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Social and Environmental Olfactory Signals Mediate Insect Behavioral Ecology and Evolution

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Social and Environmental Olfactory Signals Mediate Insect Behavioral Ecology and Evolution Acta Universitatis Agriculturae Sueciae Acta Universitatis Agriculturae Sueciae • 2016:65 No. Thesis Doctoral Doctoral Thesis No. 2016:65 Doctoral Thesis No. 2016:65 Insect pheromones are released into an atmosphere filled with Faculty of Landscape Architecture, Horticulture environmental odors. I studied the combined effect of habitat Social and Environmental Olfactory Signals Mediate Insect Behavioral Ecology and Evolution and Crop Production Science odors and pheromones on specific mate recognition in the cotton leafworm, Spodoptera littoralis, and the common fruit fly,Drosophila melanogaster. My findings show that the blend of pheromones and Social and Environmental Olfactory host volatiles functions as a single unit in mediating insect mate finding behavior, rather than as individual components. Deviations Signals Mediate Insect Behavioral from the optimal blend, through a suboptimal pheromone or host Ecology and Evolution volatile blend, strongly reduce its behavioural effect on insect attraction. Felipe Borrero-Echeverry Felipe Borrero-Echeverry completed his graduate education at the Department of Plant Protection Biology at SLU, Alnarp. He received his M.Sc. in Biology from Los Andes University, Bogotá, Colombia. Acta Universitatis Agriculturae Sueciae presents doctoral theses from the Swedish University of Agricultural Sciences (SLU). SLU generates knowledge for the sustainable use of biological natural resources. Research, education, extension, as well as environmental • Felipe Borrero-Echeverry monitoring and assessment are used to achieve this goal. Online publication of thesis summary: http://pub.epsilon.slu.se/ ISSN 1652-6880 ISBN (print version) 978-91-576-8632-9 ISBN (electronic version) 978-91-576-8633-6 Acta Universitatis Agriculturae Sueciae Doctoral Thesis No. 2016:65 Insect pheromones are released into an atmosphere filled with environmental odors. I studied the combined effect of habitat odors and pheromones on specific mate recognition in the cotton leafworm, Spodoptera littoralis, and the common fruit fly,Drosophila melanogaster. My findings show that the blend of pheromones and host volatiles functions as a single unit in mediating insect mate finding behavior, rather than as individual components. Deviations from the optimal blend, through a suboptimal pheromone or host volatile blend, strongly reduce its behavioural effect on insect attraction. Felipe Borrero-Echeverry completed his graduate education at the Department of Plant Protection Biology at SLU, Alnarp. He received his M.Sc. in Biology from Los Andes University, Bogotá, Colombia. Acta Universitatis Agriculturae Sueciae presents doctoral theses from the Swedish University of Agricultural Sciences (SLU). SLU generates knowledge for the sustainable use of biological natural resources. Research, education, extension, as well as environmental monitoring and assessment are used to achieve this goal. Online publication of thesis summary: http://pub.epsilon.slu.se/ ISSN 1652-6880 ISBN (print version) 978-91-576-8632-9 ISBN (electronic version) 978-91-576-8633-6 Social and Environmental Olfactory Signals Mediate Insect Behavioral Ecology and Evolution Felipe Borrero-Echeverry Faculty of Landscape Architecture, Horticulture and Crop Production Science Department of Plant Protection Biology Alnarp Doctoral Thesis Swedish University of Agricultural Sciences Alnarp 2016 Acta Universitatis Agriculturae Sueciae 2016:65 Cover: Spodoptera on a banana (photo: Cyrus Mahmoudi, Comgraphix) ISSN 1652-6880 ISBN (print version) 978-91-576-8632-9 ISBN (electronic version) 978-91-576-8633-6 © 2016 Felipe Borrero-Echeverry, Alnarp Print: SLU Service/Repro, Alnarp 2016 Social and Environmental Olfactory Signals Mediate Insect Behavioral Ecology and Evolution Abstract Odors are essential in mediating insect reproductive behavior. Environmental odors help insects locate suitable feeding or egg-laying sites and avoid suboptimal hosts or dangerous habitats. Sex pheromones, on the other hand, are responsible for mate find- ing and elicit courtship and mating. Although pheromones elicit stereotypical behaviors on their own, they are embedded in a background of environmental odors in nature. Using the cotton leafworm, Spodoptera littoralis, and the common fruit fly, Drosophila melanogaster, I studied the effect of blending environmentally relevant odors with pheromones on insect behavior. For the cotton leafworm, we first developed an attractive cotton volatile blend. We next used this blend to determine the physiological effect of DMNT, a strong behavior- al antagonist, on the cotton leafworm olfactory system. I then blended the individual