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Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi.

Two strains of Drosophila melanogaster (resistant and susceptible) were parasitized by a virulent or avirulent strain of the parasitoid wasp Leptopilina boulardi. The success of encapsulation depends on both the genetic status of the host strain and the genetic status of the parasitoid strain: the immune cellular reaction (capsule) is observed only with the resistant strain-avirulent strain combination. The total numbers of host haemocytes increased in all 4 combinations, suggesting that an immune reaction was triggered in all hosts. Resistant host larvae infected with the virulent or avirulent strains of parasitoid wasp had slightly more haemocytes per mm(3) than did susceptible host larvae at the beginning of the reaction (less than 15 h post-parasitization). This difference disappeared later. Only the virulent parasitoid strain caused the production of a high percentage of altered lamellocytes (from a discoid shape to a bipolar shape), half the total number of lamellocytes are altered. This suggests that the alteration of lamellocyte shape alone is not sufficient to explain the lack of capsule formation seen in resistant hosts parasitized by the virulent strain. Lastly, there were very few altered lamellocytes in resistant or susceptible hosts parasitized by the avirulent parasitoid strain, two combinations in which no capsule was formed. As is now established for Drosophila-parasitoid interactions, virus-like particles contained in the long gland of the female wasp affect the morphology of the lamellocytes. The results presented here are further proof of the action (direct or indirect) of virus like particles of the virulent strain on lamellocytes.

Immunogenetic aspects of the cellular immune response of Drosophila against parasitoids

Abstract. Host-parasite relationships represent integrating adaptations of considerable complexity involving the hosts immune capacity to both recognize and destroy the parasite, and the latters ability to successfully invade the host and to circumvent its immune response. Compatibility in Drosophila-parasitic wasp (parasitoid) associations has been shown to have a genetic basis, and to be both species and strain specific. Studies using resistant and susceptible strains of Drosophila melanogaster infected with virulent and avirulent strains of the wasp Leptopilina boulardi demonstrate that the success of the host cellular immune response depends on the genetic status of both host and parasitoid. Immunological, physiological, biochemical, and genetic data form the bases of a two-component model proposed here to account for the observed specificity and complexity of two co-evolved adaptations, host nonself recognition and parasitoid virulence.

Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi

To develop inside their insect hosts, endoparasitoid wasps must either evade or overcome the hosts immune system. Several ichneumonid and braconid wasps inject polydnaviruses that display well-studied immune suppressive effects. However, little is known about the strategies of immunoevasion used by other parasitoid families, such as figitid wasps. The present study provides experimental evidence, based on superparasitism and injection experiments, that the figitid species Leptopilina boulardi uses an active mechanism to suppress the Drosophila melanogaster host immune response, i.e. the encapsulation of the parasitoid eggs. The immune suppressive factors are localised in the long gland and reservoir of the female genital tractus, where virus-like particles (VLPs) have been observed. Parasitism experiments using a host tumorous strain indicate that these factors do not destroy host lamellocytes but that they impair the melanisation pathway. Interestingly, they are not susceptible to heating and are not depleted with prolonged oviposition experience, in contrast to observations reported for L. heterotoma, another figitid species. The mechanisms that prevent encapsulation of eggs from L. boulardi and L. heterotoma differ in several respects, suggesting that different physiological strategies of immunosuppression might be used by specialised and generalist parasitoids.

Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species

Abstract Species of the genus Leptopilina are larval parasitoids of Drosophilidae, mainly species of the genus Drosophila. We provide four lines of evidence (i.e. morphological descriptions, crossing experiments, ITS2 sequences and RFLP’s) to show that at least six species of Leptopilina occur in Africa, of which three previously unidentified species are described here. The phylogenetic position of these three new African species (L. orientais n. sp., L. freyae n. sp. and L. guineaensis n. sp.) is established in relation to the species already known (L. heterotoma Thomson, 1862, L. victoriae Nordlander, 1980 and L. boulardi Barbotin et al., 1979) from Africa. This relationship is based on a comparison of sequences of the ITS2 of the ribosomal DNA. The geographical distributions over the Afrotropical region of these Leptopilina species are illustrated.

Encapsulation ability of Drosophila melanogaster: A genetic analysis☆

Insects are able to effectively recognize parasitoid eggs or larvae and to eliminate them by formation of a hemocytic capsule. Although the cellular process is now well documented, the genetic aspects of recognition of foreignness and the encapsulation process are still poorly understood. Experiments using the isofemale-strain method showed that the encapsulating ability of Drosophila melanogaster exercised against a parasitic wasp varies within a given population and that this variability is under partial genetic control.

