Abstract
Although host–parasitoid interactions are becoming well characterized at the organismal and cellular levels, much remains to be understood of the molecular bases for the host immune response and the parasitoids' ability to defeat this immune response. Leptopilina boulardi and L. heterotoma, two closely related, highly infectious natural parasitoids of Drosophila melanogaster, appear to use very different infection strategies at the cellular level. Here, we further characterize cellular level differences in the infection characteristics of these two wasp species using newly derived, virulent inbred strains, and then use whole genome microarrays to compare the transcriptional response of Drosophila to each. While flies attacked by the melanogaster group specialist L. boulardi (strain Lb17) up-regulate numerous genes encoding proteolytic enzymes, components of the Toll and JAK/STAT pathways, and the melanization cascade as part of a combined cellular and humoral innate immune response, flies attacked by the generalist L. heterotoma (strain Lh14) do not appear to initiate an immune transcriptional response at the time points post-infection we assayed, perhaps due to the rapid venom-mediated lysis of host hemocytes (blood cells). Thus, the specialist parasitoid appears to invoke a full-blown immune response in the host, but suppresses and/or evades downstream components of this response. Given that activation of the host immune response likely depletes the energetic resources of the host, the specialist's infection strategy seems relatively disadvantageous. However, we uncover the mechanism for one potentially important fitness tradeoff of the generalist's highly immune suppressive infection strategy.
Highlights
Parasitic wasps are exceedingly diverse, they often act as keystone species in natural ecosystems, and because of their ability to evade and/or suppress insect immune defenses they have become the most successful group of biological control agents [1]
Leptopilina boulardi (Lb17) and Leptopilina heterotoma (Lh14) Compared to Other Characterized Strains Several studies have described the organismal and cellular level infection dynamics of L. heterotoma and L. boulardi in D. melanogaster hosts, mainly using wasp strains collected in Europe and Africa
One characterized L. boulardi strain, G486 from Congo, is distinct from other described strains in that it is relatively avirulent in immune-competent D. melanogaster larvae, and compared to virulent strains has relatively elongated virus-like particle (VLP) with few vesicles [46] and a unique venom protein profile [47]
Summary
Parasitic wasps are exceedingly diverse, they often act as keystone species in natural ecosystems, and because of their ability to evade and/or suppress insect immune defenses they have become the most successful group of biological control agents [1]. Drosophila can mount a potent innate immune response against parasitic wasps and other pathogens. This immune response is often divided into two main components, the humoral response and the cellular response. The humoral response has been intensely studied for its role in combating bacterial and fungal infections, but may be responsible for aspects of macroparasite killing. It is governed by the fat body, which controls release of immune active extracellular proteins such as antimicrobial peptides (AMPs) and complement-like proteins (e.g., Teps) into the hemolymph. Drosophila responds to septic injury with bacteria and fungi by up-regulating many genes from the Toll and Imd pathways [6,7]
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