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Phenotypic Plasticity in Reproductive Effort: Malaria Parasites Respond to Resource Availability

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Phenotypic Plasticity in Reproductive Effort: Malaria Parasites Respond to Resource Availability

Philip L G Birget et al. Proc Biol Sci.

Abstract

The trade-off between survival and reproduction is fundamental in the life history of all sexually reproducing organisms. This includes malaria parasites, which rely on asexually replicating stages for within-host survival and on sexually reproducing stages (gametocytes) for between-host transmission. The proportion of asexual stages that form gametocytes (reproductive effort) varies during infections-i.e. is phenotypically plastic-in response to changes in a number of within-host factors, including anaemia. However, how the density and age structure of red blood cell (RBC) resources shape plasticity in reproductive effort and impacts upon parasite fitness is controversial. Here, we examine how and why the rodent malaria parasite Plasmodium chabaudi alters its reproductive effort in response to experimental perturbations of the density and age structure of RBCs. We show that all four of the genotypes studied increase reproductive effort when the proportion of RBCs that are immature is elevated during host anaemia, and that the responses of the genotypes differ. We propose that anaemia (counterintuitively) generates a resource-rich environment in which parasites can afford to allocate more energy to reproduction (i.e. transmission) and that anaemia also exposes genetic variation to selection. From an applied perspective, adaptive plasticity in parasite reproductive effort could explain the maintenance of genetic variation for virulence and why anaemia is often observed as a risk factor for transmission in human infections.

Keywords: gametocytes; genetic variation; life-history strategy; phenotypic plasticity; resource allocation trade-off; reticulocytes.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Cartoon of a reaction norm for conversion rate against conditions experienced by parasites inside the mammalian host, adapted from [6]. Importantly, the x-axis does not represent time since infection, but a given stress, or combination of stressors, experienced at any point during the infection that reduces the condition/state of parasites. The dotted line represents a decrease in conversion rate (‘restraint’) as the parasites experience a loss of condition/state, but the exact functional form of this is not known. If the within-host environment has deteriorated substantially and recovery of condition/state is unlikely or impossible parasites should make a terminal investment by putting all resources into transmission (‘escape’). Factors in the boxes denote circumstances thought to induce reproductive restraint or terminal investment, but the effect of variable red blood cell resources during anaemia is unclear. (Online version in colour.)
Figure 2.
Figure 2.
Mean ± standard error of the mean (SE) normocyte density (a) and reticulocyte density (b) on days 0–2 PI (n = 68) by PHZ treatment (0, 30, 120 mg kg−1) and genotype. Normocyte and reticulocyte densities are significantly different between PHZ treatments but not between genotypes. (Online version in colour.)
Figure 3.
Figure 3.
Reaction norms for conversion rate (mean ± SE gametocyte density for days 2 and 3 PI) of four genotypes across PHZ treatments (left to right along x-axis represents a decrease in total red blood cell density and an increase in reticulocyte proportion). All genotypes increase their conversion as PHZ dose increases, but to different extents (note, there is no significant difference between AJ and ER). The points are dodged horizontally for clarity. (Online version in colour.)
Figure 4.
Figure 4.
Gametocyte density for each mouse (mean of days 2 and 3 PI) correlates with RBC age structure (the mean proportion of RBCs that are reticulocytes across days 0, 1 and 2 PI for each mouse), and fitted lines illustrate the reaction norms for the different genotypes (note, there is no significant difference between AJ and ER). Data from the control group cluster around the origin (median reticulocyte frequency: 0.014), data from the 30 mg kg−1 group span a reticulocyte frequency from 0.06 to 0.19 (median 0.14), and a dose of 120 mg kg−1 produced a range between 0.21 and 0.29 (median 0.25). (Online version in colour.)

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