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Ancient Plasmodium genomes shed light on the history of human malaria

Megan Michel, Eirini Skourtanioti, Federica Pierini, Evelyn K. Guevara, Angela Mötsch, Arthur Kocher, Rodrigo Barquera, Raffaela A. Bianco, Selina Carlhoff, Lorenza Bove, Suzanne Freilich, Karen Giffin, Taylor R. Hermes, Alina Hiß, Florian Knolle, Elizabeth A. Nelson, Gunnar U. Neumann, Luka Papac, Sandra Penske, Adam B. Rohrlach, Nada Salem, Lena Semerau, Vanessa Villalba‐Mouco, Isabelle Abadie, Mark Aldenderfer, Jessica Beckett, Matthew Brown, Franco Campus, Tsang Chenghwa, María Cruz Berrocal, Ladislav Damašek, Kellie Sara Duffett Carlson, Raphaël Durand, Michal Ernée, Cristinel Fântăneanu, H. Frenzel, Gabriel García Atiénzar, Sonia Guillén, Ellen Hsieh, Maciej Karwowski, David J. Kelvin, Nikki Kelvin, Alexander Khokhlov, Rebecca Kinaston, Arkadii Korolev, Kim-Louise Krettek, Mario Küßner, Luca Lai, Cory Look, Kerttu Majander, Kirsten Mandl, Vittorio Mazzarello, Michael McCormick, María Paz de Miguel Ibáñez, Reg Murphy, Rita E. Németh, Kerkko Nordqvist, Friederike Novotny, Martin Obenaus, Lauro Olmo-Enciso, Päivi Onkamo, Jörg Orschiedt, Valerii Patrushev, Sanni Peltola, Alejandro Romero, Salvatore Rubino, Antti Sajantila, Domingo C. Salazar‐García, Elena Serrano, Shapulat Shaydullaev, Emanuela Sias, Mario Šlaus, Ladislav Stančo, Treena Swanston, Maria Teschler‐Nicola, Frédérique Valentin, Katrien Van de Vijver, Tamara L. Varney, Alfonso Vigil-Escalera Guirado, Christopher K. Waters, Estella Weiss‐Krejci, Eduard Winter, Thiseas C. Lamnidis, Kay Prüfer, Kathrin Nägele, Maria A. Spyrou, Stephan Schiffels, Philipp W. Stockhammer, Wolfgang Haak, Cosimo Posth, Christina Warinner, Kirsten I. Bos, Alexander Herbig, Johannes Krause

2024Nature39 citationsDOIOpen Access PDF

Abstract

Abstract Malaria-causing protozoa of the genus Plasmodium have exerted one of the strongest selective pressures on the human genome, and resistance alleles provide biomolecular footprints that outline the historical reach of these species 1 . Nevertheless, debate persists over when and how malaria parasites emerged as human pathogens and spread around the globe 1,2 . To address these questions, we generated high-coverage ancient mitochondrial and nuclear genome-wide data from P. falciparum , P. vivax and P. malariae from 16 countries spanning around 5,500 years of human history. We identified P. vivax and P. falciparum across geographically disparate regions of Eurasia from as early as the fourth and first millennia bce , respectively; for P. vivax , this evidence pre-dates textual references by several millennia 3 . Genomic analysis supports distinct disease histories for P. falciparum and P. vivax in the Americas: similarities between now-eliminated European and peri-contact South American strains indicate that European colonizers were the source of American P. vivax , whereas the trans-Atlantic slave trade probably introduced P. falciparum into the Americas. Our data underscore the role of cross-cultural contacts in the dissemination of malaria, laying the biomolecular foundation for future palaeo-epidemiological research into the impact of Plasmodium parasites on human history. Finally, our unexpected discovery of P. falciparum in the high-altitude Himalayas provides a rare case study in which individual mobility can be inferred from infection status, adding to our knowledge of cross-cultural connectivity in the region nearly three millennia ago.

Topics & Concepts

MalariaPlasmodium (life cycle)GenomeProtozoaBiologyEvolutionary biologyGenusPlasmodium falciparumResistance (ecology)GeneticsZoologyParasite hostingEcologyGeneImmunologyComputer scienceWorld Wide WebMalaria Research and ControlHIV Research and Treatmentvaccines and immunoinformatics approaches