volatiles and volatile blends with an incomplete and complete pheromone. The combi- nation of cotton volatiles and the complete pheromone elicits attraction. Deviations from this optimum, either by changing the pheromone composition or the cotton vola- tile blend strongly reduces male S. littoralis attraction. I then used the fruit fly to study the effect of food (vinegar) and habitat (yeast) vola- tiles on fly attraction towards pheromones. Starvation affects attraction towards a blend of vinegar and a male produced pheromone in a sexually dimorphic way. We next de- scribe a novel female fruit fly pheromone and the odorant receptor involved in its per- ception. Finally, we show that vinegar and yeast volatiles interact in a different manner with male and female produced pheromones, suggesting that although vinegar is a good feeding cue, even in the presence of pheromones, it is not an appropriate mate finding cue. My findings suggest that pheromones and host volatiles function as a single unit that mediates insect behavior, rather than as individual components. As such the olfactory cues that mediate mate finding in insects are under both natural and sexual selection simultaneously, which has strong implications for insect speciation and evolution. Keywords: Spodoptera littoralis, Drosophila melanogaster, pheromones, host volatiles, chemical ecology, olfaction, host plant volatiles, herbivore-induced plant volatiles, sexual selection, natural selection Author’s address: Felipe Borrero-Echeverry, SLU, Department of Plant Protection Biology, P.O. Box 102, 230 53, Alnarp, Sweden E-mail: [email protected] Dedication To those who find my present and future work interesting. See that the imagination of nature is far, far greater than the imagination of man. Richard P. Feynman Contents List of Publications 7 Abbreviations 10 1 Introduction 11 1.1 Insect chemical ecology 11 1.2 Model organisms 12 1.2.1 Spodoptera littoralis 12 1.2.2 Drosophila melanogaster 14 1.3 Insect olfaction 15 1.3.1 Overview 15 1.3.2 Olfaction in S. littoralis 17 1.3.3 Olfaction in D. melanogaster 19 1.4 Pheromones in insects 20 1.4.1 Overview 20 1.4.2 Pheromones in S. littoralis 21 1.4.3 Pheromones in D. melanogaster 22 1.5 Host volatile use by insects 23 1.5.1 Overview 23 1.5.2 Host plant volatiles and S. littoralis 23 1.5.3 Host volatiles and D. melanogaster 24 1.6 Interactions between pheromones and host volatiles 24 1.7 Applied aspects 25 1.7.1 Overview 25 1.7.2 Semiochemicals in Spodoptera control 27 1.7.3 Semiochemicals in Drosophila control 28 2 Aim and objectives 29 3 Summary of results and discussion 31 3.1 Part I: Interactions between host plant volatiles and pheromones in the cotton leafworm 31 3.2 Part II: Interactions between feeding cues, host volatiles and pheromones in the Common Fruit Fly 36 4 Concluding remarks 41 5 Perspectives 43 References 45 Acknowledgements 59 List of Publications This thesis is based on the work contained in the following papers, referred to by Roman numerals in the text: I Borrero-Echeverry, F., Becher, P.G., Birgersson, G.Å.O., Bengtsson, M., Witzgall, P., and Saveer, A.M. (2015). Flight attraction of Spodoptera litto- ralis (Lepidoptera, Noctuidae) to cotton headspace and synthetic volatile blends. Frontiers in Ecology and Evolution 3, 56. II Hatano, E., Saveer, A., Borrero-Echeverry, F., Strauch, M., Zakir, A., Bengtsson, M., Ignell, R., Anderson, P., Becher, P., Witzgall, P., and Dek- ker, T. (2015). A herbivore-induced plant volatile interferes with host plant and mate location in moths through suppression of olfactory signaling pathways. BMC Biology 13, 75. III Borrero-Echeverry, F., Bengtsson, M., Witzgall, P. Blends of host plant volatiles and sex pheromones encode specific mate recognition in moths. (Manuscript). IV Lebreton, S., Borrero-Echeverry, F., Gonzalez, F., Solum, M., Wallin, E., Trona, F., Grabe, V., Sachse, S., Hedenström, E., Hansson, B.S., Bengtsson, M., Birgersson, G., Walker, W.B., Dweck, H., Witzgall, P., Becher, P. (2015). Feeding regulates sex pheromone attraction and courtship in Dro- sophila females. Scientific Reports 5, 13132. V Lebreton S., Borrero-Echeverry F., Gonzalez F., Trona F., Solum M., Wallin E., Grabe V., Sachse S., Bengtsson M., Hansson B.S., Hedenström E., Birgersson G., Dweck H., Witzgall P., Becher P.G. 2016. The scent of the fly. (Manuscript). 7 VI Borrero-Echeverry F., Witzgall, P., Becher, P.G. Drosophila sex phero- mones synergize vinegar and yeast attraction. (Manuscript) Papers I, II & IV are reproduced with the permission of the publishers under Creative Commons Licenses. 8 The contribution of Felipe Borrero-Echeverry to the papers included in this thesis was as follows: I Carried out wind tunnel experiments on male moths, analyzed the data and wrote the manuscript with the co-authors. II Carried out wind tunnel experiments, analyzed wind tunnel data and assist- ed
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