Food-mediated modulation of immunity in a phytophagous insect: An effect of nutrition rather than parasitic contamination.
Inherent 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.
Université de Bourgogne, Equipe Ecologie-Evolution, UMR 6282 Biogéosciences, 6 Bd Gabriel, F-21000 Dijon, France; INRA, UMR 1065 Save ISVV, B.P.81, F-33883 Villenave d'Ornon Cedex, France; Université de Bordeaux, Bordeaux Sciences Agro, INRA, UMR 1065 Save ISVV, B.P.81, F-33883 Villenave d'Ornon Cedex, France. Electronic address: fanny.vogelweith@gmail.com.
Fanny
F
Vogelweith
Université de Bourgogne, Equipe Ecologie-Evolution, UMR 6282 Biogéosciences, 6 Bd Gabriel, F-21000 Dijon, France.
Jérôme
J
Moreau
INRA, UMR 1065 Save ISVV, B.P.81, F-33883 Villenave d'Ornon Cedex, France; Université de Bordeaux, Bordeaux Sciences Agro, INRA, UMR 1065 Save ISVV, B.P.81, F-33883 Villenave d'Ornon Cedex, France.
Denis
D
Thiéry
Université de Bourgogne, Equipe Ecologie-Evolution, UMR 6282 Biogéosciences, 6 Bd Gabriel, F-21000 Dijon, France.
Yannick
Y
Moret
D000824:Animal Nutritional Physiological Phenomena; D000818:Animals; D000900:Anti-Bacterial Agents / Q000494:pharmacology; D004156:Catechol Oxidase / Q000378:metabolism; D004792:Enzyme Precursors / Q000378:metabolism; D005638:Fruit / Q000378:metabolism / Q000382:microbiology; D006458:Hemolymph / Q000378:metabolism; D007814:Larva / Q000276:immunology / Q000382:microbiology; D064307:Microbiota; D014442:Monophenol Monooxygenase / Q000378:metabolism; D009036:Moths / Q000276:immunology* / Q000382:microbiology; D010936:Plant Extracts; D013752:Tetracycline / Q000494:pharmacology; D027843:Vitis / Q000378:metabolism / Q000382:microbiology*
D000900:Anti-Bacterial Agents; D004792:Enzyme Precursors; D010936:Plant Extracts; C038451:pro-phenoloxidase; D004156:Catechol Oxidase; D014442:Monophenol Monooxygenase; D013752:Tetracycline
Antibiotics; Eupoecilia ambiguella; Grape varieties; Immune tradeoff