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Modulating Male Aggression and Courtship: Detecting External Pheromonal and Nutritional Information

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Modulating Male Aggression and Courtship: Detecting External Pheromonal and Nutritional Information University of Montana ScholarWorks at University of Montana Graduate Student Theses, Dissertations, & Professional Papers Graduate School 2016 MODULATING MALE AGGRESSION AND COURTSHIP: DETECTING EXTERNAL PHEROMONAL AND NUTRITIONAL INFORMATION Jonathan C. Andrews University of Montana Follow this and additional works at: https://scholarworks.umt.edu/etd Let us know how access to this document benefits ou.y Recommended Citation Andrews, Jonathan C., "MODULATING MALE AGGRESSION AND COURTSHIP: DETECTING EXTERNAL PHEROMONAL AND NUTRITIONAL INFORMATION" (2016). Graduate Student Theses, Dissertations, & Professional Papers. 10931. https://scholarworks.umt.edu/etd/10931 This Dissertation is brought to you for free and open access by the Graduate School at ScholarWorks at University of Montana. It has been accepted for inclusion in Graduate Student Theses, Dissertations, & Professional Papers by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. MODULATING MALE AGGRESSION AND COURTSHIP: DETECTING EXTERNAL PHEROMONAL AND NUTRITIONAL BY JONATHAN ANDREWS B.A. in Human Biology, University of Montana, Missoula 2006 B.A. in Psychology, University of Montana, Missoula (2009) Dissertation/Thesis Presented in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in NEUROSCIENCE The University of Montana Missoula, MT December 2016 Approved by: Sandy Ross, Dean of The Graduate School Graduate School Sarah Certel, Advisor Department of Biological Sciences J. Stephen Lodmell, Chair Department of Biological Sciences Darrell Jackson Department of Biomedical and Pharmaceutical Sciences Fernando Cardozo-Pelaez Department of Biomedical and Pharmaceutical Sciences Chris Comer Dean of the College of Humanities and Sciences Jonathan Andrews 2016 2 Table of Contents Abstract…………..…………..…………..…………..…………..…………..…………..…………...……………7 Acknowledgements…………..…………..…………..…………..…………..…………..……………..……8 Chapter I…………..…………..…………..…………..…………..…………..…………..…………..…………...9 Introduction…………..…………..…………..…………..…………..…………..…………..………...9 Major contributions of Drosophila to neuroscience research…………..…………..9 Drosophila Behavior…………..…………..…………..…………..…………..…………..……….11 Commonalities in Drosophila behavior…………..…………..…………..…………..……..12 Drosophila aggression…………..…………..…………..…………..…………..…………..……..13 Cues affecting aggression…………..…………..…………..…………..…………..…………….14 Drosophila Courtship…………..…………..…………..…………..…………..…………..………15 Drosophila gustation…………..…………..…………..…………..…………..…………..……….15 Pheromone sensation…………..…………..…………..…………..…………..…………..……..19 Sensation of dietary sugars and bitter compounds…………..…………..…………....21 The Subesophageal zone of the Drosophila brain…………..…………..………………22 Octopaminergic signaling and Aggression…………..…………..…………..…………….24 Octopaminergic Signaling and Courtship…………..…………..…………..……………...25 OA in the Drosophila brain…………..…………..…………..…………..…………..…………..26 OA Structure and Synthesis…………..…………..…………..…………..…………..…………28 OA receptors…………..…………..…………..…………..…………..…………..…………..………28 OA in vertebrates…………..…………..…………..…………..…………..…………..……………30 Summary…………..…………..…………..…………..…………..…………..…………..……………31 Works Cited…………..…………..…………..…………..…………..…………..…………..………..32 Chapter II…………..…………..…………..…………..…………..…………..…………..…………..………...58 Foreword to Chapter II…………..…………..…………..…………..…………..…………..……58 Abstract…………..…………..…………..…………..…………..…………..…………..……………..59 Summary…………..…………..…………..…………..…………..…………..……………….……….59 Introduction…………..…………..…………..…………..…………..…………..…………..……….60 Results…………..…………..…………..…………..…………..…………..…………..…………..…...62 Gr32a neurons contact OA neurons in the suboesophageal ganglion………….62 Removing OA neurons changes Gr32a SOG axonal targeting…………..………….66 Gr32a expressing neurons mediate onset of aggression via OA signaling…...70 The intracellular Ca2+ response of OA SOG neurons to male CHCs requires Gr32a neurons…………..…………..…………..…………..…………..…………..…………..……75 Subset-specific effects of Gr32a neuronal function on male aggression and courtship selection…………..…………..…………..…………..…………..…………..………....78 Tissue-specific refinement of Gr32a to octopamine neuron synaptic contacts..…………..…………..…………..…………..……………………..…………....…………….80 3 Cell-specific refinement of octopamine neuron connections to Gr32a neurons….…………..…………..…………..…………..…………..…………..…………..…………..83 Discussion…………..…………..…………..…………..…………..…………..…………..………….86 Materials and Methods…………..…………..…………..…………..…………..…………..……90 References…………..…………..…………..…………..…………..…………..…………..………..107 Chapter III…………..…………..…………..…………..…………..…………..…………..…………..……..117 Introduction…………..…………..…………..…………..…………..…………..…………..……..117 Results…………..…………..