Response of life-history traits to artificial and natural selection for virulence and nonvirulence in a Drosophila parastitoid, Asobara tabida.

Co-evolution of host-parasitoid interactions is determined by the costs of host resistance, which received empirical evidence, and the costs of parasitoid virulence, which have been mostly hypothesized. Asobara tabida is a parasitoid, which mainly parasitizes Drosophila melanogaster and D. subobscura, the first species being able to resist to the parasitoid development while the second species is not. To parasitize resistant hosts, including D. melanogaster, A. tabida develops sticky eggs, which prevent encapsulation, but this virulence mechanism may be costly. Interindividual and interpopulation variation in the proportion of sticky eggs respectively allowed us to (i) artificially select and compare life-history traits of a virulent and a nonvirulent laboratory strain, and (ii) compare a virulent and a nonvirulent field strain, to investigate the hypothetical costs of virulence. We observed strong differences between the 2 laboratory strains. The nonvirulent strain invested fewer resources in reproduction and walked less than the virulent one but lived longer. Concerning the field strains, we observed that the nonvirulent strain had larger wings while the virulent one walked more and faster. All together, our results suggest that virulence may not always be costly, but rather that different life histories associated with different levels of virulence may coexist at both intra- and interpopulation levels.

The Wide Potential Trophic Niche of the Asiatic Fruit Fly Drosophila suzukii: The Key of Its Invasion Success in Temperate Europe?

The Asiatic fruit fly Drosophila suzukii has recently invaded Europe and North and South America, causing severe damage to fruit production systems. Although agronomic host plants of that fly are now well documented, little is known about the suitability of wild and ornamental hosts in its exotic area. In order to study the potential trophic niche of D. suzukii with relation to fruit characteristics, fleshy fruits from 67 plant species were sampled in natural and anthropic ecosystems (forests, hedgerows, grasslands, coastal areas, gardens and urban areas) of the north of France and submitted to experimental infestations. A set of fruit traits (structure, colour, shape, skin texture, diameter and weight, phenology) potentially interacting with oviposition choices and development success of D. suzukii was measured. Almost half of the tested plant species belonging to 17 plant families allowed the full development of D. suzukii. This suggests that the extreme polyphagy of the fly and the very large reservoir of hosts producing fruits all year round ensure temporal continuity in resource availability and contribute to the persistence and the exceptional invasion success of D. suzukii in natural habitats and neighbouring cultivated systems. Nevertheless, this very plastic trophic niche is not systematically beneficial to the fly. Some of the tested plants attractive to D. suzukii gravid females stimulate oviposition but do not allow full larval development. Planted near sensitive crops, these "trap plants" may attract and lure D. suzukii, therefore contributing to the control of the invasive fly.

Structural and functional characterization of pseudopodocyte, a shaggy immune cell produced by two Drosophila species of the obscura group.

We recently reported that most of the Drosophila species of the obscura group were unable to mount cellular capsules and no lamellocyte was ever found in the hemolymph of any of the tested species. Only three species were able to encapsulate, despite lacking lamellocytes. Their encapsulation ability was always associated with the presence of an unpreviously described kind of capsule-forming immunocytes designated as "atypical hemocytes". Here, we describe the ultrastructural and functional characteristics of this type of hemocyte. We show that these cells share many ultrastructural and morphological features with Drosophila melanogaster plasmatocytes, although they are involved in the formation of the external layers of the cellular capsule, a functional property exhibited by lamellocytes in D. melanogaster. Due to the high number of pseudopodes in these cells, we suggest to name them "pseudopodocytes". After structural and functional characterization of these atypical hemocytes, their ambiguous status between plasmatocytes and lamellocytes is discussed.

Immune resistance of Drosophila hosts against Asobara parasitoids: cellular aspects.

