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Inertial Encoding Mechanisms and Flight Dynamics of Dipteran Insects

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Inertial Encoding Mechanisms and Flight Dynamics of Dipteran Insects INERTIAL ENCODING MECHANISMS AND FLIGHT DYNAMICS OF DIPTERAN INSECTS By ALEXANDRA M. YARGER Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology CASE WESTERN RESERVE UNIVERSITY May, 2020 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of Alexandra M. Yarger candidate for the degree of Doctor of Philosophy*. Committee Chair Dr. Jessica Fox Committee Member Dr. Roy Ritzmann Committee Member Dr. Hillel Chiel Committee Member Dr. Michael Lewicki Date of Defense March 3, 2020 *We also certify that written approval has been obtained for any proprietary material contained therein. 2 Dedication To my father, Jonathon Yarger who told me to do what I want and not what’s reasonable. 3 Table of Contents TITLE PAGE.................................................................................................................1 COMMITTEE APPROVAL SHEET ...........................................................................2 DEDICATION ...............................................................................................................3 LIST OF FIGURES .......................................................................................................6 ACKNOWLEDGEMENTS ...........................................................................................7 ABSTRACT ...................................................................................................................8 CHAPTER 1 ................................................................................................................ 10 Summary ............................................................................................................................................... 11 Introduction .......................................................................................................................................... 11 What are halteres? .............................................................................................................................. 13 What are the dynamics of the halteres as flies perform natural behaviors? ............................................ 16 What are the forces acting on the haltere? ........................................................................................... 17 What are the sensory structures on the halteres that transduce these forces, and how do they function? . 19 How do haltere afferent neurons process force information? ................................................................ 22 Where does haltere information go? .................................................................................................... 23 How is haltere information integrated with vision to guide wing-steering behavior? ............................. 25 How is haltere information integrated with vision for gaze control? ..................................................... 28 Are halteres useful for behaviors other than flight? .............................................................................. 29 How do other insects sense forces for flight control? ........................................................................... 30 Open questions on haltere function for fly behavior ............................................................................. 32 CHAPTER 2 ................................................................................................................ 36 Summary ............................................................................................................................................... 37 Introduction .......................................................................................................................................... 37 Methods................................................................................................................................................. 42 Recording ethological haltere oscillations ....................................................................................... 42 Preparation for nerve recordings ..................................................................................................... 42 Electrophysiology........................................................................................................................... 43 Haltere stimulation ......................................................................................................................... 43 Results ................................................................................................................................................... 44 4 Spontaneous haltere oscillations are similar in freely-behaving and tethered flies ............................. 44 Cells activated by self-generated and motor-driven oscillations phase-lock with similar precision .... 46 Sensilla respond to low amplitudes and frequencies during motor-driven oscillations, but not during self-generated haltere oscillations ................................................................................................... 49 Eliminating neural feedback does not change the activation threshold.............................................. 50 Amplitude and frequency thresholds change with lateral displacement ............................................ 50 Sensory neurons can encode haltere lateral displacements using phase information .......................... 52 Discussion.............................................................................................................................................. 55 Supplementary materials ...................................................................................................................... 59 CHAPTER 3 ................................................................................................................ 61 Summary ............................................................................................................................................... 62 Methods................................................................................................................................................. 63 Recording ethological data ............................................................................................................. 63 Tethered oscillations ....................................................................................................................... 63 Takeoffs ......................................................................................................................................... 63 Statistics ......................................................................................................................................... 64 Results & Discussion ............................................................................................................................. 64 Calyptratae flies oscillate their halteres asynchronously during pre-flight behaviors ............................. 64 Spontaneous takeoffs in Calyptratae flies are shorter than in non-Calyptratae flies ............................... 66 Halteres influence takeoff speed, pitch stability, and leg extension velocity in Calyptratae ................... 67 Flies with fast leg extensions and stout bodies have shorter takeoffs .................................................... 70 Haltere use and morphology in closely related clades .......................................................................... 72 CHAPTER 4 ................................................................................................................ 75 Conclusions ........................................................................................................................................... 76 Single sensory neurons ....................................................................................................................... 76 Behavioral context .............................................................................................................................. 78 Future Directions .................................................................................................................................. 80 Population code and downstream effects ............................................................................................. 80 Population recordings of the haltere nerve ....................................................................................... 81 Contralateral haltere interneurons ................................................................................................... 82 Neck motor neurons ....................................................................................................................... 83 Further flight dynamics and behavior .................................................................................................. 84 Modeling effects of morphology on takeoff speed and stability ....................................................... 84 Takeoff strategies and force production........................................................................................... 85 Haltere use in walking behaviors .................................................................................................... 86 Height and orientation .................................................................................................................... 87 Expanding our catalog of behavioral and phylogenetic diversity
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