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Social Interactions of Lythrypnus Dalli and Their Effects on Aggression, Neuropeptides, Steroid Metabolism, and Sex-Typical Morphology

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Social Interactions of Lythrypnus Dalli and Their Effects on Aggression, Neuropeptides, Steroid Metabolism, and Sex-Typical Morphology Georgia State University ScholarWorks @ Georgia State University Biology Dissertations Department of Biology Spring 2005 Social Interactions of Lythrypnus dalli and their Effects on Aggression, Neuropeptides, Steroid metabolism, and Sex-Typical Morphology Michael Paul Black Follow this and additional works at: https://scholarworks.gsu.edu/biology_diss Part of the Biology Commons Recommended Citation Black, Michael Paul, "Social Interactions of Lythrypnus dalli and their Effects on Aggression, Neuropeptides, Steroid metabolism, and Sex-Typical Morphology." Dissertation, Georgia State University, 2005. https://scholarworks.gsu.edu/biology_diss/17 This Dissertation is brought to you for free and open access by the Department of Biology at ScholarWorks @ Georgia State University. It has been accepted for inclusion in Biology Dissertations by an authorized administrator of ScholarWorks @ Georgia State University. For more information, please contact [email protected]. SOCIAL INTERACTIONS OF LYTHRYPNUS DALLI AND THEIR EFFECTS ON AGGRESSION, NEUROPEPTIDES, STEROID METABOLISM, AND SEX-TYPICAL MORPHOLOGY by MICHAEL P. BLACK Under the Direction of Matthew S. Grober ABSTRACT Social interactions can have profound effects on the behavior, physiology, and overall fitness of an individual. An example of this in Lythrypnus dalli is the removal of a male from a social group resulting in a dominant female fish changing sex. The dominant female’s transformation involves a suite of changes including brain, behavior, morphology, and physiology. Following the social trigger (male removal), sex-changing individuals’ morphology, steroid levels, and changes in the behavior were quantified in the field and compared to results found previously in the laboratory. There were lower rates of aggressive and courtship behavior in the field, but the change in behavior over time had a similar pattern and there were parallels in morphology and steroid levels between lab and field sex changers. The brains of dominant females also responded to social change. Aromatase, an enzyme that converts testosterone into estrogen, and oxytocin, a neuropeptide found in mammals, have been associated with vertebrate social and reproductive behavior. The fish homologue of oxytocin, isotocin, and aromatase are both found in L. dalli. Upon removal of a male from the social group, L. dalli dominant females experienced a decrease in the number of preoptic area isotocin-immunoreactive cells over the course of sex change (7-10 days) and a decrease in brain aromatase activity (bAA) levels within hours, but not minutes, of male removal, while gonadal aromatase activity (gAA) decreased at a much slower time scale (beyond a week). Hours, but not minutes, after male removal, the sex- changing individual’s bAA correlated with aggressive behavior increases and not the amount of time following male removal. Males that had just changed from female had different gonadal allocation and higher bAA levels than established males. Subordinate females had high gAA, but their bAA was between that of males and sex changers. In conclusion, dramatic changes in anatomy and neuroendocrine function can occur in response to social cues, individuals with similar reproductive behavior and external morphology can have large neuroendocrine and internal morphologic variation, and social interactions can affect steroid metabolism locally on a short time scale independent of gonadal modulation of steroids. INDEX WORDS: estrogen, androgen, teleost, 11-ketotestosterone, reproductive, plasticity, CYP19, accessory gonadal structure, genital papilla, genitalia, challenge hypothesis SOCIAL INTERACTIONS OF LYTHRYPNUS DALLI AND THEIR EFFECTS ON AGGRESSION, NEUROPEPTIDES, STEROID METABOLISM, AND SEX-TYPICAL MORPHOLOGY by MICHAEL P. BLACK A Dissertation Submitted in Partial Fulfillment of Requirements for the Degree of Doctor of Philosophy Georgia State University 2005 Copyright by Michael Paul Black 2005 SOCIAL INTERACTIONS OF LYTHRYPNUS DALLI AND THEIR EFFECTS ON AGGRESSION, NEUROPEPTIDES, STEROID METABOLISM, AND SEX-TYPICAL MORPHOLOGY by MICHAEL P. BLACK Major Professor: Matthew S. Grober Committee: H. Elliott Albers Deborah J. Baro Charles D. Derby Larry J. Young Electronic Version Approved: Office of Graduate Studies College of Arts and Sciences Georgia State University May 2005 iv ACKNOWLEDGEMENTS There are many people who helped in shaping my ideas, collecting data, giving advice and support, providing logistics in the field, and teaching me new techniques. For the help and support I received, for work that went into this dissertation, and for