…………..…………..…………..…………..…………..……………..120 Oaβ1R-expressing neurons are present in the legs and proboscis……………120 Octopamine administration causes an increase in cAMP levels in Oaβ1R- expressing neurons…………..…………..…………..…………..…………..…………..……….122 Oaβ1R-expressing neurons also express sugar sensors…………..…………..…...124 Octopamine administration alters neuronal excitability in the periphery…127 Oaβ1R-expressing neurons mediate onset and frequency of aggressive behavior…………..…………..…………..…………..…………..…………..…………..…………..130 Ablation of Oaβ1R-expressing neurons delays courtship and copulation…131 Males lacking the Oaβ1R receptor take longer to court and perform fewer wing threats…………..…………..…………..…………..…………..…………..…………..…….133 A subset of Oaβ1R-expressing neurons is required for male aggression…..135 Discussion…………..…………..…………..…………..…………..…………..…………..………..135 Future directions…………..…………..…………..…………..…………..…………..…………..139 Material and methods…………..…………..…………..…………..…………..…………..…...140 4 Table of Figures Chapter I Figure 1: Stereotyped aggressive and courtship behaviors in Drosophila…………..…………..…………..…………..…………..…………..……………16 Figure 2: Location and Structure of Gustatory Sensilla…………..………..18 Figure 3: Structure of Drosophila Pheromones…………..…………..……….20 Figure 4: The Drosophila brain…………..…………..…………..………………….23 Figure 5: OA in the Drosophila brain…………..…………..…………..………….27 Figure 6: Octopamine structure, synthesis, and receptors……………….29 Chapter II Figure 1: Gr32a neurons contact OA neurons in the suboesophageal ganglion.…………..…………..…………..…………..…………..…………..……………...64 Figure 2: Removing OA neurons significantly alters Gr32a axonal projections.…………..…………..…………………..…………..…………………..……...68 Figure 3: Gr32a-expressing neurons promote aggression via OA signaling.…………..…………..…………………..…………..……………………………...71 Figure 4: Male CHCs evoke intracellular Ca2+ responses in OA neurons that are dependent on Gr32a neurons.…………..…………..…………………..76 Figure 5: Gr32a chemosensory neurons located in the mouth promote aggression without an elevation in male:male courtship………………...79 Figure 6. Mouth-specific Gr32a neurons contact OA neurons in the suboesophageal ganglion.…………..…………..…………………..…………..……..81 Figure 7: Gr32a neurons anatomically contact three FruM-OA neurons……………..…………..…………………..…………..…………………..…………84 Figure S1: Characterization of the Tdc2-LexA line.…..…………..………….95 Figure S2. Single GRASP component control brains demonstrate an absence of GFP expression.…..…………..…………..…………..…………..……….96 Figure S3. Gr22e and Gr59b neurons contact OA neurons in the suboesophageal ganglion.…..…………..…………..…………..…………..…………98 Figure S4. GRASP-reconstitution between Gr47a neurons and OA- expressing neurons is not observed.…..…………..…………..…………..……...99 Figure S5. Tdc2-expressing neurons are ablated by UAS-hid UAS-DsRed expression.…..…………..…………..…………..…………..…………..…………..……100 Figure S6. Eliminating OA production alters a subset of Gr32a axonal projections.….…………..…………..…………..…………..…………..…………..…….101 Figure S7. Defects in aggressive behavior parameters in Gr32a- expressing and OA deficient males.…..…………..…………..…………..…….103 Figure S8. tsh-Gal80 blocks Gal4-mediated expression in the leg…...105 5 Table S1. Analysis of male-female courtship in males with ablated mouth Gr32a-expressing neurons.…..…………..…………..…………..………106 Chapter III Figure 1: Oaβ1R neurons within the tarsi and labellum…..…………….121 Figure 2: cAMP levels change in response to OA administration……123 Figure 3: Oaβ1R neurons express water sensors.…..……………………...125 Figure 4: Oaβ1R neurons express sugar receptors…..…………..………..126 Figure 5: Oaβ1R neurons express choline acetyltransferase………….128 Figure 6: OA administration increases firing frequency in labellar Oaβ1R neurons.…..…………..…………..…………..…………..…………..………….129 Figure 7: Oaβ1R neurons promote aggression and courtship behavior……..…………..…………..…………..…………..…………..…………..……..132 Figure 8: Loss of the Oaβ1R receptor alters wing specific behavior……………………………………………………………………………………..134 Figure 9: Oaβ1R-expressing neurons in the mouth promote initiation of courtship and aggression…..…………..…………..…………..…………..…….136 6 Abstract Survival and reproduction in the natural world requires an organism to identify and react to the presence of environmental stimuli in a time and cue dependent manner. Such temporal specificity requires the development and use of specialized sensory organs that receive this external sensory information. Neurons within the specialized sensory organs respond to touch, taste, pheromones, chemicals, and light, and transduce this information to the central brain. In many systems, gustatory and olfactory chemosensation in particular, provides critical information regarding sex and species identification as well as the status of food resources. The output of neurons which receive chemical information is regulated by the action of biogenic
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