Population genomic evidence of adaptive response during the invasion history ofPlasmodium falciparumin 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 adapted to new environmental conditions (new human populations and mosquito species). Here, we analyzed the genome-wide polymorphisms of 2,635 isolates across the currentP. falciparumdistribution 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 Columbia) and one in the South (French Guiana and Brazil), and the 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 host (human and mosquito) cells and in genes involved in resistance to malaria drugs in both clusters. We found that some genes were under selection 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 onP. falciparumcolonization history and on its local adaptation in the Americas.

Temporal patterns of haplotypic and allelic diversity reflect the changing selection landscape of the malaria parasitePlasmodium falciparum

“…French Guiana is located within the Guiana Shield region of South America and harbors a low P. falciparum endemicity that is concentrated in remote regions, particularly sites connected with gold mining (Musset et al 2014;Douine et al 2020). Movement of people and parasites throughout the Guiana Shield is well documented (Douine et al 2017;Mathieu et al 2021) and previous genetic clustering analyses of South American P. falciparum have shown that the Guiana Shield region harbors a genetically distinct parasite population (Yalcindag et al 2012;Carrasquilla et al 2022;Lefebvre et al 2023). P. falciparum gene flow therefore occurs across a region that is exposed to the varied public health measures in Brazil, French Guiana, Suriname, Guyana, and Venezuela (Sanna et al 2024).…”