Blood groups of anthropoid apes and their relationship to human blood groups

Affinity between blood groups of man and those of anthropoid apes is reflected not only in similarities or identities of reactions of the red cells with many specific typing reagents, but also in overall structures of some of the main blood group systems defined in man and in apes.Besides specificities of human-type, such as A-B-O, M-N, Rh-Hr, I-i, etc. known to be present on the red cells of various species of apes, specific reagents were produced by iso- or cross-immunization of chimpanzees that detect red cell specificities characteristic for apes only. Some of those specificities were found to be shared by several ape species and to fall into separate blood group systems that are counterparts of the human blood group systems. Recently obtained serological, as well as population data, indicate that the chimpanzee R-C-E-F blood group system is the counterpart of the human Rh-Hr system. Similarly to the Rh-Hr system, it is built around a main antigen, the R^c antigen, to which secondary specificities are attached by means of multiple allelic genes. The R^c is not only the principal factor of the chimpanzee R-C-E-F group system, but also constitutes a direct link with the human Rh-Hr blood group system, since anti-R^c reagents also detect Rh₀ specificity on the human red cells. Another chimpanzee blood group system, the V-A-B-D system, is counterpart of the M-N-S-s system, and is built around the central antigen V^c. the V^c is not only the principal specificity of the chimpanzee V-A-B-D system, but it also constitutes the direct link with the human M-N-S-s system since anti-V^c reagent gives with chimpanzee red cells reactions parralleling those obtained with anti-N lectin (N^v) while in tests with human red cells it detects specificity identical or closely related to the Mi^a specificity.     

Evidence for convergent evolution of A and B blood group antigens in primates

To determine whether convergent or trans-specific evolution is responsible for the persistence of the ABO polymorphism in apes, we have sequenced segments of introns 5 and 6 of the ABO gene. Four substitutions and one insertion or deletion group human A, B, and O alleles together, separate from their chimpanzee A and gorilla B counterparts. No shared substitutions support a trans-species mode of evolution for any of the alleles examined. We conclude that the A and B antigens of the chimpanzee and gorilla, respectively, have arisen by convergent evolution. Phylogenetic analysis suggests that the human A and B alleles are ancient, having diverged at least 3 million years ago. These alleles must have therefore been trans-specifically inherited within the genus Homo. Received: 28 May 1997 / Accepted: 31 July 1997     

Conservation of intronic minisatellite polymorphisms in the SCK1/SHC2 gene of Hominidae

The neuronally expressed Shc adaptor homolog SCK1/SHC2 gene contains an unusually high number of minisatellites. In humans, twelve different minisatellite sequences are located in introns of SCK1/SHC2 and ten of them are highly polymorphic. Here we used primers developed for humans to screen ten intronic loci of SCK1/SHC2 in chimpanzee and gorilla, and undertook a comprehensive analysis of the genomic sequence to address the evolutionary events driving these variable repeats. All ten loci amplified in chimpanzee and gorilla contained hypervariable and low-variability minisatellites. The human polymorphic locus TR1 was monomorphic in chimpanzee and gorilla, but we detected polymorphic alleles in these apes for the human monomorphic TR7 locus. When we examined the repeat size among these hominoids, there was no consistent variation by length from humans to great apes. In spite of the inconsistent evolutionary dynamics in repeat length variation, exon 16 was highly conserved between humans and great apes. These results suggest that non-coding intronic minisatellites do not show a consistent evolutionary paradigm but evolved with different patterns among each minisatellite locus. These findings provide important insight for minisatellite conservation during hominoid evolution.     

Epidermal patterns of the hands and feet of the pygmy chimpanzee (Pan paniscus)

The characteristics of the epidermal ridge system were studied in a series of eighteen lesser or pygmy chimpanzees (Pan paniscus). The general ridge alignments are very similar to those of the chimpanzee (Pan troglodytes); Biegert ('61). On the average the pattern intensity (P.I.) of the palm configurations is considerably higher in the pygmy chimpanzee than in the chimpanzee, thus representing the highest total palm pattern intensity of all species of the Hominoidea. The sole configurations show parallel main results to those of the palm; however, the decreased sole pattern frequency of the pygmy chimpanzee is of a smaller predominance only as compared to the values of the other species of this superfamily. The preliminary data on the finger tip patterns, translated into P.I. values, are much higher than in chimpanzees and within the range of the mean values of gorillas (Brehme, '73), while those of the toes of pygmy chimpanzees seem to possess the lowest P.I. values of the African apes.     