Reduced cellular immune competence of a temperature-sensitive dopa decarboxylase mutant strain of Drosophila melanogaster against the parasite Leptopilina boulardi

1. The melanotic encapsulation response made by larvae of a temperature-sensitive dopa decarboxylase (DDC) mutant strain of Drosophila against the parasitic wasp Leptopilina was severely compromised in hosts with reduced levels of DDC. 2. Dopa and 5,6-dihydroxyindole (DHI) were two hemolymph components identified in hosts exhibiting a melanotic encapsulation response. 3. This is the first study to implicate DDC in insect cellular immune responses, and to provide chemical evidence that the pigment formed during such responses is eumelanin derived from tyrosine.

Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity

Parasitoids are mostly insects that develop at the expense of other arthropods, which will die as a result of the interaction. Their reproductive success thus totally depends on their ability to successfully infest their host whose reproductive success relies on its own ability to avoid or overcome parasitism. Such intense selective pressures have resulted in extremely diverse adaptations in parasitoid strategies that ensure parasitism success. For instance, wasp-specific viruses (polydnaviruses) are injected into the host by parasitoid females to modulate its physiology and immunity. This article synthesizes available physiological and molecular data on parasitoid virulence strategies and discusses the evolutionary processes at work.

COMPARATIVE STUDY OF IMMUNE COMPETENCE AND HOST SUSCEPTIBILITY IN DROSOPHILA MELANOGASTER PARASITIZED BY LEPTOPILINA BOULARDI AND ASOBARA TABIDA

Larvae of an immune-reactive (R) strain of Drosophila melanogaster readily encapsulated and killed the eggs of 2 species of parasitic wasp, Leptopilina boulardi and Asobara tabida. High pressure liquid chroma- tography with electrochemical detection identified 5,6-dihydroxyindole (DHI) and N-acetylarterenone (NAA) in the hemolymph during parasite encapsulation, indicating that the capsules enveloping the parasites are comprised of both eumelanin and sclerotin. In larvae of a host strain susceptible (S) to L. boulardi, DHI and NAA were absent, and hemolymph catecholamine profiles from these hosts resembled those of nonparasitized controls. Susceptibility was determined to be species specific for L. boulardi, because S-strain larvae were highly immune reactive against A. tabida. As with reactive R-strain hosts, DHI and NAA were detected in the he- molymph from immune-reactive S-strain larvae when they were encapsulated by A. tabida. These observations, together with previous studies, indicate that the immune response initiated by larvae of D. melanogaster against different parasites involves similar cellular and biochemical responses. The virtual absence of immune reactivity in the S strain against L. boulardi suggests these otherwise immune competent hosts are unable to recognize this parasite as a foreign entity, or that the wasp actively suppresses the cellular encapsulation response of this host strain. These investigations highlight the complexity of insect host-parasite relationships that involve the co- evolution of varied reciprocal cellular, molecular, and biochemical strategies.

Interactions between searching strategies ofDrosophila parasitoids and the polymorphic behavior of their hosts

Two strains of Drosophila melanogaster, “rover” and “sitter,” differing in locomotion while foraging were simultaneously exposed to females of either Leptopilina boulardi or Ganaspis xanthopoda (parasitic Hymenoptera). These two parasitoids show different modes of host-searching behavior, ovipositor searching, or vibrotaxis, respectively. L. boulardi parasitized the sitter host strain significantly more than the rover. In contrast, G. xanthopoda parasitized the rover strain more than the sitter. In one case, L. boulardi selected far more sitters than rovers in population cage experiments. We also describe the frequencies of rovers and sitters in three natural populations where the local parasitoid community may have partially contributed to the differences in rover and sitter frequencies.

Alterations in the activities of tyrosinase, N-acetyltransferase, and tyrosine aminotransferase in immune reactive larvae of Drosophila melanogaster

The activities of three enzymes, tyrosinase (monophenol oxidase, MPO), N-acetyltransferase (NAT), and tyrosine aminotransferase (TAT), were studied during eumelanotic encapsulation in host larvae of Drosophila melanogaster parasitized by the wasp, Leptopilina boulardi. At 24 h postinfection there was a tenfold increase in the MPO, whereas the activities of NAT and TAT were lower than those of nonparasitized controls. The data suggest that certain developmental processes are temporarily interrupted and alterations made in the metabolism of tyrosine to provide the metabolites necessary for a successful immune response. Two strains of D. melanogaster, R and Tyr-1, were parasitized and found to be immune reactive. The Tyr-1 strain is deficient in tyrosinase during the adult stage, but this mutation was found not to affect the immune capacity of the larvae. This is the first study to document concurrent alterations in the activities of various catecholamine-metabolizing enzymes during an immune response in an insect.