Fanny Vogelweith

Immunocompetence increases with larval body size in a phytophagous moth

Despite the obvious benefit of an immune system, its efficacy against pathogens and parasites may show great variation among individuals, populations and species. Understanding the causes of this variation is becoming a central theme in ecology. Many biotic and abiotic factors are known to influence immunocompetence (temperature, age, etc.). However, for a given age, size among individuals varies, probably as a result of accumulated resources. Thus, these variable resources could be allocated to immune defence and, consequently, body size may explain part of the variation in immune responsiveness. However, the influence of body size on immune defence is often overlooked. The present study investigates variations in haemocyte count and phenoloxidase activity in larvae of the phytophagous vine moth Eupoecilia ambiguella Hübner of the same age, although differing in body size. The measurements of immune function are made both when the insects are immunologically naïve and 24u2009h after a bacterial immune challenge. The base levels of these immune parameters do not covary with body size in naïve larvae. After the bacterial immune challenge, more haemocytes and phenoloxidase enzyme are mobilized, and the mobilization of these immune effectors is correlated positively with individual body size. Thus, larger larvae exhibit higher immunocompetence than smaller ones, suggesting that smaller larvae might be more vulnerable to infection. These results suggest that body size is probably an underestimated variable, which nevertheless modulates the insect immune system and should thus be considered as a covariate in insect immune system measurement. It is recommended therefore, that body size should be taken into account in ecological immunity studies with insects.

Geographical variation in parasitism shapes larval immune function in a phytophagous insect.

Two of the central goals of immunoecology are to understand natural variation in the immune system among populations and to identify those selection pressures that shape immune traits. Maintenance of the immune system can be costly, and both food quality and parasitism selection pressure are factors potentially driving immunocompetence. In tritrophic interactions involving phytophagous insects, host plants, and natural enemies, the immunocompetence of phytophagous insects is constrained by selective forces from both the host plants and the natural enemies. Here, we assessed the roles of host plants and natural enemies as selective pressures on immune variation among natural populations of Lobesia botrana. Our results showed marked geographical variation in immune defenses and parasitism among different natural populations. Larval immune functions were dependent of the host plant quality and were positively correlated to parasitism, suggesting that parasitoids select for greater investment into immunity in moth. Furthermore, investment in immune defense was negatively correlated with body size, suggesting that it is metabolically expensive. The findings emphasize the roles of host plants and parasitoids as selective forces shaping host immune functions in natural conditions. We argue that kinds of study are central to understanding natural variations in immune functions, and the selective forces beyond.

Defense strategies used by two sympatric vineyard moth pests.

Natural enemies including parasitoids are the major biological cause of mortality among phytophagous insects. In response to parasitism, these insects have evolved a set of defenses to protect themselves, including behavioral, morphological, physiological and immunological barriers. According to life history theory, resources are partitioned to various functions including defense, implying trade-offs among defense mechanisms. In this study we characterized the relative investment in behavioral, physical and immunological defense systems in two sympatric species of Tortricidae (Eupoecilia ambiguella, Lobesia botrana) which are important grapevine moth pests. We also estimated the parasitism by parasitoids in natural populations of both species, to infer the relative success of the investment strategies used by each moth. We demonstrated that larvae invest differently in defense systems according to the species. Relative to L. botrana, E. ambiguella larvae invested more into morphological defenses and less into behavioral defenses, and exhibited lower basal levels of immune defense but strongly responded to immune challenge. L. botrana larvae in a natural population were more heavily parasitized by various parasitoid species than E. ambiguella, suggesting that the efficacy of defense strategies against parasitoids is not equal among species. These results have implications for understanding of regulation in communities, and in the development of biological control strategies for these two grapevine pests.

Immune benefits from alternative host plants could maintain polyphagy in a phytophagous insect.

The tritrophic interactions hypothesis, integrating bottom-up (plant-herbivore) and top-down (herbivore-natural enemies) effects, predicts that specialist herbivores should outcompete generalists. However, some phytophagous insects have generalist diets, suggesting that maintenance of a diverse diet may confer certain fitness advantages that outweigh diet specialization. In field conditions, the European grapevine moth, Lobesia botrana, feeds on diverse locally rare alternative host plants (AHPs) although grapevines are a highly abundant and predictable food source. The laboratory studies presented here show that survival, growth, and constitutive levels of immune defences (concentration of haemocytes and phenoloxidase activity) of L. botrana larvae were significantly enhanced when they were fed AHPs rather than grape. These results indicated a strong positive effect of AHPs on life history traits and immune defences of L. botrana. Such positive effects of AHPs should be advantageous to the moth under heavy selective pressure by natural enemies and, as a consequence, favour the maintenance of a broad diet preference in this species. We therefore believe that our results account for the role of immunity in the maintenance of polyphagy in phytophagous insects.

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.

