Behavioral, Physiological, and Neurological Influences of Pheromones and Interomones in Domestic Dogs
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BEHAVIORAL, PHYSIOLOGICAL, AND NEUROLOGICAL INFLUENCES OF PHEROMONES AND INTEROMONES IN DOMESTIC DOGS By Glenna Michelle Pirner, B.S., M.S. A DISSERTATION in ANIMAL SCIENCE Submitted to the Graduate Faculty Of Texas Tech University in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY John J. McGlone, Ph.D. Chairperson of the Committee Alexandra Protopopova, Ph.D. Nathaniel Hall, Ph.D. Arlene Garcia, Ph.D. Yehia Mechref, Ph.D. Mark Sheridan, Ph.D. Dean of the Graduate School May 2018 Texas Tech University, Glenna M. Pirner, May 2018 Copyright 2016, Glenna M. Pirner ACKNOWLEDGEMENTS When I accepted a staff position as a research aide at Texas Tech University, I never dreamed that work would culminate a Ph.D., and I would like to first express my gratitude to Dr. John McGlone for giving me this opportunity. Your patience and guidance have provided me with invaluable knowledge and skills that will remain with me throughout my career. I would also like to thank Dr. Protopopova, Dr. Hall, Dr. Garcia, and Dr. Mechref for taking time to be a part of my committee and provide their feedback and advice. Your insight into each respective field has taught me to broaden my thinking and I look forward to future collaborations. I am deeply appreciative of the undergraduate research assistants and my fellow graduate students both in our lab and the department for their encouragement and support during my years here, especially Guilherme, Matt, Edgar, Lingna, Alexis, Gizell, Adrian, and Garrett. The teamwork and friendship made even the toughest days more bearable, and I wish all of you the best in your future endeavors. Last, but by no means least, I must express my love and gratitude for my parents, Glen and Wanda Schmid, my husband Jack, and our daughter Mary, without whom this would not be possible. My parents have provided support in every aspect of my life, allowing me to choose my own path and encouraging that decision at every step along the way. Jack has been loving, patient, and understanding when I have to work long hours, ii Texas Tech University, Glenna M. Pirner, May 2018 offering to watch Mary so I can study or cooking dinner because I will be home late. Above all, Mary has been my strongest source of motivation. Her unconditional love is a constant reminder that no matter what happens, at the end of the day I am right where I am supposed to be. iii Texas Tech University, Glenna M. Pirner, May 2018 TABLE OF CONTENTS ACKNOWLEDGEMENTS . .ii ABSTRACT . viii LIST OF TABLES . x LIST OF FIGURES . .xi LIST OF ABBREVIATIONS . xii I. INTRODUCTION . .1 II. LITERATURE REVIEW . 3 Background . 3 Defining Pheromones . .3 Early and current literature . 3 Terminology . 4 Perception . 5 Characteristics . 11 Conservation of molecules across species . 12 Classes of Pheromones . 13 Alarm . 13 Maternal . 14 Social/aggregation . 14 Sexual/reproductive . 15 Sex Pheromones Identified in Different Species . 18 Humans . .. 18 iv Texas Tech University, Glenna M. Pirner, May 2018 Other Species . 20 Dog Specific Information . 23 Reproductive physiology . 23 Reproductive behavior . 24 Literature Cited . 27 III. IMPACT OF 2-METHYLBUT-2-ENAL ON ACUTE STRESS RESPONSES IN CHRONICALLY STRESSED DOMESTIC DOGS . 39 Abstract . 39 Introduction . .40 Materials and Methods . 43 Results . 51 Discussion . 57 Conclusion . .62 Literature Cited . 63 IV. PHYSIOLOGICAL VARIABLES MAY BE USED IN PREDICTING STRESS RESPONSE IN LABORATORY DOGS . 67 Abstract . 67 Introduction . .68 Materials and Methods . .71 Results . 77 Discussion . 82 v Texas Tech University, Glenna M. Pirner, May 2018 Conclusion . 84 Literature Cited . 85 V. IDENTIFICATION OF PUTATIVE SEXUAL PHEROMONES IN MALE DOGS BY SOLID-PHASE MICROEXTRACTION TECHNIQUE IN COMBINATION WITH GAS CHROMATOGRAPHY-MASS SPECTROMETRY . 88 Abstract . 88 Introduction . 89 Materials and Methods . 90 Results . 93 Discussion . 105 Conclusion . 109 Literature Cited . 110 VI. EVALUATION OF PHEROMONE-INDUCED ACTIVATION IN THE HUMAN BRAIN USING FUNCTIONAL MAGNETIC RESONANCE IMAGING (FMRI) . 114 Abstract . 114 Introduction . 115 Materials and Methods . 117 Results . 124 Discussion . 129 vi Texas Tech University, Glenna M. Pirner, May 2018 Conclusion . 131 Literature Cited . 132 VI. CONCLUSION . 135 vii Texas Tech University, Glenna M. Pirner, May 2018 ABSTRACT Pheromones provide a crucial method of information transfer for many species; however, this type of communication is not well understood in the domestic dog. Beyond intraspecific communication, evidence suggests that some molecules, known as interomones, may act as a pheromone in one species but elicit unpredictable effects in a different species. 2-methylbut-2-enal (2M2B), the rabbit maternal-neonatal pheromone, is one such molecule. To determine the behavioral and physiological effects of 2M2B on chronically stressed domestic dogs two stress-induction models were used: a simulated thunderstorm and car travel. In both models, 2M2B elicited a faster return of elevated heart rate (HR) to baseline compared to control (CON). During the thunderstorm dogs treated with 2M2B spent 15.9% more time lying down compared to when treated with CON (p = 0.04). Heart rate variability measures, leukocyte differentials, and adrenocorticotropic hormone- stimulation tests were recorded from the dogs used in these studies to understand how acute stressors affect chronically stressed dogs, and how 2M2B might ameliorate this response. Average R-R interval was negatively, but not significantly, correlated with the magnitude of difference in heart rate between placebo and 2M2B ointment during the simulated thunderstorm. There is limited research on domestic dog pheromones, and there are notable inconsistencies in the literature that does exist. To identify urinary volatiles that may act as pheromones, urine was collected from five individuals in each of six groups: juvenile intact male (JIM), adult intact male (AIM), adult castrated.