Abstract

Background and objectivesPhenotypic plasticity enables organisms to maximize fitness by matching trait values to different environments. Such adaptive phenotypic plasticity is exhibited by parasites, which experience frequent environmental changes during their life cycle, between individual hosts and also in within-host conditions experienced during infections. Life history theory predicts that the evolution of adaptive phenotypic plasticity is limited by costs and constraints, but tests of these concepts are scarce.MethodologyHere, we induce phenotypic plasticity in malaria parasites to test whether mounting a plastic response to an environmental perturbation constrains subsequent plastic responses to further environmental change. Specifically, we perturb red blood cell resource availability to induce Plasmodium chabaudi to alter the trait values of several phenotypes underpinning within-host replication and between-host transmission. We then transfer parasites to unperturbed hosts to examine whether constraints govern the parasites’ ability to alter these phenotypes in response to their new in-host environment.ResultsParasites alter trait values in response to the within-host environment they are exposed to. We do not detect negative consequences, for within-host replication or between-host transmission, of previously mounting a plastic response to a perturbed within-host environment.Conclusions and implicationsWe suggest that malaria parasites are highly plastic and adapted to adjusting their phenotypes in response to the frequent changes in the within-host conditions they experience during infections. Our findings support the growing body of evidence that medical interventions, such as anti-parasite drugs, induce plastic responses that are adaptive and can facilitate the survival and potentially, drug resistance of parasites.Lay SummaryMalaria parasites have evolved flexible strategies to cope with the changing conditions they experience during infections. We show that using such flexible strategies does not impact upon the parasites’ ability to grow (resulting in disease symptoms) or transmit (spreading the disease).

Highlights

  • The ability to alter aspects of phenotype in response to changes in environmental conditions is commonly observed in multicellular organisms [1,2,3]

  • An alternative view is that parasites are confronted with frequent and fast changing within-host conditions during each infection, as well as variation in conditions experienced in different hosts

  • We compare the trait values of parasites—stemming from different types of initial hosts— in common garden hosts (ExControl vs ExPHZ), to test for effects of previous plasticity, i.e. the trait values adopted in initial hosts

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Summary

Introduction

The ability to alter aspects of phenotype in response to changes in environmental conditions (phenotypic plasticity) is commonly observed in multicellular organisms [1,2,3]. The trematode Coitocaecum parvum adopts a three-host or a two-host lifecycle depending on the availability of appropriate definitive hosts [9] Bacteriophages vary their lysis/lysogeny decision, and malaria parasites their sex ratio and reproductive effort, in response to co-infecting conspecific genotypes [10, 11]. Phenotypic plasticity enables organisms to maximize fitness by matching trait values to different environments Such adaptive phenotypic plasticity is exhibited by parasites, which experience frequent environmental changes during their life cycle, between individual hosts and in within-host conditions experienced during infections. Our findings support the growing body of evidence that medical interventions, such as anti-parasite drugs, induce plastic responses that are adaptive and can facilitate the survival and potentially, drug resistance of parasites

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