An Entomopathogenic Nematode by Any Other Name

Dillman, Adler R.; Chaston, John M.; Adams, Byron J.; Ciche, Todd A.; Goodrich-Blair, Heidi; Stock, S. Patricia; Sternberg, Paul W.

doi:10.1371/journal.ppat.1002527

Cited by 211 publications

(167 citation statements)

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“…The entomopathogenic lifestyle is highly specialized: EPNs locate and infect insect larval hosts, deposit their bacterial symbiont into the host, rapidly kill the host, and then resume normal development (11). The convergence of three separate genera in the EPN guild therefore is a striking example of adaptive plasticity among nematodes.…”

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

“…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).…”

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Olfaction shapes host–parasite interactions in parasitic nematodes

Dillman

Guillermin

Lee

et al. 2012

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

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146

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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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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

mentioning

confidence: 99%

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Olfaction shapes host–parasite interactions in parasitic nematodes

Dillman

Guillermin

Lee

et al. 2012

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

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146

164

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“…Other nematodes such as Oscheius spp. or Caenorhabditis briggsae, with entomopathogenic or necromenic life styles (Dillman et al, 2012), or bactivorous nematodes that may invade cadavers alone or with entomopathogens (Duncan et al, 2003a,b), may have evolved similar behaviour.…”

Section: Discussionmentioning

confidence: 99%

Interference competition in entomopathogenic nematodes: male Steinernema kill members of their own and other species

O’Callaghan

Zenner

Hartley

et al. 2014

International Journal for Parasitology

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a b s t r a c tThere is evidence of competition within and between helminth species, but the mechanisms involved are not well described. In interference competition, organisms prevent each other from using the contested resource through direct negative interactions, either chemical or physical. Steinernema spp. are entomopathogenic nematodes; they enter a living insect host which they kill and consume with the aid of symbiotic bacteria. Several studies have demonstrated intra-and interspecific competition in Steinernema, mediated by a scramble for resources and by incompatibility of the bacterial symbiont. Here we describe a mechanism by which male Steinernema may compete directly for resources, both food (host) and females, by physically injuring or killing members of another species as well as males of their own species. A series of experiments was conducted in hanging drops of insect haemolymph. Males of each of four species (Steinernema longicaudum, Steinernema carpocapsae, Steinernema kraussei and Steinernema feltiae), representing three of the five phylogenetic clades of the genus, killed each other. Within 48 h, up to 86% of pairs included at least one dead male, compared with negligible mortality in single male controls. There was evidence of intraspecific difference: one strain of S. feltiae (4CFMO) killed while another (UK76) did not. Males also killed both females and males of other Steinernema spp. There was evidence of a hierarchy of killing, with highest mortality due to S. longicaudum followed by S. carpocapsae, S. kraussei and S. feltiae. Wax moth larvae were co-infected with members of two Steinernema spp. to confirm that killing also takes place in the natural environment of an insect cadaver. When insects were co-infected with one infective juvenile of each species, S. longicaudum males killed both S. feltiae UK76 and Steinernema hermaphroditum. Wax moths co-infected with larger, equal numbers of S. longicaudum and S. feltiae UK76 produced mainly S. longicaudum progeny, as expected based on hanging drop experiments. Ó

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“…Koch's postulates to determine its pathogenicity (Dillman et al, 2012) and the other 121 was preserved in 100% ethanol for identification by rRNA sequencing as previously 122 described. In total, four nematodes were identified: Phasmarhabditis californica, 123…”

Section: Geomalacus Maculosusmentioning

confidence: 99%