Bonobos Maintain Immune System Diversity with Three Functional Types of MHC-B.
Fast-evolving MHC class I polymorphism serves to diversify NK cell and CD8 T cell responses in individuals, families, and populations. Because only chimpanzee and bonobo have strict orthologs of all HLA class I, their study gives unique perspectives on the human condition. We defined polymorphism of Papa-B, the bonobo ortholog of HLA-B, for six wild bonobo populations. Sequences for Papa-B exon 2 and 3 were determined from the genomic DNA in 255 fecal samples, minimally representing 110 individuals. Twenty-two Papa-B alleles were defined, each encoding a different Papa-B protein. No Papa-B is identical to any chimpanzee Patr-B, human HLA-B, or gorilla Gogo-B. Phylogenetic analysis identified a clade of MHC-B, defined by residues 45-74 of the α1 domain, which is broadly conserved among bonobo, chimpanzee, and gorilla. Bonobo populations have 3-14 Papa-B allotypes. Three Papa-B are in all populations, and they are each of a different functional type: allotypes having the Bw4 epitope recognized by killer cell Ig-like receptors of NK cells, allotypes having the C1 epitope also recognized by killer cell Ig-like receptors, and allotypes having neither epitope. For population Malebo, these three Papa-B are the only Papa-B allotypes. Although small in number, their sequence divergence is such that the nucleotide diversity (mean proportional distance) of Papa-B in Malebo is greater than in the other populations and is also greater than expected for random combinations of three Papa-B Overall, Papa-B has substantially less diversity than Patr-B in chimpanzee subspecies and HLA-B in indigenous human populations, consistent with bonobo having experienced narrower population bottlenecks.
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305; eewro1@stanford.edu peropa@stanford.edu. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305. Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305. Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305. Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305. Department of Ecology and Management of Plant and Animal Resources, Faculty of Sciences, University of Kisangani, 2012 Kisangani, Democratic Republic of the Congo. Institut National de Recherche Biomédicales, 1197 Kinshasa, Democratic Republic of the Congo. University of Kinshasa, 190 Kinshasa, Democratic Republic of the Congo. Institut de Recherche pour le Développement, Université de Montpellier, 34394 Montpellier, France; and. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138. Institut de Recherche pour le Développement, Université de Montpellier, 34394 Montpellier, France; and. Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104. Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305; eewro1@stanford.edu peropa@stanford.edu. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305.
