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.

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.

No abstract

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.

Summary1. 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. 2. 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. 3. 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. 4. 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. 5. 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.

Precise and comprehensive data on resource allocation into individual eggs are rare and this empirical void in the literature of life history strategies contrasts with the large number of theoretical studies. We show a marked decrease in reproductive investment in eggs with mother's age for egg size, sugar, protein, lipid and energy contents of eggs for a parasitic wasp. Egg size is a good predictor of offspring fitness, measured as survival of starving neonate larvae, but does not reveal possible biochemical changes. Lipids stabilize quickly at a minimal threshold while proteins and sugars decrease smoothly down to about 30% of the amount invested in the first egg. Because proteins have the highest correlation with egg size, we predict that they should be better predictors of larval fitness than lipids and sugars. Assessing the adaptive value of the observed patterns will require a multidimensional approach to egg provisioning.

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 reserves are burned at a high rate for maintenance and can be used to predict lifetime in absence of hosts. The model without hosts is adequate, but the one with hosts is not, as it predicts a continuous increase of proteins from the massive host‐feeding intake, contrasting with the observed decline. A good prediction of time of death could be achieved in that model by assuming that the large amounts of ingested proteins and carbohydrates from host‐feeding are used for maintenance, thereby enabling females to spare lipids for reproduction. We tested this assumption in a treatment with hosts and supplemental sugars, in which the maximal number of produced eggs is expected to be almost exclusively a function of lipids when other nutrients can be obtained to cover maintenance costs. Our results enable us to discriminate between competing hypotheses about nutrient allocation in models of parasitoid behavior and host–parasitoid population dynamics. They show that E. vuilletti is both a capital breeder for lipids and an income breeder for sugars, implying that this dichotomy is best superseded by a multidimensional and dynamical approach to nutrient acquisition and allocation.

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.