How Region Scaling and Energetic Costs Influence Brain Size
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Washington University in St. Louis Washington University Open Scholarship Arts & Sciences Electronic Theses and Dissertations Arts & Sciences Summer 8-15-2018 The oC sts of a Big Brain: How Region Scaling and Energetic Costs Influence Brain Size Evolution in Weakly Electric African Fishes (Mormyridae) Kimberley Varunee Sukhum Washington University in St. Louis Follow this and additional works at: https://openscholarship.wustl.edu/art_sci_etds Part of the Biology Commons, Developmental Biology Commons, Evolution Commons, and the Neuroscience and Neurobiology Commons Recommended Citation Sukhum, Kimberley Varunee, "The osC ts of a Big Brain: How Region Scaling and Energetic Costs Influence Brain Size Evolution in Weakly Electric African Fishes (Mormyridae)" (2018). Arts & Sciences Electronic Theses and Dissertations. 1655. https://openscholarship.wustl.edu/art_sci_etds/1655 This Dissertation is brought to you for free and open access by the Arts & Sciences at Washington University Open Scholarship. It has been accepted for inclusion in Arts & Sciences Electronic Theses and Dissertations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. WASHINGTON UNIVERSITY IN SAINT LOUIS Division of Biology and Biomedical Sciences Evolution, Ecology, and Population Biology Dissertation Examination Committee: Bruce A. Carlson, Chair Yehuda Ben-Shahar Carlos A. Botero Jason Knouft Allan Larson The Costs of a Big Brain: How Region Scaling and Energetic Costs Influence Brain Size Evolution in Weakly Electric African Fishes (Mormyridae) by Kimberley Varunee Sukhum A dissertation presented to the Graduate School of Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy August 2018 Saint Louis, Missouri © 2018, Kimberley V. Sukhum TABLE OF CONTENTS List of Tables……………………………………………………………………….......................v List of Figures……………………………………………………….……………………………vi Acknowledgements…………………………………………………..…………………………..vii Abstract……………...…….…………………………………………………………………...…ix Chapter 1. Introduction ……………………………………………………………………….1 1.1 Introduction……………………………………………………………………………2 1.2 The evolution of brain regions scaling………………………………………………...2 1.3 Determining degree of encephalization……………………………………………….5 1.4 Energetic costs in the evolution of encephalization…………………………………...6 1.5 Study system: Mormyrids……………………………………………………………..9 Chapter 2. Extreme enlargement of the cerebellum is associated with the evolution of active electrolocation in weakly electric African fishes…………………………12 2.1 Abstract………………………………………………………………………………13 2.2 Introduction…………………………………………………………………………..14 2.3 Results………………………………………………………………………………..15 2.3.1 The cerebellum is enlarged in mormyroid species………………………15 2.3.2 Mosaic shifts in brain region sizes are associated with the evolution of active electrosensing…………………………..……..………………..19 2.3.3 Both concerted and mosaic evolution are evident across osteoglossomorphs……………….…………..…………………………..25 2.3.4 Shifts in brain shape between mormyrids and outgroup species.….………27 2.4 Discussion……………………………………………………………………………31 2.5 Methods………………………………………………………………………………32 2.5.1 Specimens………………………………………………………………….32 2.5.2 Perfusion…………………………………………………………………...32 ii 2.5.3 Micro-computed tomography scans………………………………….…….33 2.5.4 Brain Organization and Structural Delineation…………………………….33 2.5.5 Determining brain volumes………………………………………………...36 2.5.6 Phylogenetic comparisons…………………………………………………36 2.5.7 Geometric morphometric analysis of brain shape…………………………39 2.6 Acknowledgements…………………………………………………………………..40 Chapter 3. The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes………41 3.1 Abstract………………………………………………………………………………42 3.2 Introduction…………………………………………………………………………..43 3.3 Results………………………………………………………………………………..45 3.3.1 Relative brain size varies widely among mormyrids…………………….45 3.3.2 Relative brain size does not correlate linearly with the relative size of other organs…………………………………………………………...48 3.3.3 Brain size correlates with oxygen consumption…………………………51 3.3.4 Large-brain mormyrids have relatively low hypoxia tolerance………….54 3.4 Discussion……………………………………………………………………………58 3.5 Experimental Procedures…………………………………………………………….61 3.5.1 Organ size measurements…………………………………………………61 3.5.2 Testing for fixation artifacts in organ size measurements………………...61 3.5.3 Phylogenetic comparisons and correlations………………………………62 3.5.4 Testing assumptions of PGLS…………………………………………….66 3.5.5 Randomization test for spurious correlations due to uneven residuals…...66 3.5.6 Linear vs. non-linear modeling of allometric relationships of organ sizes and oxygen consumption…………………………………………………67 3.5.7 Oxygen consumption rate measurements………………………………...67 3.5.8 Determining hypoxia tolerance…………………………………………...68 3.6 Acknowledgements…………………………………………………………………..70 iii Chapter 4. Enlarged brains result in varied costs within highly encephalized species of weakly electric mormyrid fishes…………………………………………………71 4.1 Abstract………………………………………………………………………………72 4.2 Introduction…………………………………………………………………………..73 4.3 Methods………………………………………………………………………………74 4.3.1 Animal care…………………………………………………………...