Abstract

A major challenge in disease ecology is to understand how co‐infecting parasite species interact. We manipulate in vivo resources and immunity to explain interactions between two rodent malaria parasites, Plasmodium chabaudi and P. yoelii. These species have analogous resource‐use strategies to the human parasites Plasmodium falciparum and P. vivax: P. chabaudi and P. falciparum infect red blood cells (RBC) of all ages (RBC generalist); P. yoelii and P. vivax preferentially infect young RBCs (RBC specialist). We find that: (1) recent infection with the RBC generalist facilitates the RBC specialist (P. yoelii density is enhanced ~10 fold). This occurs because the RBC generalist increases availability of the RBC specialist's preferred resource; (2) co‐infections with the RBC generalist and RBC specialist are highly virulent; (3) and the presence of an RBC generalist in a host population can increase the prevalence of an RBC specialist. Thus, we show that resources shape how parasite species interact and have epidemiological consequences.

Highlights

  • Mixed-species infections are common and interactions between co-infecting species can either promote or inhibit other parasite species in the same host (Graham 2008; Griffiths et al 2014)

  • When P. yoelii parasites were inoculated into a within-host environment that had already been altered by P. chabaudi infection, they reached significantly higher densities than in either control infections or simultaneous mixed infections (PIA vs. control; z = 2.9, P = 0.01; Parasite-Induced Anaemia (PIA) vs. Mixed infection (MI); z = 2.98, P = 0.01; Fig. 2a; Table S2)

  • On the day of infection, mice simultaneously receiving P. yoelii and P. chabaudi (MI treatment group) did not differ significantly from control mice in either resources or immunity (RBC density: z = 0.51, P = 0.99; reticulocyte density: z = 0.21, P = 0.99; proportion of reticulocytes: z = 0.12, P = 0.99; P. yoelii antibodies: treatment, F = 2.15, P = 0.09; P. chabaudi antibodies: z = 0.44, P = 0.99; Table S1; Fig. 2). These results suggest that the facilitation observed in the PIA group is mediated by host anaemia resulting in increased production of reticulocytes (Mcqueen & Mckenzie 2006)

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Summary

Introduction

Mixed-species infections are common and interactions between co-infecting species can either promote or inhibit other parasite species in the same host (Graham 2008; Griffiths et al 2014). These interactions affect disease severity, parasite fitness and the prevalence and distribution of parasite species in a host population (Ferrari et al 2009; Knowles et al 2013; Pedersen & Antonovics 2013; Viney & Graham 2013). Co-infecting parasite species can interact with one another directly or, more commonly, through changing the within-host environment (Mideo 2009). Determining how interactions between co-infecting parasite species shape infection dynamics, virulence and transmission are major questions in disease ecology

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