Patterns of microsatellite polymorphism in the range-restricted bonobo (Pan paniscus): considerations for interspecific comparison with chimpanzees (P. troglodytes)

The endangered great ape, Pan paniscus (bonobo) has the smallest range of the African apes. Virtually nothing is known about the genetic diversity or genetic structure of this species, while substantial amounts of polymorphism have been reported for the bonobo’s widespread congener, the chimpanzee (P. troglodytes). Given its restricted range, what is the extent of genetic variation in the bonobo relative to the chimpanzee, and is the bonobo genetically depauperate? To investigate patterns of genetic polymorphism, bonobos of wild origin were genotyped for 28 microsatellite loci. The mean number of alleles per locus (5.2) and the mean observed heterozygosity (0.52) in bonobos were similar to variation observed in a wild chimpanzee community (P. t. schweinfurthii). The rarer bonobo is not genetically depauperate and may have genetic diversity comparable to the eastern chimpanzee subspecies. Bonobos have approximately 55% of the allelic diversity and 66% of the observed heterozygosity exhibited by all three chimpanzee subspecies sampled across equatorial Africa. Resampling techniques were used to quantify the effects of sample size differences and number and choice of loci between bonobos and chimpanzees. The examination of these variables underscores their importance in accurately interpreting interspecific comparisons of diversity estimates.     

Ontogeny of mirror behavior in two species of great apes

Mirror image reactions of two infant apes, a female chimpanzee (Pan troglodytes) and a male orangutan (Pongo pygmaeus), born at the Zoo de Vincennes and the Jardin des Plantes of Paris, France, respectively, were studied and compared with those of children. Self-recognition was also tested following 46.5 hours of mirror exposure by application of red marks on parts of the body invisible to the animal without the aid of the mirror. Results indicated that the behavior of the two young apes followed a developmental trend similar to that of human babies. At the end of the study, the female chimpanzee (11 months of age) expressed social behavior, searched for the image behind the mirror, and showed interest in imaged movement. The orangutan (2 years and 5 months old) had begun to test movement synchronism and to display self-directed behaviors. The tests of self-recognition yielded negative results in both animals.     

Trans-species origin of Mhc-DRB polymorphism in the chimpanzee

Trans-specific evolution of allelic polymorphism at the major histocompatibility complex loci has been demonstrated in a number of species. Estimating the substitution rates and the age of trans-specifically evolving alleles requires detailed information about the alleles in related species. We provide such information for the chimpanzee DRB genes. DNA fragments encompassing exon 2 were amplified in vitro from genomic DNA of ten chimpanzees. The nucleotide sequences were determined and their relationship to the human DRB alleles was evaluated. The alleles were classified according to their positioni in dendrograms and the presence of lineage-specific motifs. Twenty alleles were found at the expressed loci Patr-DRB1,-DRB3, -DRB4, -DRB5, and at the pseudogenes Patr-DRB6, -DRB7; of these, 13 are new alleles. Two other chimpanzee sequences were classified as members of a new lineage tentatively designated DRBX. Chimpanzee counterparts of HLA-DRB1 ^* 01 and ^* 04 were not detected. The number of alleles found at individual loci indicates asymmetrical distribution of polymorphism between humans and chimpanzees. Estimations of intra-lineage divergence times suggest that the lineages are more than 30 million year old. Predictions of major chimpanzee DRB haplotypes are made.The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers M94937-M94954.     

Molecular evolution of IgG subclass among nonhuman primates: implication of differences in antigenic determinants among Apes

The cross-reactivity of five different rabbit polyclonal antibodies to human IgG and IgG subclass (IgG1, IgG2, IgG3, and IgG4) was determined by competitive ELISA with nine nonhuman primate species including five apes, three Old World monkeys, and one New World monkey. As similar to those previously reported, the reactivity of anti-human IgG antibody with plasma from different primate species was closely related with phylogenic distance from human. Every anti-human IgG subclass antibody showed low cross-reactivity with plasma from Old World and New World monkeys. The plasma from all apes except for gibbons (Hylobates spp.) showed 60 to 100% of cross-reactivity with anti-human IgG2 and IgG3 antibodies. On the other hand, chimpanzee (Pan troglodytes andPan paniscus) and orangutan (Pongo pygmaeus) plasma showed 100% cross-reactivity with anti-human IgG1 antibody, but gorilla (Gorilla gorilla) and gibbon plasma showed no cross-reactivity. The chimpanzee and gorilla plasma cross-reacted with anti-human IgG4 antibody at different reactivity, 100% in chimpanzee and 50% in gorilla, but no cross-reactivity was observed in orangutan and gibbon plasma. These results suggest the possibilities that the divergence of “human-type” IgG subclasses might occur at the time of divergence ofHomo sapience fromHylobatidae, and that the molecular evolution of IgG1 as well as IgG4 is different from that of IgG2 and IgG3 in great apes, this is probably caused by different in development of immune function in apes during the course of evolution.     

