Contrasting genomic epidemiology between sympatric Plasmodium falciparum and Plasmodium vivax populations

Philipp Schwabl, Flavia Camponovo, Collette Clementson, Angela M. Early, Margaret Laws, David A. Forero-Peña, Oscar Noya, María Eugenia Grillet, Mathieu Vanhove, Frank Anthony, Kashana James, Narine Singh, Horace Cox, Reza Niles-Robin, Caroline O. Buckee and Daniel E. Neafsey ()
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Philipp Schwabl: Harvard T.H. Chan School of Public Health
Flavia Camponovo: Harvard T.H. Chan School of Public Health
Collette Clementson: Ministry of Health
Angela M. Early: Broad Institute of MIT and Harvard
Margaret Laws: Harvard T.H. Chan School of Public Health
David A. Forero-Peña: Biomedical Research and Therapeutic Vaccines Institute
Oscar Noya: Central University of Venezuela
María Eugenia Grillet: Central University of Venezuela
Mathieu Vanhove: Harvard T.H. Chan School of Public Health
Frank Anthony: Ministry of Health
Kashana James: Ministry of Health
Narine Singh: Ministry of Health
Horace Cox: Ministry of Health
Reza Niles-Robin: Ministry of Health
Caroline O. Buckee: Harvard T.H. Chan School of Public Health
Daniel E. Neafsey: Harvard T.H. Chan School of Public Health

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract The malaria parasites Plasmodium falciparum and Plasmodium vivax differ in key biological processes and associated clinical effects, but consequences on population-level transmission dynamics are difficult to predict. This co-endemic malaria study from Guyana details important epidemiological contrasts between the species by coupling population genomics (1396 spatiotemporally matched parasite genomes, primarily from 2020–21) with sociodemographic analysis (nationwide patient census from 2019). We describe how P. falciparum forms large, interrelated subpopulations that sporadically expand but generally exhibit restrained dispersal, whereby spatial distance and patient travel statistics predict parasite identity-by-descent (IBD). Case bias towards working-age adults is also strongly pronounced. P. vivax exhibits 46% higher average nucleotide diversity (π) and 6.5x lower average IBD. It occupies a wider geographic range, without evidence for outbreak-like expansions, only microgeographic patterns of isolation-by-distance, and weaker case bias towards adults. Possible latency-relapse effects also manifest in various analyses. For example, 11.0% of patients diagnosed with P. vivax in Greater Georgetown report no recent travel to endemic zones, and P. vivax clones recur in 11 of 46 patients incidentally sampled twice during the study. Polyclonality rate is also 2.1x higher than in P. falciparum, does not trend positively with estimated incidence, and correlates uniquely to selected demographics. We discuss possible underlying mechanisms and implications for malaria control.

Date: 2024
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DOI: 10.1038/s41467-024-52545-6

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