Introduction
Parasitic infection in wild populations is ubiquitous, and coinfection with multiple parasite species is the norm. There has been a recent effort to explore within-host parasite communities through an ecological lens, rather than treating infections as isolated phenomena (Cattadori, Boag, & Hudson, 2008; A L Graham, 2008; Johnson, De Roode, & Fenton, 2015; Pedersen & Fenton, 2007; Seabloom et al., 2015). Predicting how parasite species will interact in individuals and populations coinfected with multiple species is difficult, and accounting for infection by ectoparasites, protozoan and helminth endoparasites, bacteria and viruses poses a significant challenge for disease ecologists. Different parasite guilds (here distinguished by size, life-cycle and niche as helminth macroparasites, single-celled microparasites and helminth macroparasites) impact their hosts in a variety of ways, causing qualitatively diverse types of immune responses e.g. Th1/2 immune polarisation in response to intracellular parasites and helminth macroparasites respectively(Jankovic, Sher, & Yap, 2001), and varying levels of pathology, from asymptomatic infections that approach commensalism, to more severe infections that cause morbidity or mortality. Understanding interactions between parasite species in coinfected hosts and populations is essential for understanding and predicting associated outcomes in the host. Laboratory infection models are useful in demonstrating the influence of coinfection upon the course of infection and the role of host immunity. However, only recently have studies of wild populations begun to explore multi-species parasite communities incorporating multiple parasite types in naturally infected animals (Dallas, Laine, & Ovaskainen, 2019; S Telfer et al., 2010).
Parasites alter the environment within their host in a variety of ways, and these changes can influence the course of other infections. Interactions between parasite species can be mediated both through changes in a host’s immune state (Chen, Louie, McCormick, Walker, & Shi, 2005; Andrea L Graham, Lamb, Read, & Allen, 2005; Su, Segura, Morgan, Loredo-Osti, & Stevenson, 2005), through direct ecological processes such as niche competition(Balmer, Stearns, Schötzau, & Brun, 2009; Bashey, 2015; Stancampiano, Gras, & Poglayen, 2010), or through a combination of these processes (A L Graham, 2008). They may also change between stages of a parasite’s life cycle, due to changes in immune response and the niches exploited within the host (Duncan et al., 2012).
While the importance of parasite community structure in coinfected wild animals is increasingly well understood, coinfection studies have typically focussed on within-guild interactions (Lello, Boag, Fenton, Stevenson, & Hudson, 2004; Lutermann, Fagir, & Bennett, 2015; Sandra Telfer et al., 2010), or on specific pairwise interactions between species of different guilds (Brettschneider, Anguelov, Chimimba, & Bastos, 2012; Ferrari, Cattadori, Rizzoli, & Hudson, 2009; Knowles, Palinauskas, & Sheldon, 2010; Legesse, Erko, & Balcha, 2004; Nacher et al., 2002). Mutualist and competitive interactions between species pairs observed in wild populations include interactions between microparasites (Taylor et al., 2018), and between microparasites and helminths (Ezenwa, Etienne, Luikart, Beja‐Pereira, & Jolles, 2010). Networks of positive and negative cross-species interactions have been observed in microparasites infecting wild field voles, Microtus agrestis(Sandra Telfer et al., 2010), and lions, Panthera leo(Fountain-Jones et al., 2019), in helminth communities of wild rabbits,Oryctolagus cuniculus (Lello et al., 2004), and in arthropod ectoparasite communities infecting wild sengis, Elephantulus myurus (Lutermann et al., 2015).
Cross-guild parasite communities have been more recently explored in wild populations of non-model species. Parasites of 22 rodent species in the Sonoran desert were shown to associate across tissue types and guilds, with the majority of associations being positive (Dallas et al., 2019). Here, negative associations were most commonly found between parasites which shared a physical niche, indicating that while positive associations may be governed by the state of the host, or overlap in transmission methods or distribution, negative associations primarily result from localised competition.
New bovine tuberculosis infections in wild African buffalo (Syncerus caffer ) were found to shift cross-guild communities of parasites within the hosts, increasing taxonomic richness of parasite assemblages, shifting the overall taxonomic position and favouring parasites with specific functional traits (Beechler et al., 2019). These examples illustrate the importance of considering individual infections within a context of multi-parasites ecosystems. Characterising cross-guild interact networks in a wild population of a model species will allow our understanding of these associations to be more directly related to and informed by analogous co-infection studies performed in controlled laboratory settings.
Working towards holistic models which account for as broad a range of infections as possible will improve our understanding of parasite communities, and the factors affecting distribution of individual infections, and performing these assessments in model species will allow us to more easily connect this research to related laboratory studies. Here we use cross-sectional parasitological survey data from a wild population of the house mouse (Mus musculus domesticus ) to explore associations among prevalence and intensity of infections from a broad range of infections, establish a network of positive and negative associations involving every observed parasite, and discuss potential mechanisms underlying these associations.