Evolutionary history of Plasmodium vivax and Plasmodium simium in the Americas

Rougeron, Virginie; Daron, Josquin; Fontaine, Michaël C.; Prugnolle, Franck

doi:10.1186/s12936-022-04132-7

Cited by 7 publications

(8 citation statements)

References 67 publications

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“…This pattern of low-local but relatively high-regional genetic diversity has been described previously using microsatellites [45] and is likely caused by the effect of random genetic drift in small populations that remain relatively isolated from each other, where rare alleles disappear (decreased local diversity translated in a reduction of He, and high relatedness IBD), while differentiation between sites increases. In contrast, in peri-urban communities close to Iquitos, the regional capital, a relatively high genetic diversity is observed with connectivity within and between districts, and a temporal drift of the parasite population, in concordance with previous reports [19, 46].…”

Section: Discussionsupporting

confidence: 91%

“…Other regions in Peru, such Amazonas region (next to Loreto) or the Northern Coast, were not included in this initial study and more work is needed to fully characterize the full P. vivax population in Peru, especially considering the observed low local, but high regional diversity. However, compared to other previous studies, we included more districts and remote areas spanning a larger period [19–21]. To assess the full diversity of Peruvian parasites, a more systematic sampling approach, possibly linked with NMCP and/or NMEP activities is needed.…”

Section: Discussionmentioning

confidence: 99%

“…Through genomic analyses, the P. vivax parasite population of Latin America has been described as a distinct population from the rest of the world, presenting relatively lower genetic diversity due to relatively recent introductions in the region [16–18]. In the case of the Peruvian Amazon, Iquitos city acts as a source from where parasites spread to other areas through human mobility related to socio-economic activities [19, 20]. Additionally, there is substantial gene flow between parasite populations from geographically distant areas in the region [21].…”

Section: Introductionmentioning

confidence: 99%

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Plasmodium vivaxgenomic surveillance in the Peruvian Amazon with Pv AmpliSeq assay

Kattenberg,

Cabrera-Sosa,

Figueroa-Idelfonso

et al. 2023

Preprint

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BackgroundPlasmodium vivaxis the most predominant malaria species in Latin America, constituting 71.5% of malaria cases in 2021. With several countries aiming for malaria elimination, it is crucial to prioritize effectiveness of national control programs by optimizing the utilization of available resources and strategically implementing necessary changes. To support this, there is a need for innovative approaches such as genomic surveillance tools that can investigate changes in transmission intensity, imported cases and sources of reintroduction, and can detect molecular markers associated with drug resistance.Methodology/Principal FindingsHere, we apply a modified highly-multiplexed deep sequencing assay: Pv AmpliSeq v2 Peru. The tool targets a newly developed 41-SNP Peru barcode for parasite population analysis within Peru, the 33-SNP vivaxGEN-geo panel for country-level classification, and 11 putative drug resistance genes. It was applied to 230 samples from the Peruvian Amazon (2007 – 2020), generating baseline surveillance data. We observed a heterogenousP. vivaxpopulation with high diversity and gene flow in peri-urban areas of Maynas province (Loreto region) with a temporal drift. In comparison, in an indigenous isolated area, the parasite population was genetically differentiated (FST=0.07-0.09) with moderate diversity and high relatedness between isolates in the community. In a remote border community, a clonalP. vivaxcluster was identified, with distinct haplotypes in drug resistant genes andama1, more similar to Brazilian isolates, likely representing an introduction ofP. vivaxfrom Brazil at that time. To test its applicability for Latin America, we evaluated the SNP Peru barcode inP. vivaxgenomes from the region and demonstrated the capacity to capture local population clustering at within-country level.Conclusions/SignificanceTogether this data shows thatP. vivaxtransmission is heterogeneous in different settings within the Peruvian Amazon. Genetic analysis is a key component for regional malaria control, offering valuable insights that should be incorporated into routine surveillance.Author SummaryLatin America is aiming towards malaria elimination. Genomic surveillance is crucial for a country’s malaria strategy, aiding in understanding and stopping the spread of the disease. While widely used for another malaria species (Plasmodium falciparum), limited tools exist for trackingP. vivax, a significant player in malaria-endemic areas outside of Africa, and the primary cause of malaria in Latin America.In this study, we used a new tool, Pv AmpliSeq v2 Peru assay, to examine the genetic makeup of malaria parasites in the Peruvian Amazon. This tool helps us see how the parasites from different areas are connected and tracks markers that could indicate resistance to drugs. We found that the parasites from remote areas in the Amazon were genetically different from parasites in areas surrounding the main city of Iquitos, and parasites in a remote border community were genetically more similar to Brazilian parasites.We also show that the Pv AmpliSeq v2 Peru assay can be used to study parasites from other countries in Latin America, highlighting the broader application in the region. Considering that parasites are not constrained by borders and can easily spread between neighboring countries, a regional approach can be crucial for malaria elimination.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Plasmodium vivaxgenomic surveillance in the Peruvian Amazon with Pv AmpliSeq assay

Kattenberg,

Cabrera-Sosa,

Figueroa-Idelfonso

et al. 2023

Preprint

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“…parasite species in this region, potentially through multiple waves of human migrations (Rodrigues et al, 2018;Rougeron et al, 2022;Steverding, 2020;van Dorp et al, 2020). In addition, a lower transmission intensity in LAM compared to other regions in the world can contribute to the lower diversity (Neafsey et al, 2012(Neafsey et al, , 2021.…”

Section: Discussionmentioning

confidence: 99%

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

Kattenberg,

Monsieurs,

De Meyer

et al. 2024

Ecology and Evolution

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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.

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“…Understanding the genetic basis of P. vivax colonization success in the Americas is crucial for developing effective control strategies and predicting invasions of other regions. Yet, the current literature lacks comprehensive insights into this aspect [71], highlighting the need of more studies in this field.…”

Section: Discussionmentioning

confidence: 99%

Genomic exploration of the complex journey ofPlasmodium vivaxin Latin America

Lefebvre,

Degrugillier,

Arnathau

et al. 2024

Preprint

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Plasmodium vivax, the predominant malaria parasite in Latin America, has a rich and complex colonization history in the region, with debated hypotheses about its origin. Our study employed cutting-edge population genomic techniques, to collect whole genome sequencing data from 620P. vivaxisolates, including 107 newly sequenced samples, thus representing nearly all potential source populations worldwide. Analyses of the genetic structure, diversity, ancestry, and also, coalescent-based inferences and scenario testing using Approximate Bayesian Computation, have revealed a more complex evolutionary history than previously envisioned. Indeed, according to our analysis, the current AmericanP. vivaxpopulations predominantly stemmed from a now-extinct European lineage, with the potential contribution also from unsampled populations, most likely of West African origin, during post-colonial human migration waves in the late 19th-century. This study provides a fresh perspective onP. vivaxintricate evolutionary journey and brings insights into the possible contribution of West AfricanP. vivaxpopulations to the colonization history of Latin America.

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Evolutionary history of Plasmodium vivax and Plasmodium simium in the Americas

Cited by 7 publications

References 67 publications

Plasmodium vivaxgenomic surveillance in the Peruvian Amazon with Pv AmpliSeq assay

Plasmodium vivaxgenomic surveillance in the Peruvian Amazon with Pv AmpliSeq assay

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

Genomic exploration of the complex journey ofPlasmodium vivaxin Latin America

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