Densities,Distributions, and Seasonal Movements of Gorillas and Chimpanzees in Swamp Forest in Northern Congo

The conservation of gorillas (Gorilla spp.) and chimpanzees (Pan troglodytes) depends upon knowledge of their densities and distribution throughout their ranges. However, information about ape populations in swamp forests is scarce. Here we build on current knowledge of ape populations by conducting line transect surveys of nests throughout a reserve dominated by swamp forest: the Lac Télé Community Reserve in northern Congo. We estimated gorilla and chimpanzee densities, distributions across habitats, and seasonal changes in abundance. Gorilla density was 2.9 gorillas km^–2, but densities varied by habitat (0.3–5.4 gorillas km^–2) with highest densities in swamp forest and terra firma mixed forest. Average chimpanzee density is 0.7 chimpanzees km^–2 (0.1–1.3 chimpanzees km^–2), with highest densities in swamp forest. Habitat was the best predictor of ape nest abundance, as neither the number of human indices nor the distance from the nearest village predicted nest abundance. We recorded significantly greater numbers of apes in terra firma forest during the high-water season than the low-water season, indicating that many gorillas and chimpanzees are at times concentrated in terra firma forest amid a matrix of swamp forest. Seasonally high numbers of apes on terra firma forest islands easily accessible to local people may expose them to substantial hunting pressure. Conversely, the nearly impenetrable nature of swamp forests and their low value for logging makes them promising sites for the conservation of apes.     

Genome size and «C-heterochromatic-DNA» in man and the african apes

The genome sizes and the amounts of DNA after C-banding pretreatments (C-heterochromatic DNA) were measured by quantitative cytochemical methods in man and the African apes,Gorilla gorilla andPan troglodytes. As evaluated by flow cytometry on propidium-iodide-stained lymphocytes, gorilla and chimpanzee have genome sizes larger than man. On the basis of the different resistance of metaphase chromosome DNA to the C-banding procedure, two genome compartments were defined, i.e.,C-heterochromatic-DNA andeuchromatic-DNA. The latter proved to be fairly constant in man and the African apes (as well as in two hylobatid species), whereas the variable amounts ofC-heterochromatic-DNA account well for the interspecific differences of genome size among the hominoid species studied so far. During karyotype diversification, quantitative changes (with either gains or losses) ofC-heterochromatic-DNA seem to have taken place independently in the hylobatid and the man/African ape lineages.     

Electromyography of brachial muscles in Pan troglodytes and Pongo pygmaeus

Electromyographic recordings were taken from all heads of the triceps brachii and biceps brachii muscles and from the anconeus, brachialis, and brachioradialis muscles in a chimpanzee and an orangutan as they stood still and walked quadrupedally on horizontal and inclined surfaces, engaged in suspensory behavior, reached overhead, and manipulated a variety of foods and artifacts. Like the gorilla (Tuttle and Basmajian, 1974a), the chimpanzee and orangutan possess special close-packed positioning mechanisms that allow the bulky muscles that cross their elbow joints to remain silent during quiet pendant suspension. We found no major myological features that would dramatically separate the arms of knuckle-walking African apes from those of the orangutan. With a few exceptions, which could as well be attributed to individual variation as to interspecific differences, the brachial muscles acted similarly during quadrupedal positional behaviors, irrespective of whether the hands of the subjects were knuckled (African apes), fisted (chimpanzee and orangutan), or placed in modified palmigrade postures (orangutan). Evolutionary transformations, from brachial and elbow complexes like those of Pongo to ones like Pan, or vice versa, would probably be achieved quite readily as the species changed its substrate preferences and positional habits.     

Evidence for an HLA-C-like locus in the orangutan Pongo pygmaeus

 HLA-B and C are related class I genes which are believed to have arisen by duplication of a common ancestor. Previous study showed the presence of orthologues for both HLA-B and C in African apes but only for HLA-B in Asian apes. These observations suggested that the primate C locus evolved subsequent to the divergence of the Pongidae and Hominidae. From an analysis of orangutan Tengku two HLA-C-like alleles (Popy C*0101 and Popy C*0201) were defined as well as three HLA-B-like (Popy-B) alleles. By contrast, no Popy-C alleles were obtained from orangutan Hati, although three Popy-B alleles were defined. Thus an HLA-C-like locus exists in the orangutan (as well as a duplicated B locus), implying that the primate C locus evolved prior to the divergence of the Pongidae and Hominidae and is at least 12–13 million years old. Uncertain is whether all orangutan MHC haplotypes contain a C locus, as the failure to find C alleles in some individuals could be due to a mispairing of HLA-C-specific primers with certain Popy-C alleles. These results raise the possibilities that other primate species have a C locus and that the regulation of natural killer cells by C allotypes evolved earlier in primate evolution than has been thought. Received: 18 January 1999 / Revised: 23 March 1999     

