Plasticity and genetic variation in traits underpinning asexual replication of the rodent malaria parasite, Plasmodium chabaudi

Abstract

Background: The ability of malaria (Plasmodium) parasites to adjust investment into sexual transmission stages versus asexually replicating stages is well known, but plasticity in other traits underpinning the replication rate of asexual stages in the blood has received less attention. Such traits include burst size (the number of merozoites produced per schizont), the duration of the asexual cycle, and invasion preference for different ages of red blood cell (RBC).

Methods: Here, plasticity [environment (E) effects] and genetic variation [genotype (G) effects] in traits relating to asexual replication rate are examined for 4 genotypes of the rodent malaria parasite Plasmodium chabaudi. An experiment tested whether asexual dynamics differ between parasites infecting control versus anaemic hosts, and whether variation in replication rate can be explained by differences in burst size, asexual cycle, and invasion rates.

Results: The within-host environment affected each trait to different extents but generally had similar impacts across genotypes. The dynamics of asexual densities exhibited a genotype by environment effect (G×E), in which one of the genotypes increased replication rate more than the others in anaemic hosts. Burst size and cycle duration varied between the genotypes (G), while burst size increased and cycle duration became longer in anaemic hosts (E). Variation in invasion rates of differently aged RBCs was not explained by environmental or genetic effects. Plasticity in burst size and genotype are the only traits making significant contributions to the increase in asexual densities observed in anaemic hosts, together explaining 46.4% of the variation in replication rate.

Conclusions: That host anaemia induces several species of malaria parasites to alter conversion rate is well documented. Here, previously unknown plasticity in other traits underpinning asexual replication is revealed. These findings contribute to mounting evidence that malaria parasites deploy a suite of sophisticated strategies to maximize fitness by coping with, or exploiting the opportunities provided by, the variable within-host conditions experienced during infections. That genetic variation and genotype by environment interactions also shape these traits highlights their evolutionary potential. Asexual replication rate is a major determinant of virulence and so, understanding the evolution of virulence requires knowledge of the ecological (within-host environment) and genetic drivers of variation among parasites.

Keywords: Anaemia; Cycle duration; Genotype by environment; G×E; In-host survival; Life history trait; Phenotypic plasticity; Red blood cell preference; Virulence.

Fig. 1

The difference in RBC environments between control (grey) and PHZ-treated (blue) hosts on the day before infection. For a total RBC density and b the proportions of RBC that are reticulocytes (box plot featured here and throughout present the median, interquartile range, and outliers). The difference in RBC environments between control and PHZ-treated hosts during infections for c RBC density (mean ± SEM) and d proportion of reticulocytes for each genotype (AJ: solid line + round point, AS: dashed line + triangle point, CR: dotted line + square point, ER: dot-dash line + cross point, mean ± SEM)

Fig. 2

Mean (± SEM) daily asexual parasite density for each genotype in naïve control (grey) and PHZ-treated hosts (blue), for genotypes a AJ, b AS, c CR, and d ER

Fig. 3

Burst size a, and asexual cycle duration b, for each genotype in naïve control (grey) and PHZ-treated hosts (blue). The dotted line in b marks a cycle duration of 24 h

Fig. 4

Invasion rates of normocytes (mature RBC, green) and reticulocytes (immature RBC, orange). For a all genotypes and b for different PHZ treatments (all genotypes combined). The rate reflects the probability of contact and successful invasion between uninfected cells and merozoites