Patrice Eslin

Variation in Drosophila concentration of haemocytes associated with different ability to encapsulate Asobara tabida larval parasitoid

Abstract Asobara tabida (Braconidae), a larval parasitoid of Drosophila species, successfully develops in a large proportion of Drosophila melanogaster, while most of larvae of D. simulans, a sibling of D. melanogaster, encapsulate the parasite. Study of the haemograms demonstrated that D. simulans larvae carried 4–5 times more cells in the haemolymph than larvae of D. melanogaster. The same difference in haemocyte number was observed between the reactive D. simulans hosts, which were able to encapsulate the parasitoid egg within 24 h after parasitization, and the unreactive ones, which did not form a capsule within the same period of time. Therefore, the success of the host defense reaction against A. tabida eggs was considered to relate, at least partially, to the number of haemocytes circulating in the haemolymph within a few hours following parasitization. It was also suggested that the encapsulation of A. tabida eggs may be the result of a physiological race between the ability of the host haemocytes to form the capsule, and the aptitude of the parasite to protect against encapsulation.

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.

Racing against host's immunity defenses: a likely strategy for passive evasion of encapsulation in Asobara tabida parasitoids

The hymenopteran Asobara tabida Nees (Braconidae, Alysiinae) develops as a solitary endophagous parasite in larvae of several Drosophila species. Most A. tabida eggs possess a sticky chorion which attaches to the tissue of the host organs within a few hours following oviposition. A. tabida sticky eggs usually avoid encapsulation, though the probability of survival decreases in hosts carrying a larger number of circulating hemocytes. Here, we hypothesized that the elicitation of the encapsulation reaction may result from a race between two phenomena: the hosts hemocytic reaction and the embedment of the parasitic egg within the host tissues. In order to test this hypothesis, we measured the speed of capsule formation in D. melanogaster larvae of different ages, knowing that the number of circulating hemocytes increases with the age of the larvae. Using a non-virulent A. tabida strain, the eggs of which do not attach to the host tissue, we found that the speed of capsule formation increased correlatively with the age of the D. melanogaster larva. Therefore, the hypothesis of a physiological race between hosts immunity defenses and parasites avoidance of hosts defenses is strongly supported by our results. Also, A. tabida eggs which attach to the hosts tissue before the attack by the hemocytes has taken place may be considered as a strategy of passive evasion from encapsulation.

Invasive host for invasive pest: when the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotina) in Europe

The vinegar fly Drosophila suzukii Matsumara (Diptera: Drosophilidae), native to Asia, recently invaded Europe and North America. By contrast to other frugivorous Drosophila species, D. suzukii lays eggs on ripening fruits, heavily reducing fruit production. Although cultivated host plants of D. suzukii are well documented, very little is known about wild hosts in the invaded areas. The American black cherry Prunus serotina Ehrh., a tree species native to North America, became one of the main woody forest invaders in Europe. One cause of its invasion success is the huge amount of fruit produced by P. serotina trees. A field survey showed that P. serotina is a suitable reservoir for the development and persistence of D. suzukii populations in European natural systems (on the forest area investigated, up to 70% of all the fruits of P. serotina were infested in one of the sampling sites). Laboratory tests demonstrated that D. suzukii prefers ripening cherries to ripe ones, therefore increasing the chance of the larvae to fully develop and reach maturity before the mesocarp of the fruit totally decays. Infestation of P. serotina cherries could reduce the life span of fruits, as well as their attractiveness to seed consumers and dispersers, yet P. serotina could represent a suitable plant reservoir promoting D. suzukii invasion in Europe and North America.

Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load.

Unlike other Drosophila species, the invasive Drosophila suzukii Matsumura (Diptera: Drosophilidae) shows a remarkable pest status. Among the physiological traits that may explain the high level of resistance to parasitoids of Drosophila larvae, the haemocyte load is shown repeatedly to play an important role. To determine whether haemocyte load can explain immunity resistance of D. suzukii to parasitoids, the haemocytes of parasitized and healthy larvae are quantified in two Japanese and three French populations of D. suzukii. Parasitization tests are conducted with two larval parasitoids: the paleartic Leptopilina heterotoma Thomson (Hymenoptera: Figitidae) and the Asian Asobara japonica Belokobylskij (Hymenoptera: Braconidae). Based on morphological and functional criteria, D. suzukii has classes of haemocytes similar to those described in Drosophila melanogaster. However, healthy larvae of the five populations tested possess particularly large numbers of haemocytes compared with D. melanogaster. Haemocyte load is also higher in larvae from the French populations than in the Japanese strains. The ability of D. suzukii larvae to encapsulate eggs of L. heterotoma is associated with a particularly high load of circulating haemocytes. However, it is notable that A. japonica induces a strong depression of the haemocyte population in this resistant host associated with an inability to encapsulate parasitoid eggs. The results show that the cellular immune system plays a major role in the failure of larval parasitoids to develop in most instances in larvae of D. suzukii, possibly contributing to the success of this species as an invader.

