Population genomic evidence of structured and connected Plasmodium vivax populations under host selection in Latin America

Abstract

Pathogen genomic epidemiology has the potential to provide a deep understanding of population dynamics, facilitating strategic planning of interventions, monitoring their impact, and enabling timely responses, and thereby supporting control and elimination efforts of parasitic tropical diseases. Plasmodium vivax, responsible for most malaria cases outside Africa, shows high genetic diversity at the population level, driven by factors like sub‐patent infections, a hidden reservoir of hypnozoites, and early transmission to mosquitoes. While Latin America has made significant progress in controlling Plasmodium falciparum, it faces challenges with residual P. vivax. To characterize genetic diversity and population structure and dynamics, we have analyzed the largest collection of P. vivax genomes to date, including 1474 high‐quality genomes from 31 countries across Asia, Africa, Oceania, and America. While P. vivax shows high genetic diversity globally, Latin American isolates form a distinctive population, which is further divided into sub‐populations and occasional clonal pockets. Genetic diversity within the continent was associated with the intensity of transmission. Population differentiation exists between Central America and the North Coast of South America, vs. the Amazon Basin, with significant gene flow within the Amazon Basin, but limited connectivity between the Northwest Coast and the Amazon Basin. Shared genomic regions in these parasite populations indicate adaptive evolution, particularly in genes related to DNA replication, RNA processing, invasion, and motility – crucial for the parasite's survival in diverse environments. Understanding these population‐level adaptations is crucial for effective control efforts, offering insights into potential mechanisms behind drug resistance, immune evasion, and transmission dynamics.

Genomic exploration of the complex journey ofPlasmodium vivaxin Latin America

“…The geographic distribution of genetic diversity across the Latin American region revealed that P. vivax populations along the Pacific coast (Colombia and Peru) exhibited lower genetic diversity (π) compared with Amazonian populations (Brazil, French Guiana, and Venezuela) (S9 Fig.). This is in line with previous studies [36,54], and could stem from transmission pattern variations across regions [36]. Indeed, coastal areas experience more periodic malaria transmission events compared with the Amazon region, where transmission is more stable throughout the year [55,56].…”

“…2c). Specially, two distinct genetic clusters were identified, as previously observed [13,29,36]: (1) isolates from Mexico, Honduras, and Colombia gathered together as a Central American group, and (2) isolates from the French Guiana, Guyana, and Venezuela formed another distinct cluster as an Amazonian group (Fig. 2d).…”

“…For instance, Sutanto et al [50] established a genetic connection between Colombian and Peruvian isolates, indicating a possible cross-border spread between theses countries. Other studies confirmed genetic links between the various ancestral populations previously identified in Brazilian and Peruvian P. vivax populations, suggesting significant gene flow between these countries [36], as well as with other Amazonian countries such as Guyana [36], French Guiana and Venezuela [13]. These results highlight the possibility of gene flows between Peru, Brazil, Guyana, Venezuela, and French Guyana that could be explained by the large asymptomatic human reservoirs and the dormant stage characteristic of P. vivax [51][52][53].…”

“…2 and 3). As previously reported [13,29,36], in Latin America, two separate genetic clusters were identified, representing the Central American region (Mexico, Honduras, and Colombia) and the Amazonian region (French Guiana, Guyana, and Venezuela). Genetic structure analyses also indicated the presence of an admixed cluster that included P. vivax populations from Brazil and Peru (Fig.…”

“…The analysis based on PCA, ancestry plots, ML phylogenetic tree, and population admixture graphs revealed a consistent genetic structure among the Latin American P. vivax populations within the Americas and as well as to P. vivax populations worldwide, as previously described [29,36,49]. On a worldwide scale, four distinct genetic clusters corresponding to different geographical regions were identified: (1) Oceania, East, and Southeast Asia; (2) Africa; (3) Middle East and South Asia; and (4) Latin America (Fig.…”