David Giron

LIFETIME NUTRIENT DYNAMICS REVEAL SIMULTANEOUS CAPITAL AND INCOME BREEDING IN A PARASITOID

Models of host handling decisions and physiologically structured host–parasitoid population dynamics make diverging assumptions, untested as of this writing, about the allocation rules of nutrients to survival and reproduction. Our aim is to develop a data-rich multidimensional dynamical budget of nutrient acquisition and allocation in survival and reproduction in the host-feeding, synovigenic bruchid ectoparasitoid Eupelmus vuilletti (Hymenoptera: Eupelmidae) over the entire lifetime of the animal in order to address the above questions. We quantified sugar, glycogen, protein, and lipid reserves of single females at birth and death and their daily maintenance needs. We recorded each host-feeding and oviposition event over entire lifetimes and quantified the amounts acquired and invested in eggs using microcolorimetric techniques. We then built two nutrient budgets, with and without hosts, encompassing 20 measured biochemical parameters and tested their predictions using time of death. Carbohydrate reserv...

Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts

The life cycles of many organisms are constrained by the seasonality of resources. This is particularly true for leaf-mining herbivorous insects that use deciduous leaves to fuel growth and reproduction even beyond leaf fall. Our results suggest that an intimate association with bacterial endosymbionts might be their way of coping with nutritional constraints to ensure successful development in an otherwise senescent environment. We show that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts, most likely Wolbachia, to manipulate the physiology of its host plant resulting in the ‘green-island’ phenotype—photosynthetically active green patches in otherwise senescent leaves—and to increase its fitness. Curing leaf-miners of their symbiotic partner resulted in the absence of green-island formation on leaves, increased compensatory larval feeding and higher insect mortality. Our results suggest that bacteria impact green-island induction through manipulation of cytokinin levels. This is the first time, to our knowledge, that insect bacterial endosymbionts have been associated with plant physiology.

A specialist root herbivore exploits defensive metabolites to locate nutritious tissues

The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.

Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence

Summary Plant hormones play important roles in regulating plant growth and defence by mediating developmental processes and signalling networks involved in plant responses to a wide range of parasitic and mutualistic biotic interactions. Plants are known to rapidly respond to pathogen and herbivore attack by reconfiguring their metabolism to reduce pathogen/herbivore food acquisition. This involves the production of defensive plant secondary compounds, but also an alteration of the plant primary metabolism to fuel the energetic requirements of the direct defence. Cytokinins are plant hormones that play a key role in plant morphology, plant defence, leaf senescence and source–sink relationships. They are involved in numerous plant–biotic interactions. These phytohormones may have been the target of arthropods and pathogens over the course of the evolutionary arms race between plants and their biotic partners to hijack the plant metabolism, control its physiology and/or morphology and successfully invade the plant. In the case of arthropods, cytokinin-induced phenotypes can be mediated by their bacterial symbionts, giving rise to intricate plant–microbe–insect interactions. Cytokinin-mediated effects strongly impact not only plant growth and defence but also the whole community of insect and pathogen species sharing the same plant by facilitating or preventing plant invasion. This suggests that cytokinins (CKs) are key regulators of the plant growth-defence trade-off and highlights the complexity of the finely balanced responses that plants use while facing both invaders and mutualists.

Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition.

Kin selection theory predicts that individuals will show less aggression and more altruism towards relatives. However, recent theoretical developments suggest that with limited dispersal, competition between relatives can override the effects of relatedness. The predicted and opposing influences of relatedness and competition are difficult to approach experimentally because conditions that increase average relatedness among individuals also tend to increase competition. Polyembryonic wasps in the family Encyrtidae are parasites whose eggs undergo clonal division to produce large broods. These insects have also evolved a caste system: some embryos in a clone develop into reproductive larvae that mature into adults, whereas others develop into sterile soldier larvae that defend siblings from competitors. In a brood from a single egg, reproductive altruism by soldiers reflects clone-level allocation to defence at the cost of reproduction, with no conflict between individuals. When multiple eggs are laid into a host, inter-clone conflicts of interest arise. Here we report that soldier aggression in Copidosoma floridanum is inversely related to the genetic relatedness of competitors but shows no correlation with the level of resource competition.

Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect

In holometabolous insects reproductive success is strongly determined by the nutritional resources available to the females. In addition to nutrients derived from adult feeding, resources for egg production may come from the limited reserves accumulated during the larval stages. The pattern of allocation of these larval reserves to egg production is expected to be strongly linked to the nutritional ecology of the adult. We investigate the temporal pattern of allocation of larval reserves to reproduction in a host–feeding parasitoid wasp. As predicted by the dynamics of allocation of an adult meal, larval reserves are the main source of nutrients for four or five days after emergence. However, despite the high frequency of host–feeding and the high nutrient content of a haemolymph meal, which we predicted would lead to larval reserves being conserved in the event of host deprivation, larval reserves contribute to egg production throughout the lifetime of the female. We propose several mechanistic and adaptive explanations for our results, including the possible existence of a limiting or key nutrient for egg production of exclusively larval origin. We make further predictions concerning the pattern of allocation of larval resources in parasitoids with different adult nutritional requirements.

