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Riverscape Genetics: Insights Into the Drivers of Divergence in Coastal Brazilian Fishes

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Riverscape Genetics: Insights Into the Drivers of Divergence in Coastal Brazilian Fishes Riverscape Genetics: Insights Into the Drivers of Divergence in Coastal Brazilian Fishes by Andréa Tonolli Thomaz A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in The University of Michigan 2017 Doctoral Committee: Professor L. Lacey Knowles, Chair Professor James Diana Associate Professor Timothy Y. James Professor Diarmaid Ó’Foighil Emeritus Professor Gerald Smith Andréa T. Thomaz [email protected] ORCID iD: 0000-0002-9755-2674 © Andréa T. Thomaz 2017 DEDICATION To my mom Ana thank you for teaching me how to fly ii ACKNOWLEDGMENTS This dissertation started to be conceived years before I enter in my Ph.D. Exactly ten years ago I was finishing my undergraduate in Brazil and, with that, came the certitude that I would like to pursue academia and, more precisely, the project presented here. During these ten years many people helped me to overcome the several steps until the end of my Ph.D., and I’m truly thankful for all of them. Firstly, I would like to thank the University of Michigan, the Rackham Graduate School and, more specifically, the Department of Ecology and Evolutionary Biology (EEB) and the Museum of Zoology (UMMZ) for opening their doors and giving me all the necessary support for an international student pursue its research in this institution. Thank you for always believing in my studies and financially supporting them with Block Grants, Rackham Graduate Student Research Grants, Rackham International Student Award, and Rackham Predoctoral Fellowship Program and the Tinkle Award that I was awarded during my Ph.D. Also, although I was not officially a member of the Fish Division at the UMMZ, I’m grateful for all the opportunities this division offered me, including the Ichthyology Student Award for developing my fieldwork in Brazil, the curator assistantship position that allowed me to gain expertise by working in the fish collection and for the Hubbs, Carl L. and Laura C. Fellowship that allowed me to work full time on my research for two years. All the handling of specimens, including paper work, shipping and housing at the fish collection, wouldn’t be able to be done without Doug Nelson’s help, support and ichthyological stories. Also, Robbin Murrell and Cindy Carl were essential for all the logistic support and answering all my questions (and I had many!). I would like to thank the National Science Foundation (NSF) for awarding my advisor and I with the Doctoral Dissertation Improvement Grant (DDIG). This support was essential for developing all the sequencing and methodologies necessary for the accomplishment of this dissertation. During my master’s I had the chance to attend a seminar presented by a professor with orange nail polish on her toes (not sure why I still remember this detail) that was developing the most innovative research in phylogeography, in my opinion. Years after, she accepted me as a iii student in her lab and this was the most intense learning experience I have had in my life. In reality, it was not just about methodologies, but what I will really take for my life that I have learned from her is the way of approaching a question, the reasoning, the hypotheses testing, and thinking outside the box. Lacey, thank you for the opportunity of being your student, for all the conversations and discussions. I’m not going to lie, you are tough sometimes :) but I’m a better scientist today because of you, and I will keep working hard to improve. Also, this dissertation wouldn’t have been possible without the support of my first advisor, Luiz R. Malabarba (Brazil). Mala, I’m very lucky to have you as my “fish” advisor, and you will always be. I’m extremely grateful for your generosity with me over the entire time, helping me with fieldwork, permits, being my fish guide, talking about biogeography, making barbecues every time I visited Brazil, and for always believing in my capacity, thank you! I’m grateful for having the chance to work with our “borrowed” postdoc Mark Christie, who introduced me to the world of simulations and river modeling with an incredible patience and dedication. The things I learned with you will have a life long impact on my research. The work presented here was only possible with many fieldwork trips. I would like to thank all my friends that provided their time and fishing expertise, sorting, taking pictures, and celebrating every single individual that we got in our nets, they are: Vinícius Bertaco, Fernando Carvalho, Tiago P. Carvalho, Juliano Ferrer, Alice Hirschmann, Fernando Jerep, Giovanni Neves, Udson Santos, Priscilla C. Silva and Juliana Wingert. This work was only possible because of you