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Tempo and Mode of Lineage and Morphological Diversification in a Hyperdiverse Freshwater Fish Radiation (Teleostei: Characiformes)

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Tempo and Mode of Lineage and Morphological Diversification in a Hyperdiverse Freshwater Fish Radiation (Teleostei: Characiformes) AN ABSTRACT OF THE DISSERTATION OF Michael D. Burns for the degree of Doctor of Philosophy in Fisheries Science presented on April 17, 2018. Title: Tempo and Mode of Lineage and Morphological Diversification in a Hyperdiverse Freshwater Fish Radiation (Teleostei: Characiformes) Abstract approved: ________________________________________________ Brian L. Sidlauskas Characiform fishes form one of the most diverse freshwater fish clades in the world. Comprising more than 2000 species and distributed primarily in South America and Africa, characiforms vary dramatically in their ecomorphology. However, the evolutionary processes responsible for the immense ecomorphological diversity remains unknown. Recently, a study postulated that the unparalleled ecomorphological diversification arose through an ancient adaptive radiation, as evidenced by the clear segregation of morphological traits, such as body shape, among different trophic and habitat groups. However, no formal macroevolutionary analyses have been conducted on the entire order of Characiformes and the mechanism responsible for the diversity remains unknown. Here, I conduct a macroevolutionary analysis of body shape diversification to determine if Characiformes evolved through an adaptive radiation. I estimated the first time-calibrated molecular phylogeny for the order Characiformes, assembled the first ever geometric morphometric body shape dataset, and compiled an exhaustive trophic ecology database. In my second chapter, I combined these datasets to test whether body shape adapted to shifts into different trophic guilds and to reconstruct body shape diversification in the Old and New World radiations. I found that body shape adaptation resulted in many non-repeated morphologies; lineages that shifted into the same trophic ecology evolved different morphotypes, except for convergent piscivores. Furthermore, we found that body shape diversification between the Old and New World radiations followed very different pathways, with the New World radiation occupying twice as much morphospace as their Old World counterparts. Both radiations exhibited higher morphological disparity than would be expected under Brownian motion, early in cladogenesis, matching expectations of an adaptive radiation. In my third chapter, I tested whether evolutionary modularity increased body shape diversification in the order. I found that characiform body shape was comprised of three independent modules that diversified at different times and rates while under different selective regimes. I postulate that the high evolutionary modularity plausibly explains why many body shapes evolved only once, when lineages evolved similar trophic ecologies across the radiation. The generality of the relationship between evolutionary modularity and increased morphological disparity has not been well studied in vertebrate lineages. More studies need to look at the role that evolutionary modularity and integration can have in shaping deterministic and contingent patterns of evolution across broad and restricted radiations of vertebrates. In my fourth chapter, I analyzed the rates of lineage and morphological diversification to determine whether Characiformes exhibited an early burst of speciation and morphological evolution as predicted by classical adaptive radiations. I found that the rate of speciation and evolution on the first morphological principal component were very high early in cladogenesis and quickly slowed down, following a pattern of adaptive radiation. However, the evolutionary simulations indicate that heavily pruning the tree overestimates the speciation rate early in cladogenesis, making the results consistent with a constant rates model. Higher taxon sampling is needed to fully understand whether the order exhibited the speciation patterns consistent with an adaptive radiation. My dissertation presents the first ever time-calibrated molecular phylogeny of Characiformes, the largest geometric morphometric dataset of Characiformes, and the most densely sampled clade-wide analysis of modularity in fishes. I found that characiform body shape likely radiated early in cladogenesis giving rise to many of the distinct morphologies that define the order. ©Copyright by Michael D. Burns April 17, 2018 All Rights Reserved Tempo and Mode of Lineage and Morphological Diversification in a Hyperdiverse Freshwater Fish Radiation (Teleostei: Characiformes) By Michael D. Burns A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented April 17, 2018 Commencement June 2018 Doctor of Philosophy dissertation of Michael D. Burns presented on April 17, 2018 APPROVED: Major Professor, representing Fisheries Science Head of the Department of Fisheries and