Phytophagous insects can be divided in two large groups according to their feeding habit: ectophages feeding externally on plant tissues and endophages living concealed within plant tissues and feeding internally. In spite of a reasonable understanding of the history and origins of the endophagous feeding habit, its evolution and adaptive significance remains unclear. Three major hypotheses have been proposed to explain the endophagous-feeding life history mode: The nutrition hypothesis, the microenvironment hypothesis and the enemy hypothesis. Among these hypotheses, feeding selectively on the most nutritional tissues is undoubtedly considered as a major advantage and most probably played a major role in the emergence, evolution and/or radiation of the endophagous feeding mode. This behavior can also be reinforced by manipulating the plant physiology and gall-inducer arthropods are usually distinguished from other insect-generated shelters by the fact that they involve active plant physiological alterations such as the differentiation of additional tissues to feed on, the upregulation of protein and/or sugar synthesis in situ, and/or the modification of source-sink relationships leading to nutrient translocation towards the insect’s feeding site. However, plant manipulation appears not to be restricted to gall-inducers only, as suggested by the autumnal formation of ‘green-islands’ around mining caterpillars in yellow leaves.
We aim to understand proximal and ultimate mechanisms at the basis of a plant-herbivore adaptive life-style. This necessitates studying the intimate molecular, biochemical and physiological mechanisms used by leaf-miner insects to manipulate their host-plant environment but also their fitness consequences for the insect.
Results/Conclusions
Our results on the Malus domestica/Phyllonorycter blancardella plant-leaf mining system show: (i) The ability of this leaf-miner caterpillar to manipulate its host plant in order to generate a microenvironment with all the nutrient supply needed for its survival. (ii) A decrease in plant defence compounds within the mined area. (iii) 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. (iv) The primary role played by endosymbiotic bacteria (Wolbachia) in the synthesis of these cytokinins and in the induction of nutrient-rich tissues. All together, these results clearly show the ability of leaf-miner insects to manipulate their host plant physiology and to create an “optimal” nutritional micro-environment through cytokinin production by their endosymbiotic partners. Wolbachia is suspected to play an essential role which, if this is the case, will be the first evidence of a Wolbachia-mediated effect on plant physiology.