guys. During the six years in the same department and lab, many people have come and gone, but I was very lucky to have the chance to share some time with them, each of which had a positive effect on my research, and interesting memories/impressions I have of each one: Diego you are the guy for GIS; Qixin your scripts saved my life, Anna your heart is humongous; Rob and his calm walking style; JP playing Frozen when I started to freak out; Tristan and his always positive vibe; Carlos it was nice meeting you; Mariah, I will put you in a little box and keep it in my closet; Katie I owe you a beer! Raquel thank you for all hugs and advice - I love them; Jordan you are not from my lab, but I like to think you are; Pame crazy for R. I also want to thank Joyce, Lu and Rê for being my Brazilian family here. Also, Ann Arbor gave me the chance to make good friends. Thank you all for the delicious brunches we had (with mimosas), the pottery fun, after work wine or beer to relax, swimming on the river, the running challenges, iv bike rides to Dexter, dart games, snow fights, soccer games, dancing, numerous barbecues, etc. Thank you all for the good times! Tiago, thank you for being my boyfriend, my best friend and my favourite ichthyologist. I know being almost seven years apart it was not easy, but, independent of the distance, you are always present in my thoughts and in my heart. Your support over all these years was fundamental to me. Finally, I need to thank my foundation, my family. Even though they do not understand very well what I do, they always gave me the unconditional emotional and financial support. Dad, thank you for always pushing me to do my best (since my grades were never good enough to you :p). Mom, thank you for raising me to be an independent woman. Kelly, thank you for your affection. Paty, you explained to me the meaning of a Ph.D. when I was in the sixth grade, and since then I was dreaming of this day. v TABLE OF CONTENTS DEDICATION …………………………………………………………………………………... ii ACKNOWLEDGMENTS …………………………………………………………………….... iii LIST OF TABLES …………………………………………………………………………….... ix LIST OF FIGURES ……………………………………………………………………………... x ABSTRACT ………………………………………………………………………………….... xii CHAPTER I. Introduction ………………………………………………………………..…… 1 Background …………………………………………………………………………….... 1 Freshwater Fish Phylogeography ………………………………………………………... 2 Freshwater Fish Phylogeography in the Neotropics ………………………...…………... 3 Study Region …………………………………………………………………………..… 4 Chapter Overview ……………………………………………………………………….. 6 References ……………………………………………………………………………….. 7 CHAPTER II. Testing the effect of palaeodrainages versus habitat stability on genetic divergence in riverine systems: study of a Neotropical fish of the Brazilian coastal Atlantic Forest …………………………………………………………………………………………... 12 Abstract ………………………………………………………………………………… 12 Introduction …………………………………………………………………………….. 13 Material and Methods ………………………………………………………………….. 17 Inference of Paleodrainages …………………………………………………… 17 Atlantic Forest Niche Modelling ……………………………………………….. 17 Tissues and molecular genetic methods …………………………………………….. 18 Phylogenetic inference and demographic dynamics …………………………… 18 Testing the effect of palaeodrainages and habitat stability ……………………. 19 Results ………………………………………………………………………………….. 20 Discussion ……………………………………………………………………………… 25 vi Palaeodrainages as key in structuring patterns of genetic variation ………….. 26 The importance (or unimportance) of distributional stability …………………. 27 Processes structuring species diversity in coastal Brazil ………………………… 29 Summary ……………………………………………………………………….. 29 References ……………………………………………………………………………… 30 APPENDIX A ……………………………………………………………………….…. 37 CHAPTER III. The architecture of river networks can drive the evolutionary dynamics of aquatic populations ………………………………………………………………..………..… 42 Abstract ………………………………………………………………………………… 42 Introduction …………………………………………………………………………….. 42 Material and Methods ………………………………………………………………….. 44 Agent-based modeling in rivers ………………………………………………... 44 Landscape vs. Riverscapes ……………………………………………………... 46 Riverscape architectures ……………………………………………………..… 47 Results …………………………………………………………………………………...48 Landscape vs. Riverscapes ……………………………………………………... 48 Riverscape architectures ……………………………………………………….. 50 Discussion ……………………………………………………………………………… 53 References ……………………………………………………………………………… 56 APPENDIX B ………………………………………………………………………….. 60 CHAPTER IV. Genomic signatures of paleodrainages in a freshwater fish along the southeastern coast of Brazil: genetic structure reflects past riverine properties …………. 65 Abstract ………………………………………………………………………………… 65 Introduction …………………………………………………………………………….. 66 Material and Methods ………………………………………………………………….. 67 Sampling and RADseq genomic data generation and processing ……………... 67 Tests of genetic structure associated
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