Effet de la plante hôte sur l'immunité des insectes phytophages : influence du cépage de vigne sur la capacité des vers de la grappe à se défendre contre des bio-agresseurs

In tritrophic interactions involving phytophagous insects, host plants and natural enemies, trophic levels are highly dependent on each other. Host plant may strongly affect directly phytophagous insect and indirectly natural enemies growing on these phytophagous insects. When a natural enemy attacks a phytophagous insect, the host immune system constitutes the last chance for the host to survive to an infection. A great variation of insect immune system is generally found in populations for susceptibility to pathogens, suggesting that variable selection pressures may have shaped and driven adaptation of immune traits. This project aims to determine the influence of both host plant and natural enemies on the larval immune system of grapevine moth pests, Lobesia botrana and Eupoecilia ambiguella.During these three years, we have demonstrated a strong influence of grape variety on immune effectors of grapevine moth larvae. In addition, the grape variety modulates a trade-off between the constitutive and induced immune pathways. The variable presence of microbes on the surface of grape berries does not explain the trade-off in immune function. Beyond the grape variety effect, we also demonstrated a strong influence of parasitoids on the immune parameters of the grapevine moth larvae. In France, the most immunocompetent populations of grapevine moth are also the most parasitized. This positive correlation between successful parasitism and larval immune parameters seems not explained by a plastic response of the larval immune system to parasitoids presence, but rather by a local selection of larval immune system in response to parasitism pressure suffered by larvae for several years.The different experiments realized in my thesis confirm the complexity of the tri-trophic interactions between host plant, phytophagous insects and natural enemies. The integration of phytophagous insect immune system seems essential in understanding the interactions linking these three protagonists.Lors des interactions tri-trophiques impliquant une plante hôte, ses insectes phytophages et leurs ennemis naturels (parasitoïdes, prédateurs...), chaque niveau trophique est fortement dépendant des autres. La plante hôte peut influencer directement les traits d’histoire de vie des insectes phytophages et indirectement les ennemis naturels se développant aux dépens de ces insectes phytophages. Lorsque qu’un ennemi naturel comme un parasitoïde attaque l’insecte phytophage, son système immunitaire constitue sa dernière chance de survie. Une grande variation dans l’immunité des insectes est généralement observée dans les populations naturelles, suggérant que différentes pressions de sélection peuvent moduler et conduire à une adaptation des paramètres immunitaires. Ma thèse vise à déterminer les influences conjointes de la plante hôte et des parasitoïdes, sur les paramètres immunitaires des chenilles de deux ravageurs de la vigne, Cochylis (Eupoecilia ambiguella) et Eudémis (Lobesia botrana).Durant ces 3 années, nous avons mis en évidence une forte influence du cépage de vigne sur les effecteurs immunitaires des chenilles de vers de la grappe. De plus, le cépage de vigne semble être à l'origine d'un compromis entre les voies immunitaires constitutives et induites. La présence variable de bactéries à la surface des baies ne semble pas être à l'origine de ce compromis. Outre le cépage de vigne, nous avons démontré une forte action des parasitoïdes sur l'immunité des vers de la grappe. A l'échelle nationale, les populations d’Eudémis les plus immunocompétentes sont également les populations les plus parasitées. Cette corrélation positive entre le succès de parasitisme et les paramètres immunitaires des chenilles ne semble pas expliquée par une réponse plastique du système immunitaire des chenilles à la présence des parasitoïdes, mais plutôt par une sélection locale du système immunitaire, en réponse à la pression de parasitisme subie par ces chenilles sur plusieurs années. Les différentes études réalisées dans le cadre de ma thèse confirment la complexité des relations tri-trophiques entre la plante hôte, l’insecte phytophage et ses ennemis naturels. L’intégration du système immunitaire de l’insecte phytophage semble primordiale dans la compréhension des interactions unissant ces trois protagonistes

Effect of the host plant on the immunity of a phytophagous insect : influence of grape variety on the ability of the European grapevine moth to defend themselves against bio-aggressors

