Mechanisms of host seeking by parasitic nematodes

Abstract

The phylum Nematoda comprises a diverse group of roundworms that includes parasites of vertebrates, invertebrates, and plants. Human-parasitic nematodes infect approximately one billion people worldwide and cause some of the most common neglected tropical diseases, particularly in low-resource countries [1]. Parasitic nematodes of livestock and crops result in billions of dollars in losses each year [1]. Many nematode infections are treatable with low-cost anthelmintic drugs, but repeated infections are common in endemic areas and drug resistance is a growing concern with increasing therapeutic and agricultural administration [1]. Many parasitic nematodes have an environmental infective larval stage that engages in host seeking, a process whereby the infective larvae use sensory cues to search for hosts. Host seeking is a complex behavior that involves multiple sensory modalities, including olfaction, gustation, thermosensation, and humidity sensation. As the initial step of the parasite-host interaction, host seeking could be a powerful target for preventative intervention. However, host-seeking behavior remains poorly understood. Here we review what is currently known about the host-seeking behaviors of different parasitic nematodes, including insect-parasitic nematodes, mammalian-parasitic nematodes, and plant-parasitic nematodes. We also discuss the neural bases of these behaviors.

Olfactory circuits and behaviors of nematodes

“…Different nematode species share conserved positional sensory neuroanatomy [8,9], and thus understanding how C. elegans microcircuits generate olfactory behaviors may have direct implications for how analogous microcircuits operate in parasitic nematodes. Although the microcircuits underlying olfactory preferences in parasitic nematodes are poorly understood, recent studies have elucidated the divergent olfactory preferences of different parasitic nematode species.…”

“…In addition, parasitic nematodes of livestock and plants result in billions of dollars in economic and food losses each year [62]. Many parasitic nematodes have an environmental infective stage, called the infective juvenile (IJ) or infective third-stage larva (L3i) in the case of insect-parasitic and mammalian-parasitic nematodes, that actively searches for hosts to infect using olfaction in combination with other sensory modalities [9]. A better understanding of olfaction in parasitic nematodes could therefore lead to new strategies for preventing parasitic nematode infections.…”

“…A unique aspect of nematode neurobiology is conserved neuroanatomy: electron microscopy studies of anterior sensory anatomy have demonstrated that even distantly related species have approximately the same number of neurons located in roughly the same positions within the body [8,9]. In addition, laser ablation studies have demonstrated that sensory neuron function is often conserved across free-living and parasitic nematode species [9].…”

“…In addition, laser ablation studies have demonstrated that sensory neuron function is often conserved across free-living and parasitic nematode species [9]. For this reason, studies of C. elegans olfaction can directly inform studies of olfaction in parasitic worms.…”

“…In summary, parasitic nematodes show species-specific olfactory behaviors despite the fact that sensory neuroanatomy is roughly conserved across nematode species [8,9]. Efforts to study olfactory neural circuits in parasitic nematodes are ongoing.…”