Drosophila Cellular Immunity Against Parasitoid Wasps: A Complex and Time-Dependent Process

Abstract

Host-parasitoid interactions are among the most studied interactions between invertebrates because of their fundamental interest - the evolution of original traits in parasitoids - and applied, parasitoids being widely used in biological control. Immunity, and in particular cellular immunity, is central in these interactions, the host encapsulation response being specific for large foreign bodies such as parasitoid eggs. Although already well studied in this species, recent data on Drosophila melanogaster have unquestionably improved knowledge of invertebrate cellular immunity. At the same time, the venomics of parasitoids has expanded, notably those of Drosophila. Here, we summarize and discuss these advances, with a focus on an emerging "time-dependent" view of interactions outcome at the intra- and interspecific level. We also present issues still in debate and prospects for study. Data on the Drosophila-parasitoid model paves the way to new concepts in insect immunity as well as parasitoid wasp strategies to overcome it.

Keywords: Drosophila; Leptopilina; encapsulation; hematopoiesis; immunity; parasitoid wasp; venom.

Figure 1

Schematic hematopoiesis in a Drosophila melanogaster larva. Hemocytes, mainly plasmatocytes and crystal cells, are circulating in the larval hemolymph. These circulating hemocytes can derive from embryonic prohemocytes or are also formed within the sessile compartment during most of the larval stages. This compartment is composed of sub-cuticular groups of cells, mainly prohemocytes and plasmatocytes, present in the different larval segments. At the end of the L3 stage, the first lobes of the lymph gland increase in size due to the proliferation of hemocytes that will be released just after pupation in healthy larvae. In normal conditions, self-renewing prohemocytes are considered as progenitors for the three main hemocytes types. After parasitoid oviposition, circulating or sessile plasmatocytes can also proliferate and transdifferentiate into crystal cells and lamellocytes. In parasitized hosts, lamellocytes can also differentiate from prohemocytes within the lymph gland and be released earlier than pupation to participate in the encapsulation.

Figure 2

Different possible outcomes for parasitoids. On the top: when a D. melanogaster L2 larva is parasitized by the virulent L. boulardi ISm line, the parasitoid egg develops normally and the parasitoid larva hatches from its chorion 24 to 48 h later after parasitism. The parasitoid larva continues its moderate growth until the fly larva pupates and after a few days the puparium is mainly occupied by the parasitoid that has eaten almost all the fly larva tissues. Twenty days after oviposition, an adult parasitoid egress from the pupal case instead of a fly. On the center: when a D. melanogaster resistant L2 larva is parasitized by the avirulent L. boulardi G486 line, the parasitoid egg is rapidly encapsulated and a melanized capsule is formed after 48 h that remains visible in the larva. The capsule is retrieved in the emerging adult fly. On the bottom: when a D. suzukii larva is parasitized by the generalist L. heterotoma wasp, the egg hatches and the parasitoid larva remains alive after 48 h, with no observed capsule or melanisation. After 96 h, the parasitoid larva is dead or dying and is slowly embedded in a cell-formed melanized capsule. The capsule continues to enlarge until pupation and it is well visible through the pupal case and then retrieved in the abdomen of the emerging fly. The upper scale indicates the development time from oviposition and the observed stages. The scales provided on the pictures are given in millimeters (mm).