Comparison of allele O sequences of the human and non-human primate ABO system

 Like humans, non-human primates express the antigens A and B of the ABO histoblood group system. In chimpanzees, only A and O types are found, while the types A, B, AB, and O are found in macaques. The sequences of exons 6 and 7 of two chimpanzee O alleles (O ^del and O ^x ), two macaque species O alleles (rhesus monkey and crab-eating macaque), and sequences of exon 7 of two major chimpanzee A alleles (A ^1ch and A ^2ch ) were established. The sequences of cDNAs corresponding to the chimpanzee and rhesus monkey O alleles were characterized from exon 1 to 7 and from exon 4 to 7, respectively. A comparison of our results with ABO gene sequences already published by others demonstrates that human and non-human primate O alleles are species-specific and result from independent silencing mutations. These observations reinforce the hypothesis that the maintenance of the ABO gene polymorphism in primates reflects convergent evolution more than transpecies inheritance of ancestor alleles. Received: 30 July 1998 / Revised: 12 December 1998     

Comparative mapping of ZFY in the hominoid apes

Summary Within our project of comparative mapping of candidate genes for sex-determination/testis differentiation, we used a cloned probe from the human ZFY locus for comparative hybridization studies in hominoids. As in the human, the ZFY probe detects X- and Y-specific restriction fragments in the chimpanzee, the gorilla, the orangutan, and the gibbon. Furthermore, the X-specific hybridization site in the great apes resides in Xp21.3, the same locus defining ZFX in the human. The Y-specific locus of ZFY maps closely to the early replicating pseudoautosomal segment in the telomeric or subtelomeric position of the Y chromosomes of the great apes, again as found in the human. Thus, despite cytogenetically visible structural alterations within the euchromatic parts of the Y chromosomes of the human species and the great apes, a segment of the Y chromosome defined by the pseudoautosomal region and ZFY seems to be more strongly conserved than the rest of the Y chromosome.     

Mass spectral analyses of the two major apolipoproteins of great ape high density lipoproteins

The two major apolipoproteins associated with human and chimpanzee (Pan troglodytes) high density lipoproteins (HDL) are apoA-I and dimeric apoA-II. Although humans are closely related to great apes, apolipoprotein data do not exist for bonobos (Pan paniscus), western lowland gorillas (Gorilla gorilla gorilla) and the Sumatran orangutans (Pongo abelii). In the absence of any data, other great apes simply have been assumed to have dimeric apoA-II while other primates and most other mammals have been shown to have monomeric apoA-II. Using mass spectrometry, we have measured the molecular masses of apoA-I and apoA-II associated with the HDL of these great apes. Each was observed to have dimeric apoA-II. Being phylogenetically related, one would anticipate these apolipoproteins having a high percentage of invariant sequences when compared with human apolipoproteins. However, the orangutan, which diverged from the human lineage between 16 and 21 million years ago, had an apoA-II with the lowest monomeric mass, 8031.3 Da and the highest apoA-I value, 28,311.7 Da, currently reported for various mammals. Interestingly, the gorilla that diverged from the lineage leading to the human–chimpanzee branch after the orangutan had almost identical mass values to those reported for human apoA-I and apoA-II. But chimpanzee and the bonobo that diverged more recently had identical apoA-II mass values that were slightly larger than reported for the human apolipoprotein. The chimpanzee A-I mass values were very close to those of humans; however, the bonobo had values intermediate to the molecular masses of orangutan and the other great apes. With the already existing genomic data for chimpanzee and the recent entries for the orangutan and gorilla, we were able to demonstrate a close agreement between our mass spectral data and the calculated molecular weights determined from the predicted primary sequences of the respective apolipoproteins. Post-translational modification of these apolipoproteins, involving truncation and oxidation of methionine, are also reported.     

