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Trends in the Evolution and Ecology of Functional Morphology in Neotropical Cichlids

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Trends in the Evolution and Ecology of Functional Morphology in Neotropical Cichlids Trends in the Evolution and Ecology of Functional Morphology in Neotropical Cichlids by Jessica Hilary Arbour A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto © Copyright by Jessica Hilary Arbour 2015 Trends in the Evolution and Ecology of Functional Morphology in Neotropical Cichlids Jessica Arbour Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto 2015 Abstract The uneven distribution of biological diversity has been a subject of great interest in the study of evolutionary biology. Advances in molecular phylogenetics and comparative methods have facilitated an increasing number of studies relating to the impacts of neutral and adaptive processes on morphological diversity, especially those relating to the predictions of adaptive radiation. While such studies have largely focused on restricted, island radiations, such as African Rift Lake cichlids and Caribbean anoles, recent years have seen an expansion of the analysis of morphological evolution within more broadly-distributed clades. Due to their species-richness, ecological/morphological diversity and age, the continentally-distributed freshwater fish Cichlinae (Neotropical cichlids) represent an ideal system for the study of morphological evolution and its relationship to ecological diversity. Combining data from biomechanics, morphometrics, modern and fossil specimens, and dietary analyses with a comprehensive molecular phylogeny and modern phylogenetic comparative methods I examined functional morphological evolution in Neotropical cichlids and the impact of factors such as selection, adaptation, extinction and ecological opportunity on diversification. Analysis of the functional morphospace of Neotropical cichlids revealed complex selective regimes that have contributed to their modern functional diversity. Rates of functional evolution varied with ii ecological opportunity in Neotropical cichlids, declining in South American through time and increasing upon the colonization of new habitats in Central America. Extinct, fossil cichlid species demonstrate the stability of selective processes on ecomorphological evolution over tens of millions of years. Functional morphology was also significantly correlated with dietary composition. While feeding roles constrained trait evolution along particular morphological axes, dietary specialization increased evolutionary rates, facilitating the evolution of more extreme morphologies. Neotropical cichlid morphological diversity has been influenced by selection and adaptive diversification especially in relation to trade-offs in bentho-pelagic foraging, and patterns of evolution in South America are consistent with a continental adaptive radiation. iii Acknowledgments Firstly, I would like to thank my supervisor Hernán López-Fernández, who provided me with countless research opportunities, offered valuable perspectives on my research from his expertise in phylogenetics and the natural history of Neotropical fishes, pushed me to aim high, and allowed me the freedom to discover and pursue research questions of my own. His mentorship has helped me to grow as a scientist and as a person. The members of my supervisory committee, Nathan Lovejoy (U of T), Don Jackson (U of T) and Peter Wainwright (UC Davis), have provided a wealth of advice through my doctoral program. Deborah McLennan (U of T) and Mark Cadotte (U of T) served on my appraisal committee and I appreciated their constructive comments on my research proposal. David Evans (U of T) and Adam Summers (University of Washington) brought their enthusiasm and insight to my final exam committee. I am also grateful to the ichthyology curators and staff of the Royal Ontario Museum (Mary Burridge, Erling Holm, Rick Winterbottom, Marg Zur and Don Stacey), whose assistance with the ROM’s fish collections and support over the last several years has been indispensable. I am also grateful to my undergraduate honours supervisor, Jeffrey Hutchings (Dalhousie), who gave me my first opportunity to study fish morphology and started me down this path in evolutionary research. Individuals at other institutions have facilitated access to data and specimens for my dissertation research. John Armbruster (AUM), D. Werneke (AUM), Roberto Reis (PUCRS), Mark Sabaj-Pérez (ANSP) and John Lundberg (ANSP) provided access to cichlid specimens used in morphological and functional analyses. Maria Claudia Malabarba (Universidade Federal do Rio Grande do Sul) provided access to and assistance with fossil cichlid collections. Kirk Winemiller (Texas A&M), Carmen Montaña (North Carolina State University), Jennifer iv Cochran-Biedermann (Texas Tech University) and Allison Pease (Winona State University) were kind enough to share with me ecological data from their Neotropical fish research programs. I have also been fortunate enough to receive financial support from NSERC (CGS M and CGS D), the Ontario government (OGS) and various fellowships/award from the University of Toronto. I would like to thank a number of ROM Ecology and Evolutionary Biology graduate students who have been both wonderful collaborators and friends. I have been fortunate to be able to share and discuss my teaching, research, and field experiences with Sarah Steele and Frances Hauser. Katriina Ilves was a mentor to me during the later stages of my academic program at U of T, and I value her camaraderie. Viviana Astudillo, Matthew Kolman, Nathan Lujan and Shannon Refvik contributed to the thoughtful and productive environment in the ROM ichthyology lab. I have also thoroughly enjoyed my opportunities for academic conversation and collaboration with Derek Larson and Caleb Brown of the ROM Palaeontology lab. I am grateful to my parents, Joseph and Edith Arbour, who encouraged my interest in math and science from a young age. My sister Victoria Arbour has been a crucial source of encouragement and advice through all of my academic years, and I have benefitted greatly from her thoughtfulness, maturity and breadth of experiences. Ginny Arbour, Oliver Arbour and Penny Staples provided unconditional support during my graduate years. Special thanks go to my partner David Staples, who has always believed in me and in my academic dreams. David, thank you for being there for every step of this journey, and hopefully for many more to come. v Table of Contents Abstract ...................................................................................................................................... ii Acknowledgements ................................................................................................................... iv Table of Contents ...................................................................................................................... vi List of Tables ............................................................................................................................. xi List of Figures ......................................................................................................................... xiv List of Appendices ................................................................................................................ xviii General Introduction ..................................................................................................................... 1 I.1 Background ............................................................................................................................ 1 I.1.1 Morphological diversity ............................................................................................ 1 I.1.1 Functional morphology ............................................................................................. 2 I.1.1 Adaptive radiation and ecological opportunity ......................................................... 3 I.1.1 Study system – Neotropical cichlids ......................................................................... 4 I.2 Aims and Scope ..................................................................................................................... 9 I.3 Overview of the Chapters .................................................................................................... 10 I.4 Contributions ....................................................................................................................... 12 1. Chapter One: Adaptive landscape and functional diversity of Neotropical cichlids: implications for the ecology and evolution of Cichlinae (Cichlidae; Cichliformes) .......... 13 1.1 Abstract ............................................................................................................................... 14 1.2 Introduction ......................................................................................................................... 15 1.3 Methods ............................................................................................................................... 17 vi 1.3.1 Phylogeny and taxonomic sampling ....................................................................... 17 1.3.2 Measuring Cichlinae functional morphology ......................................................... 19 1.3.2.1 Muscle masses ............................................................................................ 20 1.3.2.2 Lower jaw lever mechanics ........................................................................ 21 1.3.2.3 Bite occlusion ............................................................................................
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