Population Genomic Evidence of Adaptive Response during the Invasion History of Plasmodium falciparum in the Americas

Abstract Plasmodium falciparum, the most virulent agent of human malaria, spread from Africa to all continents following the out-of-Africa human migrations. During the transatlantic slave trade between the 16th and 19th centuries, it was introduced twice independently to the Americas where it adapte...

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Bibliographic Details
Published in:Molecular biology and evolution 2023-05, Vol.40 (5)
Main Authors: Lefebvre, Margaux J M, Daron, Josquin, Legrand, Eric, Fontaine, Michael C, Rougeron, Virginie, Prugnolle, Franck
Format: Article
Language:English
Subjects:
Americas
Analysis
Animals
Biochemistry, Molecular Biology
Biodiversity
Discoveries
Ecology, environment
Emerging diseases
Genes
Genetic aspects
Genomics
Human health and pathology
Humans
Infectious diseases
Life Sciences
Malaria
Malaria, Falciparum - genetics
Metagenomics
Microbiology and Parasitology
Plasmodium falciparum
Plasmodium falciparum - genetics
Polymorphism, Genetic
Populations and Evolution
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Summary:Abstract Plasmodium falciparum, the most virulent agent of human malaria, spread from Africa to all continents following the out-of-Africa human migrations. During the transatlantic slave trade between the 16th and 19th centuries, it was introduced twice independently to the Americas where it adapted to new environmental conditions (new human populations and mosquito species). Here, we analyzed the genome-wide polymorphisms of 2,635 isolates across the current P. falciparum distribution range in Africa, Asia, Oceania, and the Americas to investigate its genetic structure, invasion history, and selective pressures associated with its adaptation to the American environment. We confirmed that American populations originated from Africa with at least two independent introductions that led to two genetically distinct clusters, one in the North (Haiti and Colombia) and one in the South (French Guiana and Brazil), and an admixed Peruvian group. Genome scans revealed recent and more ancient signals of positive selection in the American populations. Particularly, we detected positive selection signals in genes involved in interactions with hosts (human and mosquito) cells and in genes involved in resistance to malaria drugs in both clusters. Analyses suggested that for five genes, adaptive introgression between clusters or selection on standing variation was at the origin of this repeated evolution. This study provides new genetic evidence on P. falciparum colonization history and on its local adaptation in the Americas.
ISSN:0737-4038
1537-1719
DOI:10.1093/molbev/msad082