Lipogenesis in an adult parasitic wasp

The goal of this study was to determine the extent of lipogenesis in the parasitoid Eupelmus vuilletti (Hymenoptera: Eupelmidae). Carbohydrate and lipid metabolism were followed in glucose-fed and starved females over 3 days. Fed females increased their glycogen level, while maintaining their lipid level. Starved females used most of their glycogen, while maintaining their lipid level too. Thus, females either use exclusively sugars to preserve their lipid reserves, or maintained a steady renewal of lipids through lipogenesis. The incorporation of radioactively marked glucose into lipids showed however that lipogenesis did not occur at a sufficient level to increase lipid reserves and to compensate for lipid use. This result has important implications for understanding nutrients allocation strategy in this species as the amount of lipids is almost totally fixed upon the emergence. From an evolutionary perspective, we call for detailed physiological studies of lipogenesis in a wide range of adult hymenopterans, as the absence of lipogenesis could be common to all of Aculatea.

Cytokinin-mediated leaf manipulation by a leafminer caterpillar.

A large number of hypotheses have been proposed to explain the adaptive significance and evolution of the endophagous-feeding mode, nutritional benefits being considered to be one of the main advantages. Leaf-mining insects should feed on most nutritional tissues and avoid tissues with high structural and/or biochemical plant defences. This selective feeding behaviour could furthermore be reinforced by manipulating the plant physiology, as suggested by the autumnal formation of ‘green islands’ around mining caterpillars in yellow leaves. The question we address here is how such metabolic manipulation occurs and what the nutritional consequences for the insect are. We report a large accumulation of cytokinins in the mined tissues which is responsible for the preservation of functional nutrient-rich green tissues at a time when leaves are otherwise turning yellow. The analogy with other plant manipulating organisms, in particular galling insects, is striking.

Lifetime gains of host‐feeding in a synovigenic parasitic wasp

Abstract.  Understanding behavioural decisions relative to host use for feeding or reproduction by foraging parasitoids requires not only the study of metabolic pathways followed by nutrients, but also the quantification of lifetime fitness gains of each alternative behaviour. By using a combination of observational and manipulative approaches, the lifetime host‐feeding gains are measured both in terms of fecundity and longevity in the parasitoid Eupelmus vuilletti. Host‐feeding increases both egg production and longevity. The increase in fecundity is mainly determined by the amount of lipids obtained whereas the lifespan extension is mainly determined by carbohydrates. Proteins obtained through host‐feeding have been implicated previously in egg production by parasitoids but protein intake has no effect on fecundity and longevity in E. vuilletti. The amount of nutrients gained through host‐feeding and invested in eggs is variable and changes over the lifetime of the animal. Therefore, lifetime feeding gains are best understood through the construction of dynamical budgets running over the entire lifespan of an insect.

Plant–insect interactions under bacterial influence: ecological implications and underlying mechanisms

Plants and insects have been co-existing for more than 400 million years, leading to intimate and complex relationships. Throughout their own evolutionary history, plants and insects have also established intricate and very diverse relationships with microbial associates. Studies in recent years have revealed plant- or insect-associated microbes to be instrumental in plant-insect interactions, with important implications for plant defences and plant utilization by insects. Microbial communities associated with plants are rich in diversity, and their structure greatly differs between below- and above-ground levels. Microbial communities associated with insect herbivores generally present a lower diversity and can reside in different body parts of their hosts including bacteriocytes, haemolymph, gut, and salivary glands. Acquisition of microbial communities by vertical or horizontal transmission and possible genetic exchanges through lateral transfer could strongly impact on the host insect or plant fitness by conferring adaptations to new habitats. Recent developments in sequencing technologies and molecular tools have dramatically enhanced opportunities to characterize the microbial diversity associated with plants and insects and have unveiled some of the mechanisms by which symbionts modulate plant-insect interactions. Here, we focus on the diversity and ecological consequences of bacterial communities associated with plants and herbivorous insects. We also highlight the known mechanisms by which these microbes interfere with plant-insect interactions. Revealing such mechanisms in model systems under controlled environments but also in more natural ecological settings will help us to understand the evolution of complex multitrophic interactions in which plants, herbivorous insects, and micro-organisms are inserted.