Microbiota turnover during complete metamorphosis: cause or consequence?

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The insects are the most diverse group of animals, with almost 1 million species being described. The vast majority of insects undergoes complete metamorphosis, a radical re-organization of the whole body including the destruction and de novo assembly of almost all organs during development. The adaptive advantage of such life history is not clear. The complete re-organization of the body comes at a cost: the loss of the gut microbiota during complete rebuilding of the gut the possible risk of opportunistic infections. Alternatively, this re-organization constitutes a significant adaptive advantage: the radical re-organization of the body including the gut allows resetting the microbiota. This results in the ability to use different sources of food in the larval and adult stage and occupy different niches more easily. The project has three main objectives. 1) To compare the changes in the gut microbiota throughout development in holo- and hemimetabolous insects. I predict that the gut microbiota of holometabolous insects undergoes significant changes both in abundance and composition during metamorphosis while hemimetabolous insects show a linear increase. This will be investigated by sampling species from the major insect orders across the life stages.2) To test whether microbiota turnover is under the control of host gut immunity. The prediction is that genes are up-regulated throughout metamorphosis independent of the gut microbiota and that the host immune system controls the gut microbiota during metamorphosis. This will be studied using RNAseq analysis of different developmental stages in specimens of holo-and hemimetabolous insects. Highly expressed immune genes will be knocked-down to experimentally demonstrate the role of the host immune system to shape changes in the gut microbiota. Objective 3) will experimentally change the gut microbiota during ontogeny as proof of principle of the adaptive value of complete metamorphosis. In short, hemimetabolous insects will undergo a microbiota turnover similar to holometabolous insects. Hemimetabolous insects can be adapted to a new diet, by changing the gut microbiota experimentally before adult eclosion. This will be achieved by experimental manipulation of the gut microbiota in selected hemimetabolous insects using antibiotics and microbiota transplants. This research program will generate significant new insight to answer the question why complete metamorphosis of insects evolved and hence contribute to our understanding of the diversification of the most diverse group of multicellular life, the holometabolous insects.