's future fertility. This theory predicts that in species lacking long-term pair bonds and menopause, males should not exhibit a preference for young mates. We tested this prediction by studying male preferences in our closest living relative, the chimpanzee (Pan troglodytes). We show that despite their promiscuous mating system, chimpanzee males, like humans, prefer some females over others. However, in contrast to humans, chimpanzee males prefer older, not younger, females. These data robustly discriminate patterns of male mate choice between humans and chimpanzees. Given that the human lineage evolved from a chimpanzee-like ancestor, they indicate that male preference for youth is a derived human feature, likely adapted from a tendency to form unusually long term mating bonds.

Age Factors↗