Wildlife Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Michael D. Burns, Author ACKNOWLEDGEMENTS This dissertation would not have been possible without the help of many different people. First, I would like to thank my M.S. advisor, Kathleen Cole, for convincing me that Brian Sidlauskas would be an amazing PhD advisor. I want to thank Brian Sidlauskas for being everything Kassi said and more. Brian’s guidance has been instrumental in me becoming the researcher that I am today. His mentoring has shaped the way that I think, write, and teach; I am forever grateful for what he has helped me achieve. I also want to thank Brian for taking me to various meetings near and far and always allowing me to work on independent projects because the side hussle is my scientific muse. I want to thank the late Rich Vari for teaching a marine ichthyologist (me) all about tropical freshwater fishes. His patience and kindness were instrumental to the early success of my dissertation work. More importantly, I want to thank Rich for teaching me how to be a professional scientist by balancing work and life. Rich was a total scientific rockstar, but carried himself with extreme kindness, humbleness, and grace. His compassion was truly inspirational. Thank you for being you, Rich. The entire community misses you very much. I want to thank my committee for always having great input and helping me see the forest for the phylogenetic trees. I want to thank Vicki Tolar-Burton for helping me to love writing again. I lost it for awhile, but Vicki’s kindess and acceptance reignited my passion for written word. Thank you to all of my labmates, past and present, including Ben Frable, Kendra Hoekzema, Whitcomb Bronaugh, Casey Dillman, and Thaddaeus Buser. Kendra, thank you for teaching me how to be a disciplined reaearcher. Whit, thank you for being my sports outlet in the lab. Ben and Thaddaeus, thank you for always bringing the laughs to lab meeting and scientific conferences. Much of my scientific happiness has been forged in our late night chats at different meetings. I want to thank Peter Konstantinidis for super helpful discussions on fish morphology and evolution. Peter being hired by OSU was life changing for me. I want to thank Devin Bloom for being a secret (or not so secret?) role model of mine by showing me that someone like me can be successful in academia. I want to thank my parents for always believing in me, pushing me to expand my horizons, and always forcing me to find my own answers to the questions I asked. I believe that my mom and dad must have learned parenting under the late Socrates. They employed the Socratic Method of debate at every family dinner, and thus dinner served as my first committee meetings. I could not be more grateful for this because my scientific iron was forged in the fire of grilled burgers. Mom, I want to thank you for teaching me to be tough, you are the strongest person I have ever met and much of what I learned from you helped keep me sane during my PhD. Dad, I want to thank you for being my hero. Words cannot describe how much your kindness and love has shaped the person I am today. I hope in some small way my PhD fulfills your dream of being a scientist because I would not be one today without your endless passion for biology (even though you like birds more than fish now). I want to thank my brothers, Dan and Andrew, for always inspiring me. Dan, Andrew, from the day I was born, I have been chasing each of you, either on bikes or intelluctually. I might never catch you, but you will always help me reach higher than I ever could have on my own. I want to thank the Fregosi family for adopting me as their own during my PhD. Their love and acceptance lessened the blow of being away from my own family. I want to thank Selene for being everything. I really mean everything. Selene you are my emotional support, travel buddy, confidant, copy editor, sounding board, and best friend. None of this would have been possible without you helping me at every step. Thank you. I want to thank two amazing doggos, Piper “Fox” Fregosi and Murphy Jameson Burns. You borked, barked, and whined me into happiness everytime I was sad. Lastly, but definitely not leastly, I want to thank Brooks Burr, my undergraduate advisor. Brooks you took a chance on a 19-year-old who just loved sun, fishing and tropical fish aquaria. You taught me about science. You taught me about evolution. You taught me about ichthyology. You taught me all of this while never making me feel dumb, belittled, or beneath you. Your stories of growing up in the early 60’s in California, surfing breaks on a custom Dale Vezy longboard, made me realize that a scientist could be a regular person. You made me realize I could be a scientist. You were everything I needed in an advisor at that age and much of the passion you instilled in me then has kept me going now. I dedicate my dissertation to you Brooks because you saw my PhD as a reality while I was still a 19-year-old catching bass in Thompson Lake, dreaming I was on a tropical beach.
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