A role for nematocytes in the cellular immune response of the DrosophilidZaprionus indianus

Balint Z Kacsoh,Todd A Schlenke,Julianna Bozler

doi:10.1017/s0031182013001431

Abstract

SUMMARYThe melanotic encapsulation response mounted by Drosophila melanogaster against macroparasites, which is based on haemocyte binding to foreign objects, is poorly characterized relative to its humoral immune response against microbes, and appears to be variable across insect lineages. The genus Zaprionus is a diverse clade of flies embedded within the genus Drosophila. Here we characterize the immune response of Zaprionus indianus against endoparasitoid wasp eggs, which elicit the melanotic encapsulation response in D. melanogaster. We find that Z. indianus is highly resistant to diverse wasp species. Although Z. indianus mounts the canonical melanotic encapsulation response against some wasps, it can also potentially fight off wasp infection using two other mechanisms: encapsulation without melanization and a non-cellular form of wasp killing. Zaprionus indianus produces a large number of haemocytes including nematocytes, which are large fusiform haemocytes absent in D. melanogaster, but which we found in several other species in the subgenus Drosophila. Several lines of evidence suggest these nematocytes are involved in anti-wasp immunity in Z. indianus and in particular in the encapsulation of wasp eggs. Altogether, our data show that the canonical anti-wasp immune response and haemocyte make-up of the model organism D. melanogaster vary across the genus Drosophila.

Highlights

The wasp species L. guineaensis, Ganaspis sp. 1, Ganaspis sp. 2, Trichopria sp. 1 and Asobara citri were all highly successful infectors of Z. indianus, the wasps Ganaspis xanthopoda and Asobara japonica induced a high proportion of death in Z. indianus hosts, and Z. indianus was relatively resistant against all other wasp species
Given L. guineaensis and A. citri are thought to be native to Africa and to overlap with the ancestral Z. indianus home range, it is tempting to speculate that they have adapted to specialize on Z. indianus hosts
We found that Z. indianus can use the canonical melanotic encapsulation response described from D. melanogaster to kill the eggs of some wasp species

Summary

Introduction

Cellular encapsulation of pathogens by haemocytes (blood cells) is common to diverse invertebrate hosts (Salt, 1963, 1970; Ratner and Vinson, 1983; Gotz, 1986; Lackie, 1988; Gillespie et al 1997), is important for pathogen resistance in insect vectors of human disease (Richman and Kafatos, 1996) and is functionally similar to granuloma formation in vertebrates (Adams, 1976) In this immune response, pathogens in the haemolymph (blood) are recognized as foreign, which activates haemocytes to migrate towards, adhere to, and consolidate around the pathogen, forming a multi-cellular multi-layered capsule. Because haemocyte morphology is highly variable across invertebrate lineages, organization of a general haemocyte classification scheme has been difficult and many different named haemocyte classes participate in the encapsulation responses of different host species (Wigglesworth, 1959; Jones, 1962; Rizki, 1962; Lackie, 1988; Gupta, 1994; Lavine and Strand, 2002)

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