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Patterns and Rates of Ecological Diversification Among Neotropical Cichlid Fishes

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Patterns and Rates of Ecological Diversification Among Neotropical Cichlid Fishes Patterns and rates of ecological diversification among Neotropical cichlid fishes by Edward D. Burress A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama August 5, 2017 Keywords: adaptive radiation, morphology, parallel evolution pharyngeal jaw, phylogeny, speciation Copyright 2017 by Edward D. Burress Approved by Jonathan W. Armbruster, Chair, Professor of Biological Sciences and Curator of Fishes Jason E. Bond, Professor and Department Chair of Biological Sciences Jack W. Feminella, Professor and Associate Dean of Academic Affairs in the College of Sciences and Mathematics F. Stephen Dobson, Professor Abstract The rapid rise of phenotypic diversity and corresponding ecological roles is an emblematic pattern of cichlid evolution, particularly within clades of the East African Great Lakes. Herein, I evaluate the phenotypic and ecological diversification of Neotropical cichlids through time and among clades using a combination of geometric morphometrics, dietary analysis, and comparative phylogenetic methods. I found that the shape of the lower pharyngeal jaw (LPJ), which is part of a major phenotypic innovation among cichlids (i.e., pharyngognathy), is correlated with dietary patterns among Neotropical cichlids. The evolution of trophic roles such as molluscivory, algivory, and piscivory were associated with modifications in LPJ shape and tooth types. Additionally, LPJ shape evolution was correlated with body shape evolution among Neotropical cichlids; however, this pattern was driven by one of the major lineages (the Heroini) in which the evolution of these traits were highly correlated. This discrepancy among major clades may have arisen due to changes in the adaptive landscape as the Heroini colonized Middle America. Indeed, I detected diversity dependent evolution of LPJ shape following the colonization of Middle America, but not following the colonization of South America. Therefore, dissimilar evolutionary and ecological opportunities provided by the subsequent colonization of South and Middle America likely elicited different constraints during their diversification. Ecosystem-scale colonization events have been similarly important events throughout the evolutionary history of some lineages. I found that following the colonization the Paraná and Uruguay Rivers, distantly related pike cichlids (Crenicichla) diversified in situ and in ii parallel into similar novel ecomorphs associated with trophic specializations, namely molluscivory, crevice feedings, and periphyton grazing. These results indicate that phenotypic and ecological diversity among Neotropical cichlids has varied dramatically among clades, through time, and in response to ecological opportunities provided by the colonization of new environments. iii Acknowledgments I’m grateful and forever in debt to my past academic advisors for guiding me toward what ultimately manifested in this work. Stewart Skeate fostered my initial fascination in nature and exploration. Sue Hart nurtured a warm-hearted outlook on the daunting path through academia. James Carson introduced me to statistics. Michael M. Gangloff provided continual insight and support in my endeavors. Lynn Siefferman let me wonder and dream, provided guidance in life and work, and fostered strength and focus in all things. My current advisor, Jonathan Armbruster, provided resources, a conducive environment, and intellectual freedom to pursue my academic interests. My committee, Jason Bond, Jack Feminella, and Steve Dobson, provided their vast insight on science and life. Many colleagues have contributed to the work and ideas herein, including (in no particular order) Milton Tan, Lubomír Piálek, Oldřich Říčan, Jorge R. Casciotta, Adriana Almirón, Alejandro Duarte, Marcelo Loureiro, and Jordan M. Holcomb. I’m grateful to Kid Cudi and Bon Iver for making music that got me through many late hours in the museum. Many researchers, perhaps mostly unknown to them, have greatly cultivated my interests and motivated much of my own work, including Peter Wainwright, Katie Wagner, Ole Seehausen, Kirk Winemiller, Hernán López‐Fernández, Dolph Schluter, Axel Meyer, Jonathan Losos, and Karel Liem. Many friends, lab mates, and colleagues have played intricate and irreplaceable roles in my professional and/or social life, including (in no particular order) Malorie Hayes, Mark and Heather Stuart, Carrie Klase, Taylor Fraychak, Milton Tan, Carla Stout, Shobnom Ferdous, Erin O’Reily, Jessica Gilpin, and Dave Werneke. My wife, Pamela iv Burress, which I met during my time at Auburn, has been supportive, loving, and understanding throughout my work and has made these years special. Lastly, my parents, Edward and Robin Burress, have always been supportive of my journey through all the bumps and turns. v Table of Contents Abstract ......................................................................................................................................... ii Acknowledgments........................................................................................................................ iv List of Tables ............................................................................................................................. viii List of Figures .............................................................................................................................. ix General Introduction ................................................................................................................... 1 References ....................................................................................................................... 3 Chapter 1. Ecological diversification associated with the pharyngeal jaw diversity of Neotropical cichlid fishes ............................................................................................................................... 6 Abstract ........................................................................................................................... 6 Introduction ..................................................................................................................... 7 Methods ........................................................................................................................... 9 Results ........................................................................................................................... 13 Discussion ..................................................................................................................... 16 References ..................................................................................................................... 23 Chapter 2. Pharyngeal jaw evolution and trophic niche filling after the colonization of the Americas by cichlid fishes ........................................................................................................ 44 Abstract ......................................................................................................................... 44 Introduction ................................................................................................................... 45 Methods ......................................................................................................................... 48 vi Results ........................................................................................................................... 53 Discussion ..................................................................................................................... 57 References ..................................................................................................................... 63 Chapter 3. Body and pharyngeal jaw shape evolution are correlated across the Neotropical cichlid phylogeny ...................................................................................................................... 82 Abstract ......................................................................................................................... 82 Introduction ................................................................................................................... 83 Methods ......................................................................................................................... 86 Results ........................................................................................................................... 90 Discussion ..................................................................................................................... 93 References ..................................................................................................................... 98 Chapter 4. Island- and lake-like parallel adaptive radiations replicated in rivers ................... 114 Abstract ....................................................................................................................... 114 Introduction ................................................................................................................. 114 Methods ....................................................................................................................... 117 Results ......................................................................................................................... 122 Discussion ..................................................................................................................
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