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Anlage 4 Der Promotionsordnung Gemäß Ecological Immunology and Host Plant Adaptation in Lepidopteran Herbivores Dissertation To Fulfill the Requirements for the Degree of „doctor rerum naturalium“ (Dr. rer. nat.) Submitted to the Council of the Faculty of Biology and Pharmacy of the Friedrich Schiller University Jena by Dipl-Biol. Andrea Barthel born on 31.07.1985 in Mühlhausen Das Promotionsgesuch wurde eingereicht und bewilligt am: 14.07.2014 Gutachter: 1. Prof. Dr. David G. Heckel 2. Prof. Dr. Rolf Beutel 3. Prof. Dr. Andreas Vilcinskas Das Promotionskolloquium wurde abgelegt am: 29.10.2015, Jena Contents 1 Contents Chapter 1: General Introduction ............................................................................................ 3 1.1 Innate immunity in insects ............................................................................................................ 3 1.1.1 Classical immune system ....................................................................................................... 3 1.1.2 Counteracting the insect immunity: Bacillus thuringiensis and Serratia entomophila ......... 7 1.1.3 Ecological immunology ......................................................................................................... 8 1.2 Trade-offs in life-history: Consequences of the innate immune response in insects .................. 12 1.3 Insects, plants and their complex interactions ............................................................................. 14 1.3.1 Specialist - generalist paradigm ........................................................................................... 14 1.3.2 Plant-herbivore interactions in a tritrophic context ............................................................. 16 1.3.3 Study organisms: Heliothis subflexa and Heliothis virescens ............................................. 17 1.4 Aim of this thesis ........................................................................................................................ 20 Chapter 2: Overview of Manuscripts ................................................................................... 23 Chapter 3: Manuscript I ........................................................................................................ 26 3.1 Abstract ....................................................................................................................................... 26 3.2 Introduction ................................................................................................................................. 27 3.3 Material and Methods ................................................................................................................. 29 3.4 Results ......................................................................................................................................... 31 3.5 Discussion ................................................................................................................................... 37 3.6 Supplementary Material .............................................................................................................. 42 Chapter 4: Manusript II ........................................................................................................ 52 4.1 Abstract ....................................................................................................................................... 52 4.2 Introduction ................................................................................................................................. 53 4.3 Material and Methods ................................................................................................................. 55 4.4 Results ......................................................................................................................................... 60 4.5 Discussion ................................................................................................................................... 64 4.6 Supplementary Material .............................................................................................................. 68 Chapter 5: Manuscript III ..................................................................................................... 72 5.1 Abstract ....................................................................................................................................... 72 5.2 Introduction ................................................................................................................................. 73 5.3 Material and Methods ................................................................................................................. 75 5.4 Results ......................................................................................................................................... 81 5.5 Discussion ................................................................................................................................... 87 5.6 Supplementary Material .............................................................................................................. 91 2 Contents Chapter 6: General Discussion .............................................................................................. 96 6.1 Network of interactions affecting immune system functions in herbivores ................................ 96 6.2 Trade-offs associated with immunity in herbivores .................................................................. 105 6.3 Interactions among Physalis plants, the specialist H. subflexa and B. thuringiensis ................ 109 Chapter 7: Summary ........................................................................................................... 114 7.1 Environmental factors have an impact on immune defense strategies of the generalist Heliothis virescens and the specialist Heliothis subflexa ................................................................ 114 7.2 Immune system activation induces changes in sexual traits of H. virescens females ............... 115 7.3 Tritrophic interactions play an important role in the adaptation of the specialist H. subflexa on Physalis plants............................................................................................................................ 116 Chapter 8: Zusammenfassung ............................................................................................ 118 8.1 Umweltfaktoren haben einen Einfluss auf die Funktionsweise des Immunsystems im Generalisten Heliothis virescens und im Spezialisten Heliothis subflexa ....................................... 118 8.2 Die Aktivierung des Immunsystems induziert Veränderungen in der Reproduktion von weiblichen H. virescens .................................................................................................................. 119 8.3 Tritrophische Interaktionen spielen eine wichtige Rolle in der Adaption des Spezialisten H. subflexa an Physalis-Pflanzen .................................................................................................... 120 Chapter 9: References .......................................................................................................... 122 Chapter 10: Acknowledgements ......................................................................................... 145 Chapter 11: Curriculum vitae ............................................................................................. 148 Chapter 12: Selbstständigkeitserklärung ........................................................................... 152 Chapter 1: General Introduction 3 1 General Introduction One of the most fascinating aspects of nature is the complexity of ecosystems, wherein herbivorous insects and plants represent about one half of the world’s macroscopic biodiversity (Strong et al. 1984). Since herbivorous insects cannot exist in the absence of plants, insects and plants have developed a reciprocal co-evolutionary relationship (Ehrlich and Raven 1964). Just as herbivorous insects exploit various plant habitats, microorganisms have evolved to attack these insects. This has created the situation where insects require a range of efficient defense mechanisms to cope with all potential pathogens as specifically and immediately as possible. Since environments differ in their threats they pose, immune system variation is high between individual herbivores (Sadd and Schmid-Hempel 2009). Ecological immunology attempts to explain these variations by invoking evolutionary costs and trade- offs between immunity and other life history traits (Sadd and Schmid-Hempel 2009). Studies on insect ecology and the driving forces for immune system variation are essential to better understand immunity in the context of natural environments. 1.1 Innate immunity in insects 1.1.1 Classical immune system Immediately upon hatching an insect faces many challenges from opportunistic bacteria, parasites, viruses as well as potentially pathogenic organisms. Obviously, protection against these challenges requires an efficient immune system that can cope with all potential pathogens as specifically and immediately as possible. Insects represent the most diverse group of all known animal species on earth and have successfully conquered almost all environments (May 1988). To cope with certain aspects of this environmental variety, insects have evolved a multilayered innate immune system consisting of various defense mechanisms that are similar to many aspects of the vertebrate innate immune
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