All animals are infected by microbial partners that can be passengers or residents and influence many biological traits of their hosts. Even if important factors that structure the composition and abundance of microbial communities within and among host individuals have been recently described, such as diet, developmental stage or phylogeny, few studies have conducted cross-taxonomic comparisons, especially on host species related by trophic relationships. Here, we describe and compare the microbial communities associated with the cabbage root fly Delia radicum and its three major parasitoids: the two staphylinid beetles Aleochara bilineata and A. bipustulata and the hymenopteran parasitoid Trybliographa rapae. For each species, two populations from Western France were sampled and microbial communities were described through culture independent methods (454 pyrosequencing). Each sample harbored at least 59 to 261 different bacterial phylotypes but was strongly dominated by one or two. Microbial communities differed markedly in terms of composition and abundance, being mainly influenced by phylogenetic proximity but also geography to a minor extent. Surprisingly, despite their strong trophic interaction, parasitoids shared a very low proportion of microbial partners with their insect host. Three vertically transmitted symbionts from the genus Wolbachia, Rickettsia, and Spiroplasma were found in this study. Among them, Wolbachia and Spiroplasma were found in both the cabbage fly and at least one of its parasitoids, which could result from horizontal transfers through trophic interactions. Phylogenetic analysis showed that this hypothesis may explain some but not all cases. More work is needed to understand the dynamics of symbiotic associations within trophic network and the effect of these bacterial communities on the fitness of their hosts.

In this paper, we compare the host selection behaviours of two parasitoids, Aphidius rhopalosiphi and Aphidius picipes, in order to analyse whether behavioural adaptations to the defensive behaviour of their host (the grain aphid Sitobion avenae) could, in part, be responsible for the simultaneous presence of both species in cereal fields. The oviposition behaviour of A. picipes differed from that of A. rhopalosiphi by including a number of ‘fluttering wings’ sequences followed by immobility. It resulted in a 44 times longer host-handling time for A. picipes than for A. rhopalosiphi. Hosts attacked by A. picipes exhibited fewer defensive behaviours than hosts attacked by A. rhopalosiphi. A. picipes and A. rhopalosiphi rejected respectively 0% and 53% of unparasitized hosts presenting cornicle secretions, one of the defensive means of aphids. Furthermore, A. picipes females rejected 100% of the hosts that were already parasitized, whereas A. rhopalosiphi was previously described to reject only 20 to 40% of such hosts. Such differences could be explained by the way the two species deal with the aphid defensive behaviour. Field analyses, showed that A. rhopalosiphi was already present in wheat fields in early April whereas A. picipes appeared later and only achieved a low level of parasitism. However, when both species were present simultaneously, they shared the same resource.

Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum by comparing the microbiota of Wolbachia-free and infected adult flies of both sexes. We used high-throughput DNA sequencing (Illumina MiSeq, 16S rRNA, V5-V7 region) and performed a community and a network analysis. In both sexes, Wolbachia infection significantly decreased the diversity of D. radicum bacterial communities and modified their structure and composition by reducing abundance in some taxa but increasing it in others. Infection by Wolbachia was negatively correlated to 8 bacteria genera (Erwinia was the most impacted), and positively correlated to Providencia and Serratia. We suggest that Wolbachia might antagonize Erwinia for being entomopathogenic (and potentially intracellular), but would favor Providencia and Serratia because they might protect the host against chemical plant defenses. Although they might seem prisoners in a cell, endocellular symbionts can impact the whole microbiota of their host, hence its extended phenotype, which provides them with a way to interact with the outside world.

The development of integrated pest management strategies becomes more and more pressing in view of potential harmful effects of synthetic pesticides on the environment and human health. A promising alternative strategy against Delia radicum is the use of trap crops. Chinese cabbage (Brassica rapa subsp. pekinensis and subsp. chinensis) is a highly sensitive Brassicaceae species previously identified as a good candidate to attract the cabbage root fly away from other crops. Here, we carried out multi-choice experiments both in the laboratory and in field conditions to measure the oviposition susceptibilities of different subspecies and cultivars of Chinese cabbages as compared to a broccoli reference. We found large differences among subspecies and cultivars of the Chinese cabbage, which received three to eleven times more eggs than the broccoli reference in field conditions. In laboratory conditions, the chinensis subspecies did not receive more eggs than the broccoli reference. We conclude that D. radicum largely prefers to lay eggs on the pekinensis subspecies of Chinese cabbage compared to the chinensis subspecies or broccoli. Some pekinensis cultivars, which received over ten times more eggs than broccoli in the field, appear especially promising candidates to further develop trap crop strategies against the cabbage root fly.