Species-specific recognition of the carrier insect by dauer larvae of the nematode Caenorhabditis japonica

Abstract

SUMMARYHost recognition is crucial during the phoretic stage of nematodes because it facilitates their association with hosts. However, limited information is available on the direct cues used for host recognition and host specificity in nematodes. Caenorhabditis japonica forms an intimate association with the burrower bug Parastrachia japonensis. Caenorhabditis japonica dauer larvae (DL), the phoretic stage of the nematode, are mainly found on adult P. japonensis females but no other species. To understand the mechanisms of species-specific and female carrier-biased ectophoresy in C. japonica, we investigated whether C. japonica DL could recognize their hosts using nematode loading and chemoattraction experiments. During the loading experiments, up to 300 C. japonica DL embarked on male and female P. japonensis, whereas none or very few utilized the other shield bugs Erthesina fullo and Macroscytus japonensis or the terrestrial isopod Armadillidium vulgare. In the chemoattraction experiments, hexane extracts containing the body surface components of nymphs and both adult P. japonensis sexes attracted C. japonica DL, whereas those of other shield bugs did not. Parastrachia japonensis extracts also arrested the dispersal of C. japonica DL released at a site where hexane extracts were spotted on an agar plate; i.e. >50% of DL remained at the site even 60min after nematode inoculation whereas M. japonensis extracts or hexane alone did not have the same effect. These results suggest that C. japonica DL recognize their host species using direct chemical attractants from their specific host to maintain their association.

Caenorhabditis evolution in the wild

“…C. elegans shares with a number of other Caenorhabditis the trait of generalism toward invertebrate dispersal hosts, albeit not entirely promiscuous in host use [2,5,7]. However, the specialized relationship of C. japonica with the hemipteran insect Parastrachia japonensis provides the best understood natural history of any species [25,26]. It is plausible that C. drosophilae, which appears to disperse solely on Drosophila nigrospiracula to new cactus rots [27], and some other less well-understood Caenorhabditis, also evolved specialized dispersal host relationships from a more generalist ancestral state.…”

“…Moreover, dauer larvae participate in nictation behavior -they climb up substrate protrusions, standing on their tails and waving, often forming large ropy and wriggling aggregates of thousands of worms -that facilitates adhesion to and transport by dispersal vectors [2,13,31]. Invertebrate vectors appear common, albeit with few examples of flight-capable hosts [2,3,26], and frugivorous vertebrates might also contribute to Caenorhabditis natural dispersal. More recently, commercial human agriculture likely provides a means of movement, especially for cosmopolitan species such as C. elegans, C. briggsae, and C. brenneri.…”

“…However, little is known about heterogeneity across taxa in sensitivity to dauer triggers, other than that, in contrast to C. elegans, high temperature does not trigger dauer development in C. briggsae [61]. Chemosensation in dauer may be critical for successful dispersal on appropriate invertebrate vectors for overwintering, as is the case in C. japonica [26]. Much research on the genetic pathways controlling dauer development connect intimately to studies of aging and lifespan [62].…”

Two levels of host-specificity in a fig-associatedCaenorhabditis

“…In contrast to pollinating wasps, who must enter the -associated and tend to be promiscuous in carrier choice [51] (although some preferences in C. remanei have been noted [88]). The more distantly-related C. japonica has been shown to have behavioral preferences for its shield bug host [89], and similar findings have been shown for Pristionchus nematodes and their host beetles [90]. Nematode occupancy biases on pollinating wasps relative to parasitic wasps have been observed in the figassociated parasitic Schistonchus and Parasitodiplogaster nematodes [45,91].…”

Host orientation using volatiles in the phoretic nematode Caenorhabditis japonica

“…In our previous study, we demonstrated that C. japonica DL specifically embark on P. japonensis and are attracted to the hexane extracts containing body surface components of P. japonensis (Okumura et al, 2013a). These studies indicate the presence of a species-specific kairomone that is directly released by the host insect and attracts DL.…”