Evolution of plastic transmission strategies in avian malaria.

Stéphane Cornet,Antoine Nicot,Sylvain Gandon,Ana Rivero,Kenneth D. Vernick

doi:10.1371/journal.ppat.1004308

Abstract

Malaria parasites have been shown to adjust their life history traits to changing environmental conditions. Parasite relapses and recrudescences—marked increases in blood parasite numbers following a period when the parasite was either absent or present at very low levels in the blood, respectively—are expected to be part of such adaptive plastic strategies. Here, we first present a theoretical model that analyses the evolution of transmission strategies in fluctuating seasonal environments and we show that relapses may be adaptive if they are concomitant with the presence of mosquitoes in the vicinity of the host. We then experimentally test the hypothesis that Plasmodium parasites can respond to the presence of vectors. For this purpose, we repeatedly exposed birds infected by the avian malaria parasite Plasmodium relictum to the bites of uninfected females of its natural vector, the mosquito Culex pipiens, at three different stages of the infection: acute (∼34 days post infection), early chronic (∼122 dpi) and late chronic (∼291 dpi). We show that: (i) mosquito-exposed birds have significantly higher blood parasitaemia than control unexposed birds during the chronic stages of the infection and that (ii) this translates into significantly higher infection prevalence in the mosquito. Our results demonstrate the ability of Plasmodium relictum to maximize their transmission by adopting plastic life history strategies in response to the availability of insect vectors.

Highlights

All organisms experience some level of temporal variation in the quality of their environment
Twenty birds experimentally inoculated with avian malaria parasite Plasmodium relictum were followed for over 300 days post-infection to monitor the variation in blood parasitaemia
Theory How do malaria parasites adapt to the density fluctuations of their insect vectors? To answer this question we started by studying the evolution of transmission strategies using a classical epidemiological model for a vector-borne pathogen

Summary

Introduction

All organisms experience some level of temporal variation in the quality of their environment. In response to these variations, many species have evolved specific strategies that allow them to limit or shut down growth and development until the conditions improve [1]. Several viruses (e.g. lambdoid phages, herpesviruses) have evolved the ability to integrate their host genome and enter a latent phase during which within-host replication is shut down, the infection is asymptomatic and transmission is very limited [4,5]. The evolution of latent life cycle in pathogens may be viewed as an adaptation to temporal variations of the availability of susceptible hosts

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