Abstract

Malaria parasites exhibit a complex lifecycle, requiring extensive asexual replication in the liver and blood of the vertebrate host, and in the haemocoel of the insect vector. Yet, they must also undergo a single round of sexual reproduction, which occurs in the vector’s midgut upon uptake of a blood meal. Sexual reproduction is obligate for infection of the vector and thus, is essential for onwards transmission to new hosts. Sex in malaria parasites involves several bottlenecks in parasite number, making the stages involved attractive targets for blocking disease transmission. Malaria parasites have evolved a suite of adaptations (“strategies”) to maximise the success of sexual reproduction and transmission, which could undermine transmission-blocking interventions. Yet, understanding parasite strategies may also reveal novel opportunities for such interventions. Here, we outline how evolutionary and ecological theories, developed to explain reproductive strategies in multicellular taxa, can be applied to explain two reproductive strategies (conversion rate and sex ratio) expressed by malaria parasites within the vertebrate host.

Highlights

  • For all agents of infection, denoted hereafter as parasites, transmission to new hosts equates to reproductive success, which is a major component of fitness

  • The requirement of different stages for within-host survival and betweenhost transmission means that malaria parasites face life history tradeoffs common to all sexually reproducing organisms: resources must be divided between growth/maintenance and reproduction [23,24]

  • The conversion rates of P. chabaudi observed across a gradient for state coupled with the consequences for the resulting dynamics of asexuals and gametocytes suggests that RR and TI affect short term survival within the host and between-host transmission po­ tential as predicted [17]

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Summary

Introduction

For all agents of infection (parasites, pathogens, microbes), denoted hereafter as parasites, transmission to new hosts equates to reproductive success, which is a major component of fitness. Asexual replication of malaria parasites within red blood cells (RBC, for a list of acronyms see Table 1) of vertebrate hosts (the “intraerythrocytic development cycle”, IDC) facilitates within-host sur­ vival and provides a source population to fuel the production of nonreplicating sexual stages (“gametocytes”) for transmission (Fig. 2). The requirement of different stages for within-host survival and betweenhost transmission means that malaria parasites face life history tradeoffs common to all sexually reproducing organisms: resources must be divided between growth/maintenance (i.e. asexual replication) and reproduction (i.e. production of gametocytes) [23,24]. The ability of malaria parasites to alter conversion rate during infections, and in response to changes in conditions inside the host, appears to maximise fitness, i.e. be adaptive (Table 2; predictably plastic parasites) [17,21,26]. Beyond sex allocation and conversion rate, reproductive strategies remain a black box in need of investigation

What is it?
What do parasites do and why?
How do parasites assess circumstances?
Does the theory apply to human malaria parasites?
Mechanisms underpinning plasticity in conversion rate and sex allocation
Adaptive value
Plasticity
Genetic variation
Pleiotropy
Evolution-proofing interventions
Ecological traps
Summary
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