Parasitic nematodes simultaneously suppress and benefit from coccidian coinfection in their natural mouse host.

Melanie Clerc,Amy B Pedersen,Andy Fenton,Simon A Babayan

doi:10.1017/s0031182019000192

Abstract

Within-host interactions among coinfecting parasites are common and have important consequences for host health and disease dynamics. However, these within-host interactions have traditionally been studied in laboratory mouse models, which often exclude important variation and use unnatural host-parasite combinations. Conversely, the few wild studies of within-host interactions often lack knowledge of parasite exposure and infection history. Here we exposed laboratory-reared wood mice (Apodemus sylvaticus) that were derived from wild-caught animals to two naturally-occurring parasites (nematode: Heligmosomoides polygyrus, coccidia: Eimeria hungaryensis) to investigate the impact of coinfection on parasite infection dynamics, and to determine if the host immune response mediates this interaction. Coinfection led to delayed worm expulsion and prolonged egg shedding in H. polygyrus infections and lower peak E. hungaryensis oocyst burdens. By comparing antibody levels between wild and colony-housed mice, we also found that wild mice had elevated H. polygyrus-IgG1 titres even if currently uninfected with H. polygyrus. Using this unique wild-laboratory system, we demonstrate, for the first time, clear evidence for a reciprocal interaction between these intestinal parasites, and that there is a great discrepancy between antibody levels measured in the wild vs those measured under controlled laboratory conditions in relation to parasite infection and coinfection.

Highlights

Individuals in their natural environment can be exposed to and infected with a multitude of parasites, either sequentially or simultaneously (Pedersen and Fenton, 2007; Telfer et al, 2008), which can lead to within-host interactions between parasite species (Graham, 2008; Seabloom et al, 2015)
While the titre of H. polygyrus-specific IgG1 changed over time, there was no difference in the dynamics of H. polygyrus-specific IgG1, or in the final amount of H. polygyrusspecific IgG1 at the end of the experiment between the H. polygyrus-only and the coinfected mice (Fig. 5A, Table 3)
By using the offspring of originally wild-derived wood mice and their naturally co-evolved parasites H. polygyrus and E. hungaryensis, we were able to demonstrate the impact of coinfection on the infection dynamics of both interacting parasites, as well as total and parasite-specific antibodies in a controlled environment

Summary

Introduction

Individuals in their natural environment can be exposed to and infected with a multitude of parasites, either sequentially or simultaneously (Pedersen and Fenton, 2007; Telfer et al, 2008), which can lead to within-host interactions between parasite species (Graham, 2008; Seabloom et al, 2015). As a result of the often unrealistic conditions used in laboratory studies, and the accompanying difficulty in translating these results to the real world, researchers have begun to investigate the underlying mechanisms of parasite within-host interactions in natural environments These studies have helped unravel the natural conditions under which parasites interact and importantly what factors determine the impacts of these interactions on host health and disease (Ezenwa et al, 2010; Ezenwa and Jolles, 2011; Turner et al, 2011; Friberg et al, 2013; Knowles et al, 2013; Pedersen and Antonovics, 2013). These studies are not without limitations, as both the exposure and infection history of wild

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