Two monoclonal antibodies highly specific for the blood group N determinant

Two monoclonal IgM antibodies, 179K and 35/5F, obtained following immunization of mice with A₂,MN or O,MN human erythrocytes, agglutinate NN and MN red cells strongly, and MM erythrocytes weakly. As shown by hemagglutination inhibition and solid phase ELISA, both antibodies are highly specific for the blood group N determinant. They react with N glycoprotein, its amino-terminal glycopeptides and with Ss glycoprotein (glycophorin B), which carries the blood group N determinant. They fail to react with M glycoprotein, M glycoprotein-derived glycopeptides, or with internal glycopeptides derived from N glycoprotein. Reaction of the antibodies with N glycoprotein is abolished by desialylation, periodate oxidation/borohydride reduction, orN-acetylation of the glycoprotein. Thus, the antibodies are specific for an epitope which includes sialylated oligosaccharide chain(s) and is located in the region of the amino-terminal leucine residue of N glycoprotein. MMU^– erythrocytes, lacking both blood group N and Ss glycophorin are non-reactive. Agglutination of MMU⁺ erythrocytes by the anti-N antibodies occursvia interaction with glycophorin B and correlates with the Ss phenotype of red cells MM,S erythrocytes are usually more strongly, agglutinated than MM,ss cells. The agglutination of MM erythrocytes decreases markedly as the pH is increased from 6 to 8, while agglutination of NN red cells is much less affected by shifts in pH over this range. As a result, both monoclonal antibodies are highly anti-N specific typing reagents when the agglutination assay is carried out at pH 8.     

Serum cholinesterase activities and inhibition profiles of nonhuman primates

Serum cholinesterase activities and inhibition profiles of 169 chimpanzees, 15 gorillas, 26 orangutans, seven gibbons, and 12 rhesus monkeys were determined. Mean values of activities against benzoylcholine (μmols/min/ml) and dibucaine, fluoride, and Ro 2-0683 numbers (percentage inhibition of benzoylcholine hydrolysis) are: chimpanzee, 2.276, 80, 64, and 97; gorilla, 9.403, 82, 71, and 96; orangutan, 0.747, 94, 6, and 98; gibbon, 0.071, 89, 7, and 94; and rhesus monkey, 0.859, 95, 10, and 99, respectively. Sernylan numbers were determined of the last 100 chimpanzee serums collected and of each of the gorilla, orangutan, gibbon, and rhesus monkey serums. Mean values of Sernylan numbers are: chimpanzee, 80; gorilla, 81; orangutan, 95; gibbon, 94; and rhesus monkey, 96. The chimpanzee and the gorilla have dibucaine, fluoride, Ro 2-0683, and Sernylan numbers within the range found in men who are homozygotes for the usual cholinesterase (genotype E₁^uE₁^u). No cholinesterase variant was found in any chimpanzee or gorilla. The orangutan, gibbon, and rhesus monkey have inhibition profiles that resemble one another, with higher dibucaine and Sernylan numbers and much lower fluoride numbers than the chimpanzee or the gorilla. The results of the inhibition tests suggest that the African apes, chimpanzee and gorilla, are related more closely to man than are the Asian apes, orangutan and gibbon.     

Lineage-Specific Homogenization of the Polyubiquitin Gene Among Human and Great Apes

Ubiquitin is a highly conserved protein, and is encoded by a multigene family among eukaryote species. The polyubiquitin genes, UbB and UbC, comprise tandem multiple ubiquitin coding units without a spacer region or intron. We determined nucleotide sequences for the UbB and UbC of human, chimpanzee, gorilla, and orangutan. The ubiquitin repeat number of UbB was constant (3) in human and great apes, while that of UbC varied: 6 to 11 for human, 10 to 12 for chimpanzee, 8 for gorilla, and 10 for orangutan. The heterogeneity of the repeat number within closely related hominoid species suggests that a lineage-specific unequal crossover and/or gene duplication occurred. A marked homogenization of UbC occurred in gorilla with a low level of synonymous difference (p_s). The homogenization of UbC also occurred in chimpanzee and less strikingly in human. The first and last ubiquitin coding units of UbC were clustered independently between species, and less affected by homogenization during the hominoid evolution. Therefore, the homogenization of ubiquitin coding units is likely due to an unequal crossing-over inside the ubiquitin units. The lineage-specific homogenization of UbC among closely related species suggests that concerted evolution has a key role in the short-term evolution of UbC.     

DA/DAPI fluorescent bands in the chromosomes of Pan paniscus

The fluorochrome pattern produced by DA/DAPI double staining in Pan paniscus chromosomes is reported. The location of DA/DAPI prominent bands differs from that reported for all other hominoid species. However, the pattern in the pygmy chimpanzee is most similar to that seen in Pan troglodytes. Comparison of the DA/DAPI pattern of the other hominoid species allows the construction of a proposed hominoid ancestral karyotype and a preliminary phylogenetic reconstruction of DA/DAPI bands for the great apes and man.