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.

Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology.

Asobara japonica (Braconidae) is an endophagous parasitoid developing in Drosophila larvae. The present study shows that A. japonica was never encapsulated in Drosophila melanogaster, and that it caused an overall inhibition of the host encapsulation reaction since injected foreign bodies were never encapsulated in parasitized hosts. Both the number of circulating hemocytes and the phenoloxidase activity decreased in parasitized larvae, and the hematopoietic organ appeared highly disrupted. We also found that A. japonica venom secretions had atypical effects on hosts compared to other braconid wasps. A. japonica venom secretions induced permanent paralysis followed by death of D. melanogaster larvae, whether injected by the female wasp during an interrupted oviposition, or manually injected into unparasitized larvae. More remarkably, these effects could be reversed by injection of ovarian extracts from female wasps. This is the first report that the venom of an endophagous braconid parasitoid can have a deadly effect on hosts, and moreover, that ovarian extracts can act as an antidote to reverse the effects of the wasps venom. These results also demonstrate that A. japonica secretions from both venom gland and ovary are required to regulate synergistically the host physiology for the success of the parasitoid.

Encapsulation ability: Are all Drosophila species equally armed? An investigation in the obscura group

Unable to form cellular capsules around large foreign bodies, the species Drosophila subobscura Collin in Gordon, 1936 was previously shown devoid of lamellocytes, the capsule-forming hemocytes in Drosophila melanogaster Meigen, 1830. This unusual case of deficiency in encapsulation ability was remarkable enough to motivate further investigations in phylogenetically related species of the obscura group. Like D. subobscura, the species Drosophila azteca Sturtevant and Dobzhansky, 1936, Drosophila bifasciata Pomini, 1940, Drosophila guanche Monclus, 1976, Drosophila miranda Dobzhansky, 1935, Drosophila persimilis Dobzhansky and Epling, 1944, and Drosophila pseudoobcura Frovola and Astaurov, 1929 were found to be unable to encapsulate large foreign bodies and also to lack lamellocytes. Surprisingly, Drosophila affinis Sturtevant, 1916, Drosophila tolteca Patterson and Mainland, 1944, and Drosophila obscura Fallen, 1823 were capable of mounting cellular capsules, although their encapsulation abilities remaine...

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.

When Parasitoids Lack Polydnaviruses, Can Venoms Subdue the Hosts? The Case Study of Asobara Species

Host regulation has been described as the many effects-- mostly physiological changes--that parasitoids cause in their host which benefit their own development (Vinson and Iwantsch, 1980). It evokes developmental disruption usually via hormonal or neurohormonal pathways, like the endocrine signaling which coordinates development of the parasitoid with that of the host so that the two partners molt in synchrony (Beckage and Gelman, 2004). It also includes all the effects on the host immune system (Strand and Pech, 1995; Schmidt et al., 2001; Pennacchio and Strand, 2006; Carton et al., 2008; Eslin et al., 2009), the first physiological barrier that endophagous parasitoids encounter after they enter the hemocoel of their host. In order to regulate their hosts immunity and physiology, parasitoids produce and release active factors in the host hemocoel. These factors may come from either the female wasps reproductive apparatus and its associated glands, or the parasitic egg or larva itself. In many species of the ichneumonid and braconid families (Ichneumonoidea), symbiotic polydnaviruses (PDVs) or virus-like particles (VLPs) (Schmidt and Schumann-Feddersen, 1989; Strand and Pech, 1995; Beckage, 1998; Drezen et al., 2003; Beckage and Gelman, 2004; Pennacchio and Strand, 2006; Bezier et al., 2009) can act as infecting agents. PDVs multiply in the calyx cells of the female wasps ovaries while