European earwig (Forficula auricularia) as a novel host for the entomopathogenic nematode Steinernema carpocapsae

Hodson, Amanda K.; Friedman, M.L.; Wu, Linglin; Lewis, Edwin E.

doi:10.1016/j.jip.2011.02.004

Cited by 23 publications

(20 citation statements)

References 31 publications

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“…To examine the versatility of the fruit fly-EPN model system, we compared the ability of symbiont IJs from seven EPN species-S. carpocapsae, S. scapterisci, S. riobrave, S. glaseri, S. feltiae, H. bacteriophora, and H. indica-to infect and kill D. melanogaster larvae. These EPN species differ dramatically in their host ranges: S. carpocapsae and S. feltiae have broad host ranges that include insects from multiple orders, S. scapterisci has a narrow host range that is limited to orthopterans, and the other species have intermediate host ranges (24,(56)(57)(58)(59). S. feltiae was also recently shown to be virulent toward D. melanogaster (3).…”

Section: Resultsmentioning

confidence: 99%

Variation in the Susceptibility of Drosophila to Different Entomopathogenic Nematodes

2015

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Entomopathogenic nematodes (EPNs) in the genera Heterorhabditis and Steinernema are lethal parasites of insects that are of interest as models for understanding parasite-host interactions and as biocontrol agents for insect pests. EPNs harbor a bacterial endosymbiont in their gut that assists in insect killing. EPNs are capable of infecting and killing a wide range of insects, yet how the nematodes and their bacterial endosymbionts interact with the insect immune system is poorly understood. Here, we develop a versatile model system for understanding the insect immune response to parasitic nematode infection that consists of seven species of EPNs as model parasites and five species of Drosophila fruit flies as model hosts. We show that the EPN Steinernema carpocapsae, which is widely used for insect control, is capable of infecting and killing D. melanogaster larvae. S. carpocapsae is associated with the bacterium Xenorhabdus nematophila, and we show that X. nematophila induces expression of a subset of antimicrobial peptide genes and suppresses the melanization response to the nematode. We further show that EPNs vary in their virulence toward D. melanogaster and that Drosophila species vary in their susceptibilities to EPN infection. Differences in virulence among different EPN-host combinations result from differences in both rates of infection and rates of postinfection survival. Our results establish a powerful model system for understanding mechanisms of host-parasite interactions and the insect immune response to parasitic nematode infection. E ntomopathogenic nematodes (EPNs) of the genera Steinernema and Heterorhabditis are insect-parasitic nematodes that are phylogenetically distant but share a similar life cycle as a result of convergent evolution (1). EPNs offer numerous advantages as model parasitic nematodes, including small size, short generation time, and amenability to in vitro culturing (2). EPN infective larvae are associated with bacterial endosymbionts: Steinernema species are associated with bacteria in the genus Xenorhabdus, and Heterorhabditis species are associated with bacteria in the genus Photorhabdus (1). At least some EPNs are capable of infecting the fruit fly Drosophila melanogaster, providing a genetically tractable system for understanding the immune response to parasitic nematodes and their bacterial endosymbionts (3-6). However, the insect immune response to EPN infection is poorly understood.During a particular developmental stage called the infective juvenile (IJ), EPNs infect insects (Fig. 1A). IJs are developmentally arrested, third-stage larvae analogous to the dauer stage of freeliving nematodes (7). IJs actively seek out insect hosts using chemosensory cues (8-10) and infect either by entering through natural body openings or by penetrating the insect cuticle (11). IJs harbor their bacterial endosymbiont in their gut and deposit it into the insect upon infection, where it assists the nematode in killing the insect, digesting insect tissues, and inhibiting the growth of o...