Lors des interactions tri-trophiques impliquant une plante hôte, ses insectes phytophages et leurs ennemis naturels (parasitoïdes, prédateurs...), chaque niveau trophique est fortement dépendant des autres. La plante hôte peut influencer directement les traits d’histoire de vie des insectes phytophages et indirectement les ennemis naturels se développant aux dépens de ces insectes phytophages. Lorsque qu’un ennemi naturel comme un parasitoïde attaque l’insecte phytophage, son système immunitaire constitue sa dernière chance de survie. Une grande variation dans l’immunité des insectes est généralement observée dans les populations naturelles, suggérant que différentes pressions de sélection peuvent moduler et conduire à une adaptation des paramètres immunitaires. Ma thèse vise à déterminer les influences conjointes de la plante hôte et des parasitoïdes, sur les paramètres immunitaires des chenilles de deux ravageurs de la vigne, Cochylis (Eupoecilia ambiguella) et Eudémis (Lobesia botrana).Durant ces 3 années, nous avons mis en évidence une forte influence du cépage de vigne sur les effecteurs immunitaires des chenilles de vers de la grappe. De plus, le cépage de vigne semble être à l'origine d'un compromis entre les voies immunitaires constitutives et induites. La présence variable de bactéries à la surface des baies ne semble pas être à l'origine de ce compromis. Outre le cépage de vigne, nous avons démontré une forte action des parasitoïdes sur l'immunité des vers de la grappe. A l'échelle nationale, les populations d’Eudémis les plus immunocompétentes sont également les populations les plus parasitées. Cette corrélation positive entre le succès de parasitisme et les paramètres immunitaires des chenilles ne semble pas expliquée par une réponse plastique du système immunitaire des chenilles à la présence des parasitoïdes, mais plutôt par une sélection locale du système immunitaire, en réponse à la pression de parasitisme subie par ces chenilles sur plusieurs années. Les différentes études réalisées dans le cadre de ma thèse confirment la complexité des relations tri-trophiques entre la plante hôte, l’insecte phytophage et ses ennemis naturels. L’intégration du système immunitaire de l’insecte phytophage semble primordiale dans la compréhension des interactions unissant ces trois protagonistes.In tritrophic interactions involving phytophagous insects, host plants and natural enemies, trophic levels are highly dependent on each other. Host plant may strongly affect directly phytophagous insect and indirectly natural enemies growing on these phytophagous insects. When a natural enemy attacks a phytophagous insect, the host immune system constitutes the last chance for the host to survive to an infection. A great variation of insect immune system is generally found in populations for susceptibility to pathogens, suggesting that variable selection pressures may have shaped and driven adaptation of immune traits. This project aims to determine the influence of both host plant and natural enemies on the larval immune system of grapevine moth pests, Lobesia botrana and Eupoecilia ambiguella.During these three years, we have demonstrated a strong influence of grape variety on immune effectors of grapevine moth larvae. In addition, the grape variety modulates a trade-off between the constitutive and induced immune pathways. The variable presence of microbes on the surface of grape berries does not explain the trade-off in immune function. Beyond the grape variety effect, we also demonstrated a strong influence of parasitoids on the immune parameters of the grapevine moth larvae. In France, the most immunocompetent populations of grapevine moth are also the most parasitized. This positive correlation between successful parasitism and larval immune parameters seems not explained by a plastic response of the larval immune system to parasitoids presence, but rather by a local selection of larval immune system in response to parasitism pressure suffered by larvae for several years.The different experiments realized in my thesis confirm the complexity of the tri-trophic interactions between host plant, phytophagous insects and natural enemies. The integration of phytophagous insect immune system seems essential in understanding the interactions linking these three protagonists

An assessment of the non-target effects of copper on the leaf arthropod community in a vineyard

Bordeaux mixture has been used for more than 150 years in viticulture and other agricultural applications because it is the most effective fungicide against grape downy mildew. However, the copper present in these mixtures is not degradable and can have environmental consequences. Even though the effect of Bordeaux mixture on downy mildew is well known, the non-target effects of this fungicide on leaf arthropod communities are poorly understood. In this study, we simultaneously monitored the direct effect of Bordeaux mixture on three grapevine leaf diseases and five leaf arthropods (beneficial and pest species) in the field over a four-month time period. We found a strong interaction between sampling year and treatment for all tested organisms. Overall, the presence of copper generally decreased both the occurrence of disease and densities of leaf arthropods. Thus, copper reduces some pest densities but also biological agent densities which might interfere with biological control. The effects and results presented here should prove valuable when implementing future crop management strategies and pest control procedures

How to improve grape moth pests control in viticulture. Which research fields should be promoted?

National audienc

Age, sex, mating status, but not social isolation interact to shape basal immunity in a group-living insect

International audienceImmunity is a crucial but costly trait. Individuals should therefore adjust their investment into immunity to their condition and infection risks, which are often determined by their age, sex, mating status and social environment. However, whether and how these four key factors can interact to shape basal immunity remains poorly understood. Here, we tested the simultaneous effects of these factors on hemocyte concentration and phenoloxidase activity in adults of the European earwig. We found that hemocyte concentration increased with age, and that this increase was stronger in males. We also found an age-dependent increase in phenoloxidase activity in males and virgin females, but not in mated females. However, the two immune parameters were independent of social isolation. Overall, our results reveal that a complex interplay between age, sex and mating status determines basal immunity and stress the importance of interactions in our understanding of immune investment

Food-mediated modulation of immunity in a phytophagous insect: an effect of nutrition rather than parasitic contamination.

