Malaria-driven adaptation of MHC class I in wild bonobo populations

Emily E Wroblewski; Lisbeth A Guethlein; Aaron G Anderson; Weimin Liu; Yingying Li; Sara E Heisel; Andrew Jesse Connell; Jean-Bosco N Ndjango; Paco Bertolani; John A Hart; Terese B Hart; Crickette M Sanz; David B Morgan; Martine Peeters; Paul M Sharp; Beatrice H Hahn; Peter Parham

doi:10.1038/s41467-023-36623-9

Malaria-driven adaptation of MHC class I in wild bonobo populations

Nat Commun. 2023 Feb 23;14(1):1033. doi: 10.1038/s41467-023-36623-9.

Authors

Emily E Wroblewski¹, Lisbeth A Guethlein², Aaron G Anderson³, Weimin Liu⁴, Yingying Li⁴, Sara E Heisel³, Andrew Jesse Connell^{4

5}, Jean-Bosco N Ndjango⁶, Paco Bertolani⁷, John A Hart⁸, Terese B Hart⁸, Crickette M Sanz^{3

9}, David B Morgan¹⁰, Martine Peeters¹¹, Paul M Sharp^{12

13}, Beatrice H Hahn^{4

5}, Peter Parham^{2

14}

Affiliations

¹ Department of Anthropology, Washington University in St. Louis, Saint Louis, 63130, MO, USA. emily.wroblewski@wustl.edu.
² Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, 94305, USA.
³ Department of Anthropology, Washington University in St. Louis, Saint Louis, 63130, MO, USA.
⁴ Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁵ Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁶ Department of Ecology and Management of Plant and Animal Resources, Faculty of Sciences, University of Kisangani, BP 2012, Kisangani, Democratic Republic of the Congo.
⁷ Institute of Human Sciences, School of Anthropology and Museum Ethnography, University of Oxford, Oxford, UK.
⁸ Frankfurt Zoological Society, Lomami National Park Project, Kinshasa, Democratic Republic of the Congo.
⁹ Congo Program, Wildlife Conservation Society, Brazzaville, Republic of the Congo.
¹⁰ Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, 60614, USA.
¹¹ Recherche Translationnelle Appliquée au VIH et aux Maladies Infectieuses, Institut de Recherche pour le Développement, University of Montpellier, INSERM, 34090, Montpellier, France.
¹² Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, EH9 3FL, UK.
¹³ Centre for Immunity, Infection, and Evolution, University of Edinburgh, Edinburgh, EH9 3FL, UK.
¹⁴ Department of Microbiology & Immunology, Stanford University School of Medicine, Stanford, CA, 94305, USA.

Abstract

The malaria parasite Plasmodium falciparum causes substantial human mortality, primarily in equatorial Africa. Enriched in affected African populations, the B*53 variant of HLA-B, a cell surface protein that presents peptide antigens to cytotoxic lymphocytes, confers protection against severe malaria. Gorilla, chimpanzee, and bonobo are humans' closest living relatives. These African apes have HLA-B orthologs and are infected by parasites in the same subgenus (Laverania) as P. falciparum, but the consequences of these infections are unclear. Laverania parasites infect bonobos (Pan paniscus) at only one (TL2) of many sites sampled across their range. TL2 spans the Lomami River and has genetically divergent subpopulations of bonobos on each side. Papa-B, the bonobo ortholog of HLA-B, includes variants having a B*53-like (B07) peptide-binding supertype profile. Here we show that B07 Papa-B occur at high frequency in TL2 bonobos and that malaria appears to have independently selected for different B07 alleles in the two subpopulations.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Histocompatibility Antigens Class I* / genetics
Malaria, Falciparum* / genetics
Pan paniscus* / genetics
Pan paniscus* / parasitology
Peptides
Phylogeny
Plasmodium*

Substances

Peptides
Histocompatibility Antigens Class I

Abstract

Publication types

MeSH terms

Substances

Grants and funding