A Sensory Code for Host Seeking in Parasitic Nematodes

Abstract

Summary Nematodes comprise a large phylum of both free-living and parasitic species that show remarkably diverse lifestyles, ecological niches, and behavioral repertoires. Parasitic species in particular often display highly specialized host-seeking behaviors that reflect their specific host preferences. Many host-seeking behaviors can be triggered by the presence of host odors, yet little is known about either the specific olfactory cues that trigger these behaviors or the neural circuits that underlie them. Heterorhabditis bacteriophora and Steinernema carpocapsae are phylogenetically distant insect-parasitic nematodes whose host-seeking and host-invasion behavior resembles that of some of the most devastating human- and plant-parasitic nematodes. Here we compare the olfactory responses of H. bacteriophora and S. carpocapsae infective juveniles (IJs) to those of Caenorhabditis elegans dauers, which are analogous life stages [1]. We show that the broad host range of these parasites results from their ability to respond to the universally-produced signal carbon dioxide (CO2) as well as a wide array of odors, including host-specific odors that we identified using TD-GC-MS. We show that CO2 is attractive for the parasitic IJs and C. elegans dauers despite being repulsive for C. elegans adults [2–4], and we identify an ancient and conserved sensory neuron that mediates CO2 response in both parasitic and free-living species regardless of whether CO2 is an attractive or a repulsive cue. Finally, we show that the parasites’ odor response profiles are more similar to each other than to that of C. elegans despite their greater phylogenetic distance, likely reflecting evolutionary convergence to insect parasitism. Our results suggest that the olfactory responses of parasitic versus free-living nematodes are highly diverse and that this diversity is critical to the evolution of nematode behavior.

Olfaction shapes host–parasite interactions in parasitic nematodes

“…They offer a number of advantages as model systems, including small size, short generation time, and amenability to laboratory culturing and behavioral analysis (12, 13). In addition, they resemble skin-penetrating human-parasitic nematodes in that they actively seek out hosts using olfactory cues (2,7,(13)(14)(15)(16). EPNs also are of interest as biocontrol agents for insect pests and disease vectors and currently are used throughout the world as environmentally safe alternatives to chemical insecticides.…”

“…In addition, some EPNs of the genus Steinernema exhibit jumping, a rare behavior among soft-bodied, limbless organisms (27, 28). Among EPNs, jumping is a highly specialized ambushing behavior in which the IJ propels itself into the air (13,27,29). Jumping is thought to be a short-range host-seeking strategy that facilitates attachment to the host when the host is in close proximity (27,30,31).…”

“…In general, cruisers are most effective at infecting stationary hosts, whereas ambushers are most effective at infecting fast-moving hosts (32). Previous studies have demonstrated that EPNs are attracted to CO 2 as well as to a number of other odorants (13)(14)(15)(33)(34)(35). However, little is known about how EPNs respond to host odors or how olfactory responses contribute to differences in host-seeking strategy.…”

“…EPNs are parasites of insects that infect and kill insect larvae (10,11). They offer a number of advantages as model systems, including small size, short generation time, and amenability to laboratory culturing and behavioral analysis (12,13). In addition, they resemble skin-penetrating human-parasitic nematodes in that they actively seek out hosts using olfactory cues (2,7,(13)(14)(15)(16).…”

Behaviour and Population Dynamics of Entomopathogenic Nematodes Following Application

“…Research aimed toward the practical goal of genetic improvement of EPN (see Chap. 2) is providing insights into the genetic basis of important traits related to survival and infectivity, while exciting comparative studies encompassing EPN along with other parasites and the intensively studied C. elegans holds prospects for understanding both the mechanisms and evolution of behaviours including dispersal and host finding (Hallem et al, 2011;Kaplan et al).…”