……74 4.3.2 Specimens………………………………………………………………….75 4.3.3 Oxygen consumption rates…………………………………………………75 4.3.4 Hypoxia tolerance………………………………………………………….76 4.3.5 Organ size measurements………………………………………………….77 4.3.6 Data and statistical analyses……………………………………………….77 4.4 Results………………………………………………………………………………..78 4.4.1 Relative brain size varies among three focal species…………………….78 4.4.2 A large-brained species has a negative correlation between relative brain size and both relative liver and skeletal/muscle mass……………..80 4.4.3 A small-brained species has a positive relationship between relative brain size and oxygen consumption ……………………………………..84 4.4.4 No relationship between hypoxia tolerance and relative brain size within species…………………………………………………………….86 4.5 Discussion……………………………………………………………………………88 Chapter 5. Conclusion…………………...…………………………………………………..93 5.1 Introduction…………………………………………………………………………..94 5.2 Mormyrids as a study system for brain size evolution……………………………….94 5.3 Selective pressure in the evolution of brain region scaling…………………………..95 5.4 Energetic costs of the evolution of extreme encephalization…………………………97 5.5 Benefits of increased brain size………………………………….………………….100 5.6 Conclusions…………………………………………………………………………101 References………………………………………………………………………………………103 iv LIST OF TABLES Table 2.1…………………………………………………………………………………………22 Table 2.2…………………………………………………………………………………………38 Table 3.1…………………………………………………………………………………………46 Table 3.2…………………………………………………………………………………………46 Table 3.3…………………………………………………………………………………………49 Table 3.4…………………………………………………………………………………………63 Table 4.1…………………………………………………………………………………………81 Table 4.2…………………………………………………………………………………………83 v LIST OF FIGURES Figure 2.1………………………………………………………………………………………...17 Figure 2.2………………………………………………………………………………………...18 Figure 2.3………………………………………………………………………………………...21 Figure 2.4………………………………………………………………………………………...23 Figure 2.5………………………………………………………………………………………...24 Figure 2.6………………………………………………………………………………………...26 Figure 2.7………………………………………………………………………………………...28 Figure 3.1………………………………………………………………………………………...47 Figure 3.2………………………………………………………………………………………...50 Figure 3.3………………………………………………………………………………………...52 Figure 3.4………………………………………………………………………………………...53 Figure 3.5………………………………………………………………………………………...56 Figure 3.6………………………………………………………………………………………...57 Figure 4.1………………………………………………………………………………………...79 Figure 4.2………………………………………………………………………………………...82 Figure 4.3………………………………………………………………………………………...85 Figure 4.4………………………………………………………………………………………...87 vi ACKNOWLEDGEMENTS First and foremost, I would like to thank my advisor, Bruce Carlson, for his mentorship and support throughout my Ph.D. I’ve come a long way as a researcher, writer, and presenter, and I owe a lot to his mentorship and advice over these 6 years. Our weekly mentoring meetings never failed to give me direction and encouragement for the next week. His ability to create a sense of community within the lab produced a work environment that was conducive not only to great science but great relationships. Further he always encouraged my interests in teaching and outreach. I also want to acknowledge the members of my thesis committee: Allan Larson, Yehuda Ben-Shahar, Jason Knouft, and Carlos Botero. Each member came to my thesis committee meetings enthusiastic and excited about my projects. Each update never failed to provoke fascinating discussion and leave me with interesting new directions to pursue. I would also like to thank other EEPB and Biology Department faculty and staff who have helped me grow as a scientist. It was because of my stellar internship with Peter Hoch in 2010 that I began to consider doing graduate work at Washington University. Joan Strassmann has been a wonderful teaching and rotation mentor. Her support throughout these years has always been appreciated. I would like to thank Ken Olsen for his mentorship in teaching. I would like to thank Marta Wegorzewska for all of her wonderful writing advice and edits. I would like to thank my colleagues in the Carlson Lab for their advice and support throughout my graduate school education: Xiaogeng Ma, Tsunehiko Kohashi, Christa Baker, Alejandro Vélez, Adalee Lube, and Erika Schumacher. Further, this work would not have been possible without