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The Evolution of Reproductive Complexity in Fishes

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The Evolution of Reproductive Complexity in Fishes City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 9-2019 The Evolution of Reproductive Complexity in Fishes Frieda Benun The Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/3470 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] THE EVOLUTION OF REPRODUCTIVE COMPLEXITY IN FISHES By FRIEDA BENUN A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2019 © 2019 FRIEDA BENUN All Rights Reserved ii The Evolution of Reproductive Complexity in Fishes By Frieda Benun This manuscript has been read and accepted for the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. ________________________ ____________________________________ Date Dr. Anthony B. Wilson Chair of Examining Committee ________________________ ____________________________________ Date Dr. Cathy Savage-Dunn Executive Officer Examination Committee: Dr. Jennifer Basil Dr. David Lahti Dr. Nicholas Santangelo Dr. Hope Klug THE CITY UNIVERSITY OF NEW YORK iii The Evolution of Reproductive Complexity in Fishes By Frieda Benun Advisor: Anthony B. Wilson ABSTRACT How does reproductive complexity evolve? In this dissertation, I investigate the evolution of parental investment and mating behavior, using both macro- and microevolutionary lenses. I use fishes, the most diverse group of vertebrates, comprising over 30,000 species, as a model to study the evolution of these traits. In Chapter 1, I introduce the evolution of parental behaviors in fishes, and I explore how fishes, in contrast to other animal groups, have repeatedly evolved paternal care. I present a systematic review of parental care for 294 families (close to 60%) of bony fish and show that male-only care is the predominant form of care in this group. I summarize current theories on parental care, emphasizing external fertilization, certainty of paternity, and territoriality as important factors in the evolution of male care, and internal fertilization as an important precursor to the evolution of female care. I review the social, neural, and physiological mechanisms underlying care behaviors. Finally, I highlight the cichlid model as a useful system in which to study both the proximate and ultimate causes of parental care. In Chapter 2, I explore the evolution of parental care and the prevalence of male-only care in bony fishes. Using the most complete phylogeny of bony fishes to date, I show that the opportunity for external fertilization in aquatic environments is a key driver of male parental care in this group. By moving the control of reproduction outside the female reproductive tract, iv external fertilization increases male confidence in paternity. Paternal care has evolved over 30 times independently in fish and is found only in pair-spawning species, where parentage confidence is high. I also demonstrate that females must trade off care against other forms of reproductive investment, while males are not similarly constrained, creating conditions under which both the costs and benefits of care favor paternal investment. In Chapter 3, I investigate the evolution of biparental care in Cichlidae. I show that evolutionary transitions between biparental and maternal care have occurred frequently, highlighting the evolutionary lability of care in this group. I demonstrate that biparental care is associated with substrate guarding, suggesting that males participate in care when they can benefit from the multiple mating opportunities associated with guarding. Consistent with my findings in Chapter 2, I show that females must trade off care against the number of eggs produced, but that male participation in care can help to offset the costs of female reproduction, allowing for larger clutches. Joint parental care is also associated with extended care duration, suggesting that both parents care when offspring require longer periods of parental investment. Chapters 4 and 5 focus on the evolution of reproductive complexity in the male pregnant pipefish, Syngnathus fuscus. In Chapter 4, I quantify maternal and paternal investment in offspring and test whether relative parental investment predicts intensified sexual selection on females in this group. By weighing newly fertilized and mature embryos, I show, contrary to my predictions, that female care exceeds that of males in this species. I also demonstrate that despite a moderately complex brood pouch, male pregnancy in S. fuscus does not include active provisioning to embryos. Comparison to other pipefish species shows that S. fuscus eggs represent some of the smallest in this group, suggesting that this species employs the “quantity over quality” approach, producing many small offspring. v In Chapter 5, I show that Syngnathus fuscus males, despite having some of the largest brood sizes of any pipefish species, consistently mate monogamously across the season. I use molecular markers to reconstruct the number of mothers contributing to the broods of field- caught males, and find that multiple mating among males is rare and occurs only towards the end of the breeding season. I suggest that sex ratio dynamics may influence male monogamy. I also propose that sexual size dimorphism may be responsible for the mating patterns in S. fuscus, as sampled females are larger than males and can fill an entire brood pouch of a male throughout most of the season. vi ACKNOWLEDGMENTS One who learns from his fellow a single chapter, or a single law, or a single verse, or a single word, or even a single letter, he must treat him with honor. —Ethics of the Fathers (Pirke Avot), 6:3. There are many, many people who generously gave me their time, whether for research advice or a listening ear, without whom this dissertation would not have been possible. I would first like to thank my advisor, Dr. Tony Wilson, for taking a leap of faith in agreeing to take me into his lab despite my lack of research experience, and for helping me to grow over the past six years from a clueless undergraduate into a critically minded scientist. His scientific rigor and intellectual acuity have strengthened not only my research, but also the way in which I read, write and think. I also wish to thank my committee members: Dr. Jenny Basil, Dr. David Lahti, Dr. Nick Santangelo, Dr. Hope Klug, and second-exam committee member Dr. Holly Kindsvater, for their guidance, patience, and expertise. Their insightful comments have gone a long way into sharpening my research. A special thank you to Jenny for her ongoing encouragement and positivity over the past six years, which have been a critical source of support and stability to my emotional well-being. I am also grateful to the many high school teachers and college professors along the way who inspired me and helped foster within me a passion for learning and scientific inquiry. Thank you to the members of the Wilson Lab, past and present. Over my first year as a doctoral student, Dr. Florentine Riquet gave me a crash course in Genetic Analysis 101, teaching me everything from PCR to allele scoring. Dr. Sunny Scobell, our resident pipefish expert, took me on my first trip to the field and offered constant support and advice on keeping animals in the vii lab. Dr. Kerstin Musolf kept the lab afloat with her yummy treats and pleasant demeanor, and always stimulated our group lab discussions with thoughtful questions. I owe a very big thanks to my officemate Jimiane Ashe who took one look at me on Day 1 (a helpless city girl trying to build IKEA furniture for the first time) and took me under her wing. She accompanied me on many of my trips to the field, showed me how to properly pipette, ran my potentially mutagenic gels while I was pregnant, and taught me many of the fundamentals of molecular biology. The walls of our little windowless office were witness to many tears (of both frustration and laughter), but I’m glad we got to share them together. Many student volunteers were indispensable in the assistance they provided. High school student Emily Hui worked diligently for two years on all aspects of my pipefish research, always with a smile. I wish to thank many of our undergraduates for the dedication and enthusiasm they brought to the lab, in no particular order: Amena Abbasi, Mila Mirzakandova, Miar Elaskandrany, Jailene Paredes, Krystal Boley, Rimsha Azhar, and Corey Lavine. I am grateful to these students, in addition to the many others from Biology I and Macaulay Honors courses, for making teaching and mentoring such a rewarding experience for me. I feel truly blessed to have been surrounded by such supportive family, which has kept my kids (and let’s be honest, me too) well-fed and cared for throughout this long journey. Thank you to “Gaga and Pa” for the weekly babysitting, and to my siblings-in-law, Miro, Aline, and Norma, who never stopped cheering me on. I am forever grateful to my parents for their endless love and encouragement, and for raising me with the confidence and perseverance that got me to the finish line. I am especially appreciative of my mom for serving as cheerleader, baby nurse, soundboard, proofreader, and, of course, the source of my inspiration to pursue a career in science. To my siblings: Joe’s optimism and superhuman strength were valuable additions to our viii California field trip, Meyer joined me on many long summer days out in the field, and Cynthia provided much-needed Facetime breaks and a semester of daily fresh fruit supplied to my office.
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