Chance or choice? Understanding parasite selection and infection in multi-host communities

Abstract

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, largevolume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological 'sinks' or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.

Community disassembly and disease: realistic—but not randomized—biodiversity losses enhance parasite transmission

“…ondatrae preferentially select Ra. catesbeiana larvae in choice trials, despite its overall low susceptibility to infection [48]. Similar 'identity effects' for particular species in diluting infection among focal hosts has also been demonstrated for other disease systems (e.g.…”

Experimental evidence that host choice by parasites is age-dependent in a fish-monogenean system

“…Host age is expected to affect host susceptibility and resistance to parasites (Sackett et at. 2018;Ashby and Bruns 2018;Johnson et al 2019;Izhar et al 2020). Through experimental evidence, our study suggests that variation in host age can drive parasite choice, leading to fundamental differences in parasite burdens among host individuals.…”

“…Host age is among the most important and heterogeneous trait driving parasite infections (Woolhouse 1998; Ben-Ami 2019). For example, juveniles or young adults can be more susceptible to infections than old adults (Izhar & Ben-Ami 2015;Ashby and Bruns 2018), which may lead to differences in exposure to parasites (Poulin 2007) and ultimately determine parasite preference/choice (Johnson et al 2019). However, previous studies have shown that older adults are also larger bodied hosts and thus might harbour higher parasite species richness (Kamiya et al 2014;Bolnick et al 2020) and abundance (Poulin 2013).…”

Towards a mechanistic understanding of competence: a missing link in diversity–disease research

“…These fundamental processes are infection , parasite development and pre-transmission survival and together encompass an organism's capacity to transmit infection (Box 1). Exposure should be treated as distinct from competence, because it can be influenced by movements, behaviours and interactions of multiple players in an ecological community, as well as parasite choice (Johnson et al ., 2019 a ) or vector selectivity (Kilpatrick et al ., 2006). Likewise, infectivity (the likelihood of transmission from donor to recipient) depends on the behaviour and susceptibility of a recipient host or vector outside of the host–parasite interaction, so should not be treated as a component of competence.…”

“…On the parasite's side, Ebert (1994) demonstrated that the ability of microsporidians to infect and reproduce within Daphnia decreases as a function of geographic distance between host genotype and parasite genotype. An added dimension to parasite adaptation is parasite choice (Johnson et al ., 2019 a ), which may evolve to strengthen or relax host–parasite encounter rates beyond those expected by density- and frequency-dependent processes alone. As hosts vary in frequency and quality over the landscape, their importance for parasite transmission may also vary, and the potential for local adaptation may make competence an evolutionary dynamic property.…”