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The fly Drosophila subobscura: A natural case of innate immunity deficiency

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Abstract

The Drosophila subobscura larvae were found to be unable to form a capsule around a parasitic egg or an inert foreign body. The specificity and physiological causes of this incapacity were also explored: analysis of the circulating hemocytes showed that no lamellocyte was ever found in D. subobscura host larvae. Therefore, the fly D. subobscura is the first discovered animal species to present an innate immunodeficiency against a wide range of parasites. This is contrary to the theories that propose that all organisms, in natural conditions, are potentially able to defend themselves against parasitization. This unexpected finding opens evolutionary debates about the cost of immune resistance not only at the level of a population, but also of a whole species. We believe this species of fruitfly could become a new model system to study genes involved in hematopoïesis, and in a larger context to better understand defence reactions in organisms.

Introduction

It is very rare for a member of a species to escape infestation by pathogens or parasites during its lifetime. Until now it has been thought that all organisms react to invaders by defending themselves, a strategy which has variable success [1]. The defence against parasites and pathogens is enacted by two different systems in vertebrates, the innate (natural) and the acquired (adaptative) immunity. Invertebrates rely solely on innate immunity, composed of both humoral and cellular components. Humoral responses mainly involve the synthesis of various antimicrobial peptides and the rapid induction of enzymatic cascades initiating hemolymph clotting and opsonization. Cellular responses rely on the activity of blood immunocompetent cells, the hemocytes, which typically phagocytose small pathogens but form melanotic capsules around metazoan parasites too large to be phagocytosed. Although they lack vertebrate-like immunoglobulin and histo-incompatibility responses, invertebrates are able to discriminate between self and non-self and to elicit an efficient response against the “agressor”.

However, this paper describes the case of an insect species which, in its natural state, is completely non-adapted for defending itself against a whole range of parasites.

The fly Drosophila subobscura is a drosophilid species of the obscura-group found in fermenting substrates such as those of fruits and sap fluxes. The larvae have the potential to be natural hosts for several species of hymenopteran endoparasitoid wasps that attack Drosophila larvae and develop in their hemocoel, particularly Asobara tabida and Leptopilina heterotoma [2]. Generally, the defence of Drosophila larvae against large parasites relies on the encapsulation process by specialized hemocytes aggregating around their surface, and melanization ensures their efficient killing by the local production of cytotoxic melanogenic intermediates and radicals [3]. We had previously shown that the number and type of hemocytes are two of the key factors required for a successful immune reaction in Drosophila species [4]. Three major types of hemocytes are implicated in encapsulation by Drosophila larvae: (i) plasmatocytes, which are small rounded cells, (ii) crystal cells, thought to contain the substrate and enzymes necessary for melanization and (iii) lamellocytes, the large flat cells that become mutually adhesive and form a multilayered sheath around the foreign target [5]. Surprisingly, D. subobscura does not seem to share this feature and it has been described as unable to form a capsule around the braconid wasp A. tabida [6], [7].

The aims of the present study were to determine (i) whether this apparent lack of immune reaction was only shown by a specific strain of D. subobscura or by the whole species, (ii) if incapacity to form a capsule was solely to be observed after infestation by A. tabida, which would suggest that it was due to an effect of this parasitoid on the host defence system as has been shown in other models, or whether it could be generalized to other parasite species and ultimately to foreign inert bodies and (iii) the physiological causes responsible for the incapacity to encapsulate.

Section snippets

Insects

Six strains of D. subobscura were used. Three originated from northern, southern and eastern France (Amiens, Gotheron and Montgenèvre, respectively) and the other three were captured in Switzerland (Nyon), Russia (Moscow) and Portugal (Madeira island), respectively. All the strains of D. subobscura apart from the Amiens one were graciously provided by the Laboratory of “Populations, Génétique et Evolution” (CNRS, Gif-sur-Yvette, France). The D. melanogaster, A. tabida and L. heterotoma strains

Ability of D. subobscura strains to encapsulate

None of the D. subobscura larvae ever encapsulated A. tabida parasites, whatever the strain (ER=0%; Table 1A).

To test for the specificity of this incapacity of D. subobscura larvae to form a capsule, two other host/parasite (or foreign body) combinations were tested. Neither a parasitization by L. heterotoma nor a 10 nl droplet of paraffin oil triggered encapsulation in D. subobscura (Table 1B and C), however a 10 nl droplet of paraffin oil triggered 81.4% encapsulation in the larvae of a

Discussion

Lamellocytes being the main cell type responsible for capsule multilayer edification in Drosophila, our results suggest that the incapacity of D. subobscura larvae to encapsulate is due to the deficiency in this species of a category of hemocytes that are normally present in all the other species of Drosophila studied to date.

The results of our study demonstrate that D. subobscura is a species totally incapable of forming melanotic capsules around foreign bodies, whether they consist of

Acknowledgements

We thank Pr. J.R. David (CNRS, Gif-sur-Yvette) and the laboratory “Biométrie et Biologie Evolutive” (CNRS, Lyon) who graciously provided us with Drosophila subobscura strains. We also wish to thank A. Roots, J. and G. Buck for their critical readings of the manuscript, and Pr. G. Prévost for her scientific support. This work was partially supported by GDR-CNRS 2153.

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