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

Moreau, Sébastien; Guillot, Sylvain; Populaire, Céline; Doury, Géraldine; Prévost, Geneviève; Eslin, Patrice

doi:10.1016/j.dci.2004.07.002

Cited by 10 publications

(8 citation statements)

References 12 publications

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“…The exceptionally high haemocyte load of D. suzukii larvae at the time of parasitization is considered as likely contributing to their resistance towards the highly virulent A. japonica . The same phenomenon is reported for the interaction between the closely‐related parasitoid Asobara citri and host Drosophila simulans (Moreau et al ., 2005).…”

Section: Discussionsupporting

confidence: 82%

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

Poyet

Havard

Prévost

et al. 2013

Physiological Entomology

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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.

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Section: Discussionsupporting

confidence: 82%

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

Poyet

Havard

Prévost

et al. 2013

Physiological Entomology

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“…Previous studies have shown that fly species and strains with a greater constitutive production of hemocytes are more resistant against and/or are better able to encapsulate parasitoid wasp eggs [12], [18], [19], [48]. Although a correlation does not necessarily imply causation, these data suggest that evolution of higher constitutive production of hemocytes is a relatively simple way for hosts to defeat one of their most common classes of parasites.…”

Section: Discussionmentioning

confidence: 80%

“…It was also found that D. melanogaster strains artificially selected for resistance against A. tabida showed a significant increase in plasmatocyte numbers [17]. Furthermore, D. simulans , which makes significantly more plasmatocytes than its sister species D. melanogaster , was significantly more resistant against the more immune-suppressive wasp A. citri [18]. Finally, D. melanogaster mutants producing a wide range of hemocyte counts showed a significant correlation (r 2 = 0.45) between constitutive plasmatocyte numbers and encapsulation ability against the wasp Leptopilina boulardi [19].…”

Section: Introductionmentioning

confidence: 99%

High Hemocyte Load Is Associated with Increased Resistance against Parasitoids in Drosophila suzukii, a Relative of D. melanogaster

2012

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Among the most common parasites of Drosophila in nature are parasitoid wasps, which lay their eggs in fly larvae and pupae. D. melanogaster larvae can mount a cellular immune response against wasp eggs, but female wasps inject venom along with their eggs to block this immune response. Genetic variation in flies for immune resistance against wasps and genetic variation in wasps for virulence against flies largely determines the outcome of any fly-wasp interaction. Interestingly, up to 90% of the variation in fly resistance against wasp parasitism has been linked to a very simple mechanism: flies with increased constitutive blood cell (hemocyte) production are more resistant. However, this relationship has not been tested for Drosophila hosts outside of the melanogaster subgroup, nor has it been tested across a diversity of parasitoid wasp species and strains. We compared hemocyte levels in two fly species from different subgroups, D. melanogaster and D. suzukii, and found that D. suzukii constitutively produces up to five times more hemocytes than D. melanogaster. Using a panel of 24 parasitoid wasp strains representing fifteen species, four families, and multiple virulence strategies, we found that D. suzukii was significantly more resistant to wasp parasitism than D. melanogaster. Thus, our data suggest that the relationship between hemocyte production and wasp resistance is general. However, at least one sympatric wasp species was a highly successful infector of D. suzukii, suggesting specialists can overcome the general resistance afforded to hosts by excessive hemocyte production. Given that D. suzukii is an emerging agricultural pest, identification of the few parasitoid wasps that successfully infect D. suzukii may have value for biocontrol.

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“…tabida and A. citri has been made) [102–104]. A much larger number of independent generalist and specialist parasite lineage pairs will need to be identified and examined to determine whether specialist pathogens typically adopt less immune suppressive strategies.…”

Section: Discussionmentioning

confidence: 99%

Contrasting Infection Strategies in Generalist and Specialist Wasp Parasitoids of Drosophila melanogaster

et al. 2007

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Although host–parasitoid interactions are becoming well characterized at the organismal and cellular levels, much remains to be understood of the molecular bases for the host immune response and the parasitoids' ability to defeat this immune response. Leptopilina boulardi and L. heterotoma, two closely related, highly infectious natural parasitoids of Drosophila melanogaster, appear to use very different infection strategies at the cellular level. Here, we further characterize cellular level differences in the infection characteristics of these two wasp species using newly derived, virulent inbred strains, and then use whole genome microarrays to compare the transcriptional response of Drosophila to each. While flies attacked by the melanogaster group specialist L. boulardi (strain Lb17) up-regulate numerous genes encoding proteolytic enzymes, components of the Toll and JAK/STAT pathways, and the melanization cascade as part of a combined cellular and humoral innate immune response, flies attacked by the generalist L. heterotoma (strain Lh14) do not appear to initiate an immune transcriptional response at the time points post-infection we assayed, perhaps due to the rapid venom-mediated lysis of host hemocytes (blood cells). Thus, the specialist parasitoid appears to invoke a full-blown immune response in the host, but suppresses and/or evades downstream components of this response. Given that activation of the host immune response likely depletes the energetic resources of the host, the specialist's infection strategy seems relatively disadvantageous. However, we uncover the mechanism for one potentially important fitness tradeoff of the generalist's highly immune suppressive infection strategy.

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

Cited by 10 publications

References 12 publications

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

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

High Hemocyte Load Is Associated with Increased Resistance against Parasitoids in Drosophila suzukii, a Relative of D. melanogaster

Contrasting Infection Strategies in Generalist and Specialist Wasp Parasitoids of Drosophila melanogaster

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