State-dependent parasitism by a facultative parasite of fruit flies

Abstract

Parasites can evolve phenotypically plastic strategies for transmission such that a single genotype can give rise to a range of phenotypes depending on the environmental condition. State-dependent plasticity in particular can arise from individual differences in the parasite's internal state or the condition of the host. Facultative parasites serve as ideal model systems for investigating state-dependent plasticity because individuals can exhibit two life history strategies (free-living or parasitic) depending on the environment. Here, we experimentally show that the ectoparasitic mite Macrocheles subbadius is more likely to parasitize a fruit fly host if the female mite is mated; furthermore, the propensity to infect increased with the level of starvation experienced by the mite. Host condition also played an important role; hosts infected with moderate mite loads were more likely to gain additional infections in pairwise choice tests than uninfected flies. We also found that mites preferentially infected flies subjected to mechanical injury over uninjured flies. These results suggest that a facultative parasite's propensity to infect a host (i.e. switch from a free-living strategy) depends on both the parasite's internal state and host condition. Parasites often live in highly variable and changing environments, an infection strategy that is plastic is likely to be adaptive.

Experimental evolution of infectious behaviour in a facultative ectoparasite

“…So how is facultative parasitism maintained in nature? Facultative parasitism can be viewed as a phenotypically plastic strategy whereby the expression of infectious traits depends on the environmental condition (Farish and Axtell 1971; Reece et al, 2009;Luong et al, 2017). Yet, the fixation of any infectious strategy could mean a reduction in infection plasticity, which could limit an organism's ability to respond rapidly to changes in highly ephemeral and variable habitats.…”

Phenotypic plasticity more essential to maintaining variation in host-attachment behaviour than evolutionary trade-offs in a facultatively parasitic mite

“…The prevalence of fly attachment in selected and control lines was recorded over three environments, each with varying levels of food (no food, low food and high food). Populations of a closely related mite species, Macrocheles subbadius , exhibit increased attachment prevalence when starved (Luong et al ., 2017). We assumed food availability to be a key component of habitat quality and that habitat quality diminishes with lower food availability.…”

“…observation). Their attachment behaviour is plastic and influenced by their own internal state (Jalil and Rodriguez, 1970; Luong et al ., 2017), the state of their potential hosts (Farish and Axtell, 1971; Campbell and Luong, 2016; Luong et al ., 2017) as well as the external environment (Farish and Axtell, 1971; Durkin and Luong, 2018).…”

Facultative parasites as evolutionary stepping-stones towards parasitic lifestyles

“…reproductive status and injury), host availability and parasite condition (e.g. level of starvation) [10]. The conditions favouring the evolution of facultative parasitism appear to be met frequently, as facultative parasitism has been reported in a range of taxonomic groups [9][10][11][12][13].…”