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Information Use and Plasticity in the Reproductive Decisions of Malaria Parasites

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Information Use and Plasticity in the Reproductive Decisions of Malaria Parasites

Lucy M Carter et al. Malar J.

Abstract

Background: Investment in the production of transmissible stages (gametocytes) and their sex ratio are malaria parasite traits that underpin mosquito infectivity and are therefore central to epidemiology. Malaria parasites adjust their levels of investment into gametocytes and sex ratio in response to changes in the in-host environment (including red blood cell resource availability, host immune responses, competition from con-specific genotypes in mixed infections, and drug treatment). This plasticity appears to be adaptive (strategic) because parasites prioritize investment (in sexual versus asexual stages and male versus female stages) in manners predicted to maximize fitness. However, the information, or 'cues' that parasites use to detect environmental changes and make appropriate decisions about investment into gametocytes and their sex ratio are unknown.

Methods: Single genotype Plasmodium chabaudi infections were exposed to 'cue' treatments consisting of intact or lysed uninfected red blood cells, lysed parasitized RBCs of the same clone or an unrelated clone, and an unmanipulated control. Infection dynamics (proportion of reticulocytes, red blood cell and asexual stage parasite densities) were monitored, and changes in gametocyte investment and sex ratio in response to cue treatments, applied either pre- or post-peak of infection were examined.

Results and conclusions: A significant reduction in gametocyte density was observed in response to the presence of lysed parasite material and a borderline significant increase in sex ratio (proportion of male gametocytes) upon exposure to lysed red blood cells (both uninfected and infected) was observed. Furthermore, the changes in gametocyte density and sex ratio in response to these cues depend on the age of infection. Demonstrating that variation in gametocyte investment and sex ratio observed during infections are a result of parasite strategies (rather than the footprint of host physiology), provides a foundation to investigate the fitness consequences of plasticity and explore whether drugs could be developed to trick parasites into making suboptimal decisions.

Figures

Figure 1
Figure 1
Plasmodium chabaudi AJ gametocyte density dynamics. (± SEM) from the day of administration of five cue treatments: C: control, U: uninfected RBCs, UL: uninfected lysed RBCs, AJ: AJ infected lysed RBCs and ER: ER infected lysed RBCs). Grey bars indicate the days when cues were administered - on day 4 PI for cohort 1 (left) and day 10 PI for cohort 2 (right) (A); cumulative gametocyte densities (± SEM) for three days post treatment with cues containing parasitized material (P: AJ, ER) or non-parasitized material (NP: C, U, UL) for cohort 1 (left) and for cohort 2 (right: where gametocyte density was significantly lower in the P group than NP group) (B); cumulative gametocyte densities (± SEM) for three days post treatment with either lysed RBC material (L: UL, AJ, ER) or non-lysed material (NL: C, U) for cohort 1 (left) and cohort 2 (right) (C).
Figure 2
Figure 2
Plasmodium chabaudi AJ sex ratio (proportion of male gametocytes) dynamics. (± SEM) from the day of administration of five cue treatments: C: control, U: uninfected RBCs, UL: uninfected lysed RBCs, AJ: AJ-infected lysed RBCs and ER: ER-infected lysed RBCs. Grey bars indicate the days when cues were administered - on day 4 PI for cohort 1 (left) and day 10 PI for cohort 2 (right) (A); mean sex ratio (± SEM) for three days post treatment with cues containing parasitized material (P: AJ, ER) or non-parasitized material (NP: C, U, UL) for cohort 1 (left) and cohort 2 (right) (B); mean sex ratio (± SEM) for three days post treatment with either lysed RBC material (L: UL, AJ, ER) or non-lysed material (NL: C, U) for cohort 1 (left: where sex ratio was significantly (borderline) higher in the lysed group), and for cohort 2 (right) (C).

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