The immunity of Drosophila relies on a variety of defenses cooperating to fight parasites and pathogens. The encapsulation reaction is the main hemocytic response neutralizing large parasites like endophagous parasitoids. The diversity of the mechanisms of immunoevasion evolved by Asobara parasitoids, together with the wide spectrum of Drosophila host species they can parasitize, make them ideal models to study and unravel the physiological and cellular aspects of host immunity. This chapter summarizes what could be learnt on the cellular features of the encapsulation process in various Drosophila spp., and also on the major role played by Drosophila hosts hemocytes subpopulations, both in a quantitative and qualitative manner, regarding the issue of the immune Asobara-Drosophila interactions.

Strategies of avoidance of host immune defenses in Asobara species.

Eggs and larvae of endophagous parasitoids face the host's immunity reaction once they penetrate the insect host's hemocele. In order to overcome the host's immune barrier, endoparasitoids have developed various strategies. Conformer parasitoids hide and/or get protected from the attack by the host's immunity cells without interfering with the host's immune system. Differently, regulator parasitoids directly attack the host's hemocytes, therefore totally inhibiting the immunity reaction of encapsulation in the parasitized host. Female wasps may also discriminate immunoreactive hosts from nonreactive, permissive ones before laying an egg. These different strategies coexist within the same genus of the braconids Asobara, endoparasitoids of Drosophila larvae. The physiological mechanisms underlying the conformer and regulator strategies in Asobara are exposed. The factors which may contribute to the diversity of the means developed by Asobara parasitoids to overcome the hosts' immunity defenses are discussed.

The fly Drosophila subobscura: a natural case of innate immunity deficiency.

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.

Conversely to its sibling Drosophila melanogaster, D. simulans overcomes the immunosuppressive effects of the parasitoid Asobara citri.

The endoparasitoid Asobara citri avoids Drosophila melanogaster immune defenses, thanks to immune suppressive effects. We investigated whether this parasitoid could also circumvent the immune reaction of D. simulans, a sibling species of D. melanogaster. The rates of infestation, successful parasitism, total encapsulation and mortality were measured after complete development of both D. melanogaster and D. simulans larvae parasitized by A. citri. Results showed that the parasitoids were almost never encapsulated in D. melanogaster larvae, while 45% were encapsulated in D. simulans. A. citri induced a targeted disruption of the hematopoietic organs and a decrease of the hemocytes load in host larvae of both species. Despite such disruptive immune effects most D. simulans larvae succeeded in encapsulating A. citri eggs, probably thanks to their ability to immediately mount a capsule after infestation. This work brings some insight into the diversity of the immune potentials evolved by Drosophila species towards parasitoids.

Evolution of hemocyte concentration in the melanogaster subgroup species.

We explore two possible hypotheses about the ecological factors driving the evolution of hemocyte load in insects. The first is parasite infection risk, its variability and the genetic diversity of parasites. The other supposes that all the other factors of environmental stress drive the evolution through a pleiotropic selection on metabolic rate. The two hypotheses are tested with data on hemocyte load and ecology of six Drosophila species of the melanogaster subgroup. Hemocyte load correlates significantly with the parasite-driven selection index, but not with the stress selection index. The result being based on too little data to conclude definitely, this work must be considered more as a methodological research based on published results on insect physiology immunity and ecology rather than an empirical evidence of such a relationship.

Comparative study of the strategies evolved by two parasitoids of the genus Asobara to avoid the immune response of the host, Drosophila melanogaster.

Asobara tabida and Asobara citri are two braconid endoparasitoids of Drosophila melanogaster larvae. We studied and compared the strategies evolved by these two species to avoid the immune reaction of their host. A. tabida has no negative impact on host cellular defenses and its eggs avoid encapsulation by adhering to host tissues. At the opposite, we found that A. citri, whose eggs are devoid of adhesive properties, affects the host encapsulation abilities, hemolymph phenoloxidase activity and concentrations of circulating hemocytes. Some of these effects could directly rely on a severe disruption of the hematopoietic organ anterior lobes observed in parasitized larvae. This is the first report of the immune suppressive abilities of a parasitoid from the Asobara genus. Results are presented and discussed with respect to the strategies of virulence evolved by other parasitoids to counteract the D. melanogaster immune system.