Constant rate of Plasmodium falciparum sexual commitment promotes variable gametocyte proportions as infection progresses over time

In areas of seasonal malaria, resuming transmission every wet season relies on persistent asexual parasites during dry season that maintain the ability to produce gametocytes until the mosquito population resurges, following the start of annual rains. Although human asymptomatic P. falciparum reservoirs in the dry season are widely recognized, the longitudinal dynamics of parasite sexual commitment and gametocytogenesis are unclear. Here, we compared the density and proportion of P. falciparum gametocytes in blood of asymptomatic subjects during the dry season versus subjects with symptomatic malaria in the wet season. Blood concentrations of phospholipids potentially involved in gametocytogenesis and parasite transcriptomes were also compared. While blood densities of gametocytes and asexual parasites were lower during the dry season, we found that gametocytes were proportionally higher during the dry versus wet season. Levels of parasite transcripts involved in sexual commitment were similar throughout the year, and phospholipid content in the plasma throughout the year did not affect sexual commitment in vitro. We demonstrate experimentally and through mathematical modelling that gametocyte density and proportion diverge as infections progress from recently transmitted to chronic carriage, without significant alterations in the rate of sexual commitment over time.