Age, pathogen exposure, but not maternal care shape offspring immunity in an insect with facultative family life

BackgroundTo optimize their resistance against pathogen infection, individuals are expected to find the right balance between investing into the immune system and other life history traits. In vertebrates, several factors were shown to critically affect the direction of this balance, such as the developmental stage of an individual, its current risk of infection and/or its access to external help such as parental care. However, the independent and/or interactive effects of these factors on immunity remain poorly studied in insects.ResultsHere, we manipulated maternal presence and pathogen exposure in families of the European earwig Forficula auricularia to measure whether and how the survival rate and investment into two key immune parameters changed during offspring development. The pathogen was the entomopathogenic fungus Metarhiziumbrunneum and the immune parameters were hemocyte concentration and phenol/pro-phenoloxidase enzyme activity (total-PO). Our results surprisingly showed that maternal presence had no effect on offspring immunity, but reduced offspring survival. Pathogen exposure also lowered the survival of offspring during their early development. The concentration of hemocytes and the total-PO activity increased during development, to be eventually higher in adult females compared to adult males. Finally, pathogen exposure overall increased the concentration of hemocytes—but not the total-PO activity—in adults, while it had no effect on these measures in offspring.ConclusionsOur results show that, independent of their infection risk and developmental stage, maternal presence does not shape immune defense in young earwigs. This reveals that pathogen pressure is not a universal evolutionary driver of the emergence and maintenance of post-hatching maternal care in insects.

The relative abundance of hemocyte types in a polyphagous moth larva depends on diet.

Hemocytes are crucial cells of the insect immune system because of their involvement in multiple immune responses including coagulation, phagocytosis and encapsulation. There are various types of hemocytes, each having a particular role in immunity, such that variation in their relative abundance affects the outcome of the immune response. This study aims to characterize these various types of hemocytes in larvae of the grapevine pest insect Eupoecilia ambiguella, and to assess variation in their concentration as a function of larval diet and immune challenge. Four types of hemocytes were found in the hemolymph of 5th instar larvae: granulocytes, oenocytoids, plasmatocytes and spherulocytes. We found that the total concentration of hemocytes and the concentration of each hemocyte type varied among diets and in response to the immune challenge. Irrespective of the diet, the concentration of granulocytes increased following a bacterial immune challenge, while the concentration of plasmatocytes and spherulocytes differentially varied between larval diets. The concentration of oenocytoids did not vary among diets before the immune challenge but varied between larval diets in response to the challenge. These results suggest that the resistance of insect larvae to different natural enemies critically depends on the effect of larval diet on the larvaes investment into the different types of hemocytes.

Lobesia botrana larvae develop faster in the presence of parasitoids.

To combat parasitism hosts often rely on their immune system, which is the last line of defense. However, the immune system may not always be effective, and other non-immunological defenses might be favored to reduce the cost of parasite infection. Here we report that larvae of the moth Lobesia botrana can rapidly accelerate their development and reach maturity earlier in response to cues perceived at a distance from parasitoids. Such a phenotypically plastic life history shift, induced by the perception of deadly enemies in the environment, is likely to be an adaptive defensive strategy to prevent parasitoid attack, and has important implications in host–parasite dynamics.

Condition-Dependent Trade-Off Between Weapon Size and Immunity in Males of the European Earwig

Investigating the expression of trade-offs between key life-history functions is central to our understanding of how these functions evolved and are maintained. However, detecting trade-offs can be challenging due to variation in resource availability, which masks trade-offs at the population level. Here, we investigated in the European earwig Forficula auricularia whether (1) weapon size trades off with three key immune parameters – hemocyte concentration, phenoloxidase and prophenoloxidase activity - and whether (2) expression and strength of these trade-offs depend on male body condition (body size) and/or change after an immune challenge. Our results partially confirmed condition dependent trade-offs between weapon size and immunity in male earwigs. Specifically, we found that after an immune challenge, weapon size trades off with hemocyte concentrations in low-condition, but not in good-condition males. Contrastingly, weapon size was independent of pre-challenge hemocyte concentration. We also found no trade-off between weapon size and phenoloxidase activity, independent of body condition and immune challenge. Overall, our study reveals that trade-offs with sexual traits may weaken or disappear in good-condition individuals. Given the importance of weapon size for male reproductive success, our results highlight how low-condition individuals may employ alternative life-history investment strategies to cope with resource limitation.

Biological protection against grape berry moths. A review

Grape is a major crop, covering 7.5xa0Mxa0ha worldwide, that is currently being confronted with three main challenges: intensive pesticide use that must be reduced, invasion by new pests/diseases, and climate change. The biological control of pests and vectors would help address these challenges. Here, we review the scientific literature on the biological control of grape moths by macroorganisms (excluding nematodes). Two components, biological control with an active human role, mainly using biocontrol agents through inundation or inoculation, and conservation biological control, are considered. The major points are the following. (1) Tortricid grape moths seriously damage grapes worldwide, causing yield losses and quality reduction. The more geographically widespread species, Lobesia botrana, continues to extend its range, invading South American and, more recently, North American vineyards. (2) Parasitoids and predators (including arthropods, birds, and bats) that can control grape pests are very diverse. (3) Different methods exist to assess pest control efficiency in the field but some of them remain to be developed. (4) Environmental factors, including host plants, landscape, grass or floral covers, and organic practices, affect the natural control of grape moths. (5) Pest resistance to parasitoids strongly depends on their immune system, which is controlled by the host plant. Future climate changes may modify this tritrophic interaction and thus affect biological control strategies. We conclude that biological control has a great deal of potential in viticulture and that addressing these key factors would improve the efficiency levels of biological control strategies. This would help growers and stakeholders to significantly reduce insecticide use in vineyards.