preliminary work and future papers that did not, an acknowledgement page cannot thank all of these people, but you know who you are. Thank you. I owe thanks to my high school science teachers, Mr. Hall, Mr. Bero, and Mr. McCall, who challenged and inspired me. I would also like to thank the support staff both at Arizona State University, including Sue Zvirgdins, Cindy Marchiafava, and Jean Chesser, and at Georgia State University, particularly LaTesha Morrison-Warren, Candice Long, Tony Burnett, Hugh Robinson, Barry Grant, Lydia Woltz, Stephanie Jennings, Tara Alexander, Kelly Powell, Cheryl King, Dixie Elmore, Diane Moody, and John Haydock. You don’t even get half of the credit you deserve. At Arizona State University, Dr. Pierre Deviche, Dr. Michael Moore, Dr. Miles Orchinik, Dr. Ron Rutowski, Dr. Matthew Grober, and Dr. Gordon Schuett all served as committee members for me when I started as a Master student and in the first years of my PhD. They were instrumental in the early formative years of my graduate studies. My committee members, Dr. Elliott Albers, Dr. Deb Baro, Dr. Chuck Derby, and Dr. Matthew Grober at Georgia State University and Dr. Larry Young at Emory University were generous with their time, advice, and assistance during the second part of my PhD. Moving with my advisor in the middle of my PhD was not an experience I would want to do again, but having you as a part of my transition made the experience easier. This dissertation was improved by the comments of my committee, as well as Dr. Ryan Earley, Ed Rodgers, and Judy Black. v My advisor, Dr. Matthew Grober, and his family, Debi, Aaron, Mia, and Cory, deserve more thanks than I can write. Being your first PhD student was a rocky road at times, but you were steadfastly optimistic and steadfastly supportive, sometimes more than I believe I deserved. As you know, I can be my own biggest critic, and you countered that well with your optimism, your good advice, and, above all, your friendship. None of this would have been possible without my parents, James and Nancy Black, my family, and my wife, Melissa. Thank you for letting me pursue my dreams wherever they lead me. I love you with all my heart. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENTS………………………………………………………………………iv TABLE OF CONTENTS….……………………………………………………………………...vi LIST OF FIGURES……...……………………………………………………………………...viii LIST OF ABBREVIATIONS………………….……………………………………………….....x CHAPTER 1 GENERAL INTRODUCTION……………………………………………………….1 2 STEROID HORMONES AND BEHAVIOR ASSOCIATED WITH SEX CHANGE IN THE FIELD……………………………………………………....12 Summary…………………………………………………………………………12 Introduction………………………………………………………………………13 Methods………………………………………………………………………….14 Results……………………………………………………………………………24 Discussion………………………………………………………………………..38 3 SOCIALLY-REGULATED SEXUAL DIFFERENCES IN PREOPTIC ISOTOCIN-LIKE IMMUNOREACTIVE CELLS.…..………………………....49 Summary…………………………………………………………………………49 Introduction………………………………………………………………………50 Methods………………………………………………………………………….52 Results…………………………………………………………………………...55 Discussion……………………………………………………………………….59 4 SOCIALLY-REGULATED RAPID CHANGES IN AGGRESSION AND BRAIN AROMATASE ACTIVITY ARE CORRELATED……………………………...63 Summary…………………………………………………………………………63 Introduction………………………………………………………………………64 vii Methods………………………………………….……………………………….65 Results…………………………………………....………………………………69 Discussion…………………………………………………………………….….76 5 RAPID BEHAVIORAL CHANGES PRECEDE CHANGES IN BRAIN AROMATASE ACTIVITY DURING SOCIALLY-MEDIATED SEX CHANGE………………...……………………………………………………....85 Summary…………………………………………………………………………85 Introduction………………………………………………………………………86 Methods……………………………………………………………………….….87 Results………………………………………………………………………....…89 Discussion………………………………………………………………………..89 6 GENERAL DISCUSSION.……………….………………………………………...97 Variation in males………………………………………………………………..98 Social effects on brain aromatase activity and neuroendocrine modulation……101 Aromatase activity in fish and other vertebrates………………………………..104 Local brain changes independent of the gonads………………………………..106 REFERENCES….……...…………………………………………………………………….....109 APPENDIX: ACKNOWLEDGEMENTS FOR PUBLISHED PAPERS..……………………142 viii LIST OF FIGURES FIGURE 1 Number of different species in each of the major vertebrate groups………………….3 2 Size-advantage model of sex change………………....……………………………......6 3 Temporal sex change model for Lythrypnus dalli…….…..………………………......8 4 Transverse section of bluebanded goby (L. dalli) gonad from a focal fish..………...23 5 Four representative behavioral profiles of L. dalli focal fish after the male has been removed………………...…………………………………………………….........25 6 Temperature-corrected displacement and jerk behavioral profiles over the course of sex change for all L. dalli sex changers on artificial habitats…………………......27 7 Scatterplot comparing mean ovarian and testicular allocations in transverse sections of L. dalli gonad in focal fish, males, and female….…………...………………...30 8
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