7 pagesInternational audienceInherent to the cost of immunity, the immune system itself can exhibit tradeoffs between its arms. Phytophagous insects face a wide range of microbial and eukaryotic parasites, each activating different immune pathways that could compromise the activity of the others. Feeding larvae are primarily exposed to microbes, which growth is controlled by antibiotic secondary metabolites produced by the host plant. The resulting variation in abundance of microbes on plants is expected to differentially stimulate the insect antimicrobial immune defenses. Under the above tradeoff hypothesis, stimulation of the insect antimicrobial defenses is expected to compromise immune activity against eukaryote parasites. In the European grape berry moth, Eupoecilia ambiguella, immune effectors directed towards microbes are negatively correlated to those directed towards eukaryotic parasites among host plants. Here, we hypothesize this relationship is caused by a variable control of the microbial community among host plants by their antibiotic metabolites. To test this hypothesis, we first quantified antimicrobial activity in berries of several grape varieties. We then measured immune defenses of E. ambiguella larvae raised on artificial diets in which we mimicked levels of antimicrobial activity of grape berries using tetracycline to control the abundance of growing microbes. Another group of larvae was raised on artificial diets made of berry extracts only to control for the effect of nutrition. We found that controlling microbe abundance with tetracycline in diets did not explain variation in the immune function whereas the presence of berry extracts did. This suggests that variation in immune defenses of E. ambiguella among grape varieties is caused by nutritional difference among host plants rather than microbe abundance. Further study of the effects of berry compounds on larval immune parameters will be needed to explain the observed tradeoff among immune system components

Should grape moth larval immunity help explaining resistance against natural enemies?

8 pagesInternational audienceIn tritrophic systems (plants, phytophagous insects and natural enemies), host plantvariation often keys the relative performance of both the herbivore and its associated naturalenemies. In bottom-up effects, host plants could affect the fitness of phytophagous insectsincluding growth rate and adult fertility. These effects are indirectly reflected in parasitoidswhose success depends on their host quality. For instance, nutrient deficiency or/and toxicdefensive compounds of the plants could slow-down the development of herbivorous insects,thus extending the window of vulnerability of attacks by natural enemies.The immune system is arguably the most common resistance mechanisms used byphytophagous insects against natural enemies such as parasites and parasitoids. However, only alimited number of studies have really linked tritrophic interactions and immune defenses ofphytophagous insects. Our work considers two grape moths, the European grapevine moth,Lobesia botrana, and the European grapeberry moth Eupoecilia ambiguella.In this study, we have tested the influence of different grapevine varieties on the baselinelevel of three immune parameters (concentration of haemocytes, activity of the prophenoloxidasesystem and antimicrobial activity) of larvae of the European grapevine moth. In this presentationwe discuss the results obtained in this experiment and their effects and importance in tritrophic

Host plant variation plastically impacts different traits of the immune system of a phytophagous insect.

7 pagesInternational audience1. Host plant quality affects herbivorous insect performance and consequently their susceptibility to natural enemies. Recently, it has been hypothesized that the immune function of herbivorous insects can be altered by their host plant, thus generating variation in their susceptibility to entomopathogens. Previous studies testing this hypothesis provided contradictory outcomes, mainly as a result of the differences in methodology such as measuring a single-immune parameter rather than considering trade-off-mediated interactions between immune defence systems of the insect. Here, we hypothesized that plant-mediated changes in insect immunity could result from the alteration of physiological immune effectors of the herbivore evident as trade-offs. 2. Larvae of an inbred strain of the European grape berry moth Eupoecilia ambiguella were reared on five artificial diets each based on a different grape variety (Chardonnay, Chasselas, Gewurztraminer, Merlot, Riesling) and tested for changes in the baseline concentration of haemocytes, activities of the prophenoloxidase (PPO) system and of antimicrobial peptides of their haemolymph. Immune responsiveness of larvae across diets was also assessed by measuring changes in haemocyte concentration and activity of the PPO system after a bacterial immune challenge. 3. We found that variation among diets significantly affected immune defences of larvae. The alteration of the E. ambiguella immune system appears plastic and partly mediated by existing physiological trade-offs between immune pathways, at least between induced antibacterial defences and the PPO system. 4. These results clearly show that host plant quality can affect immune defences and potentially disease resistance of E. ambiguella and that these changes in immunity may also result from intrinsic trade-offs between immune defence systems in insects

Contrôle des ravageurs de cultures par les ennemis naturels : la plante hôte facteur régulateur du système immunitaire des chenilles de vers de la grappe.

10 pagesNational audienceEn raison des nombreux dégâts occasionnés par les vers de la grappe dans les vignobles, trouver un moyen de lutte efficace est devenu un réel challenge. A l’heure actuelle, la lutte biologique apparaît comme une alternative possible à la lutte chimique. Cependant, les résultats obtenus suite aux lâchers de parasitoïdes sont extrêmement variables dans leur efficacité. Des études approfondies de la biologie des vers de la grappe et de leurs parasitoïdes sont donc nécessaires afin d’affiner les méthodes de lutte biologique. Le système immunitaire des insectes représente la dernière ligne de défense des phytophages contre les parasitoïdes. Dans cette étude nous mettons en évidence l’influence du cépage de vigne, à la fois sur les défenses immunitaires et sur le taux de parasitisme des vers de la grappe par des parasitoïdes. Ces résultats suggèrent alors qu’il est important de tenir compte de l’immunité du ravageur dans les programmes de luttes biologiques. En effet, comme certains cépages réduisent ou augmentent l’expression de certains effecteurs immunitaires clés des ravageurs, l’efficacité des agents biologiques visant à lutter contre ces derniers peut être compromise ou améliorée selon les cas. Par conséquent, pour une efficacité de lutte maximale, le choix des agents biologiques de contrôle de ravageurs de la vigne dépendra du cépage de vigne considéré