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Host Selection by the Olfactory System in Drosophila Suzukii

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Host Selection by the Olfactory System in Drosophila Suzukii Encoding of fruit odours by the peripheral olfactory system in Drosophila suzukii: Fruitprints for host selection and prospects for sustainable management Claire France Nicolle Duménil Thesis submitted for the degree of Doctor of Philosophy on 30th September 2019 Defended on 13th February 2020 Cardiff University The work for this thesis was supervised by: Doctor Wynand van der Goes van Naters1 (Principal investigator) Doctor Michael Birkett2 Professor William Symondson1 Professor John Pickett3 Doctor József Vuts2 Doctor Jing-Jiang Zhou2 The thesis was examined by: Doctor James Hodge4 Doctor Carsten Muller1 1 Cardiff School of Biosciences, Cardiff University, United Kingdom. 2 Department of Biointeractions and Crop Protection, Rothamsted Research, United Kingdom. 3 Cardiff School of Chemistry, Cardiff University, United Kingdom. 4 School of Physiology, Pharmacology and Neuroscience, Bristol University, United Kingdom. Work placement: Division of Molecular Biosciences, School of Biosciences, Cardiff University (UK) Department of Biointeraction and Crop Protection, Rothamsted Research (UK) Funding: The work undertaken from 1st October 2015 until 30th September 2019 was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) -funded South West Biosciences Doctoral Training Partnership (SWBioDTP) [grant reference BB/M009122/1]. Acknowledgments This 4-years project was a wonderful adventure. I owe the great pleasure to have worked on this project to Wynand, Bill and Mike, for having selected me as their candidate. I am very thankful to the SWBioDTP who granted the funding and for an excellent training program. I am grateful to the International Society of Chemical Ecology (ISCE), for awarding me a student travel bursary and a prize for best oral presentation at their 3rd Joined ISCE-APACE meeting. To the Society of Chemical Industry (SCI), Agriscience Chemical Biology and the Royal Entomological Society for the opportunity to present my work to international scientific audiences and for awarding me a prize on a Twitter competition, a Poster presentation and an article describing my work in an issue of Antennae. For their contribution to my PhD work, many thanks to John Caulfield, Christine Woodcock, David Withall, Keith Chamberlain and Stephen Powers (Research). For field observation, plant, insect collections and training: Alberto Grassi, Enzo Mescalchin and Claudio Ioriatti. (Fondazione Edmund Mach - Istituto Agrario di San Michele All'Adige) and Florian Sinn (Südtiroler Beratungsring für Obst- und Weinbau). Wynand, many thanks for your excellent teaching, very interesting discussions and experiments. I am thankful for your patience, optimism and enthusiasm. It was a pleasure to work with you and I am hopeful to continue to study insect olfaction and setup my own RIG someday. Mike, many thanks for your great hosting, advice and support. József, many thanks for your patience and for teaching me all techniques I needed. Working together was very enriching. John, Bill and Jing-Jiang, I thank you all for all your excellent advice, support and stories. To all of you, I am very happy we formed a team and I am looking forward to further meetings and collaborations. Many thanks to Astrid and Jean-Christophe for your enthusiasm, your support and teachings through and beyond my Msc degree. I am looking forward to working together again. I was surrounded by wonderful friends who listened to my complaints of non- behaving flies, and non-working equipment for four years. For your support, advice, our coffee breaks and our adventures: Thank you Gaia, Steffi, Lieselot, Irene, Anneka, Sandrine, Suzanne, Florence, Sarah, Matthew, Gareth, Karl. I am also grateful to Helen and Sonia, for their support and kindness. A mes parents, Merci de m’avoir toujours encouragé pendant mes études. Je vous suis reconnaissante de la liberté et de l’amour que vous m’avez apporté et qui m’ont beaucoup aidé à accomplir ce rêve. Je suis heureuse de vous rendre fiers. i << Fais de ta vie un rêve et de ton rêve une réalité >> - Antoine de Saint-Exupéry ii Summary The fly Drosophila suzukii is an invasive pest responsible for major economic losses in fruit industries. Females lay eggs through a punctured hole in the skin of ripening fruits which otherwise would be available for retail. Since 2010 the fly is included in the World Invasive Species Compendium, developed by CAB international (CABI) and on the Pest Alert List of the European Plant Protection Organization (EPPO) as an invasive agricultural pest threatening fruit production. Intensive research has been carried out to improve current management methods and develop Integrated Pest Management (IPM) techniques. One of the challenges is to develop species specific tools which require fundamental research on species-specific host selection processes. D. suzukii is also valuable to study host selection and the mechanisms of host detection in a polyphagous pest insect. It has a fascinating ecology and its close relatedness to one of the most intensively studied biological research models Drosophila melanogaster facilitates its study. Using a highly sensitive sensory system, females detect and select host plants to lay eggs in the ripening fruits. Semiochemicals released by these fruits may be used to lure them to traps or disrupt host detection. The aim of the research presented in this thesis was to determine how host fruit odours are encoded by the peripheral olfactory system in D. suzukii to enable host fruit detection and discrimination. The results provide a model of olfactory detection of hosts for polyphagous insects. The key result is that the peripheral olfactory system encodes ripe fruit odours via combinations of only a few classes of olfactory receptor neurons (ORNs). The combinatorial activation of the fruit specific ORNs guides host selection behaviour and enables the flies to discriminate among oviposition substrates. This model offers a novel approach for identifying semiochemicals to use in pest management. It enables a rapid screen of chemicals for potential attraction to oviposition sites by determining if the responses they elicit are part of the fruitprint: the pattern of neuron activity induced by host-fruit odours in the peripheral olfactory system. iii Table of contents Acknowledgments .................................................................................................................................. i Summary .............................................................................................................................................. iii Table of contents .................................................................................................................................. iv Table of figures ..................................................................................................................................... xi List of tables ........................................................................................................................................xiii List of abbreviations ............................................................................................................................ xiv List of chemicals ................................................................................................................................. xvi 1 GENERAL INTRODUCTION ...................................................................................................... 1 1.1 DROSOPHILA SUZUKII ............................................................................................................. 2 1.1.1 Identity and description ................................................................................................... 2 1.1.1.1 Taxonomy ............................................................................................................................ 2 1.1.1.2 Morphology .......................................................................................................................... 2 1.1.1.3 Life cycle .............................................................................................................................. 3 1.1.2 Ecology for successful invasion ...................................................................................... 4 1.1.2.1 Host range ........................................................................................................................... 4 1.1.2.1.1 Fruit hosts ........................................................................................................................ 5 1.1.2.1.2 Susceptibility of cultivars .................................................................................................. 6 1.1.2.1.3 Hosts thorough the year .................................................................................................. 6 1.1.2.2 Geographic range ................................................................................................................ 6 1.1.2.3 Population dynamics ............................................................................................................ 7 1.1.2.4 Climatic conditions ............................................................................................................... 7 1.1.3 Management of an invasive agricultural pest .................................................................. 8 1.1.3.1 Extent of damages ..............................................................................................................
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