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Section: Resultsmentioning

confidence: 99%

Variation in the Susceptibility of Drosophila to Different Entomopathogenic Nematodes

2015

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“…These six EPN species also were chosen because of their differing host ranges. H. bacteriophora and S. carpocapsae are thought to have very broad host ranges, with S. carpocapsae capable of infecting more than 250 different species of insects from 13 orders under laboratory conditions (36,37). By contrast, S. scapterisci is an orthopteran specialist with a much narrower host range than most EPNs; its only known natural host is the mole cricket (38)(39)(40).…”

Section: H B a C Te Ri O P H O Ra S C A Rp O C A P S A E S S C mentioning

confidence: 99%

“…Mole crickets are the only known natural host for S. scapterisci (40), and house crickets are related to mole crickets and can serve as laboratory hosts for both S. scapterisci and S. carpocapsae (50). Earwigs were chosen because some earwig species are thought to be preferred natural hosts for S. carpocapsae (37). Waxworms were selected because they are a common laboratory host for EPNs and typically are used as bait when collecting EPNs from soil; thus, many described EPNs are attracted to waxworms, even in complex soil environments (42,51).…”

Section: H B a C Te Ri O P H O Ra S C A Rp O C A P S A E S S C mentioning

confidence: 99%

Olfaction shapes host–parasite interactions in parasitic nematodes

Dillman

Guillermin

Lee

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

146

164

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Many parasitic nematodes actively seek out hosts in which to complete their lifecycles. Olfaction is thought to play an important role in the host-seeking process, with parasites following a chemical trail toward host-associated odors. However, little is known about the olfactory cues that attract parasitic nematodes to hosts or the behavioral responses these cues elicit. Moreover, what little is known focuses on easily obtainable laboratory hosts rather than on natural or other ecologically relevant hosts. Here we investigate the olfactory responses of six diverse species of entomopathogenic nematodes (EPNs) to seven ecologically relevant potential invertebrate hosts, including one known natural host and other potential hosts collected from the environment. We show that EPNs respond differentially to the odor blends emitted by live potential hosts as well as to individual host-derived odorants. In addition, we show that EPNs use the universal host cue CO 2 as well as host-specific odorants for host location, but the relative importance of CO 2 versus host-specific odorants varies for different parasite-host combinations and for different host-seeking behaviors. We also identified host-derived odorants by gas chromatography-mass spectrometry and found that many of these odorants stimulate host-seeking behaviors in a species-specific manner. Taken together, our results demonstrate that parasitic nematodes have evolved specialized olfactory systems that likely contribute to appropriate host selection.entomopathogens | chemosensation | Heterorhabditis | Steinernema M any parasitic nematodes actively seek out hosts using sensory cues (1). Host seeking is a complex behavior that involves chemosensory, thermosensory, hygrosensory, and mechanosensory cues (1-4). Olfaction is a critical component of host-seeking behavior: Many parasitic nematodes use CO 2 and other host volatiles for host location (1, 2, 5-8). However, little is known about how parasites respond to host-derived odors.Entomopathogenic nematodes (EPNs) are powerful models for the study of odor-driven host-seeking behavior. EPNs comprise a guild-a group of phylogenetically divergent species that exploit the same class of resources in a similar way (9)-that includes the genera Heterorhabditis, Steinernema, and Oscheius (10, 11). 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). 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. The three genera of EPNs are phylogenetically distant but have highly similar lifestyles as a result of convergent evolution to insect parasitism (17).EPN...

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“…was reduced and in S. feltiae treated plots the densities of four non-target species of chrysomelid and carabid beetles were reduced (Buck & Bathon 1993;Koch & Bathon 1993). In large scale applications of S. carpocapsae in pistachios, populations of the earwig, Forficula auricularia L. (Dermaptera: Forficulidae), and the tenebrionid beetle, Blapstinus discolor Horn (Coleoptera: Tenebrionidae), were temporarily reduced (Hodson et al 2012) and the susceptibility of earwigs confirmed in the laboratory (Hodson, Friedman, Wu, & Lewis, 2011).…”

Section: Other Susceptible Arthropods In the System Are Infectedmentioning

confidence: 99%