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.