Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes

Abstract

BackgroundEntomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remain elusive. EPN infective juveniles (IJs) actively search for hosts to infect using a diverse array of host-emitted odorants. Here we investigate whether their host-seeking behavior is subject to context-dependent modulation.ResultsWe find that EPN IJs exhibit extreme plasticity of olfactory behavior as a function of cultivation temperature. Many odorants that are attractive for IJs grown at lower temperatures are repulsive for IJs grown at higher temperatures and vice versa. Temperature-induced changes in olfactory preferences occur gradually over the course of days to weeks and are reversible. Similar changes in olfactory behavior occur in some EPNs as a function of IJ age. EPNs also show temperature-dependent changes in their host-seeking strategy: IJs cultured at lower temperatures appear to more actively cruise for hosts than IJs cultured at higher temperatures. Furthermore, we find that the skin-penetrating rat parasite Strongyloides ratti also shows temperature-dependent changes in olfactory behavior, demonstrating that such changes occur in mammalian-parasitic nematodes.ConclusionsIJs are developmentally arrested and long-lived, often surviving in the environment through multiple seasonal temperature changes. Temperature-dependent modulation of behavior may enable IJs to optimize host seeking in response to changing environmental conditions, and may play a previously unrecognized role in shaping the interactions of both beneficial and harmful parasitic nematodes with their hosts.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0259-0) contains supplementary material, which is available to authorized users.

Olfactory circuits and behaviors of nematodes

“…C. The response of Ste. scapterisci IJs to CO 2 shifts from repulsion to attraction as the IJs age [90]. IJs were tested in a 1 hr chemotaxis assay with 1% CO 2 .…”

“…For example, both EPN IJs and skin-penetrating IJs exhibit temperature-dependent olfactory plasticity: culturing IJs at different temperatures changes their odor preferences [90]. In the case of the EPN Steinernema carpocapsae , the response to 80% of the tested odorants changed as a function of their previous cultivation temperature.…”

“…IJs are long-lived and can survive in the soil through multiple seasons. The volatiles emitted by both animals and plants change seasonally, and thus temperature-dependent modulation of olfactory behavior may enable IJs to locate hosts despite seasonal changes in volatile emissions [90]. …”

“…Some parasitic nematodes also show age-dependent changes in their olfactory preferences [90]. For example, the EPN Steinernema scapterisci is initially repelled by CO 2 but becomes attracted to CO 2 as the IJs age (Figure 2C).…”

“…For example, the EPN Steinernema scapterisci is initially repelled by CO 2 but becomes attracted to CO 2 as the IJs age (Figure 2C). This change in CO 2 -evoked behavior may reflect a change in host-seeking strategy: CO 2 avoidance by younger IJs may cause them to disperse into the environment in search of new host niches with more available resources (a high cost but potentially high reward behavior), whereas CO 2 attraction by older IJs may cause them to remain in the proximity of existing host niches (a low cost but lower reward behavior) [90]. …”