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Colour Vision and Mate Choice in the Family Poeciliidae

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Colour Vision and Mate Choice in the Family Poeciliidae Beauty in the Eyes of the Beholders: Colour Vision and Mate Choice in the Family Poeciliidae by Benjamin Alexander Sandkam B.Sc. (Integrative Biology), University of Illinois at Urbana-Champaign, 2009 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biological Sciences Faculty of Science © Benjamin Alexander Sandkam 2015 SIMON FRASER UNIVERSITY Fall 2015 Approval Name: Benjamin Alexander Sandkam Degree: Doctor of Philosophy (Biological Sciences) Title: Beauty in the Eyes of the Beholders: Colour Vision and Mate Choice in the Family Poeciliidae Examining Committee: Chair: Gerhard Gries Professor Felix Breden Senior Supervisor Professor Wendy Palen Supervisor Associate Professor Kimberly Hughes Supervisor Professor Department of Biological Science Florida State University Michael Hart Internal Examiner Professor Department of Biological Sciences Karen Carleton External Examiner Associate Professor Department of Biology University of Maryland, College Park Date Defended/Approved: September 21, 2015 ii Ethics Statement iii Abstract Sexual selection plays a major role in numerous aspects of evolution. Many models have attempted to explain how mate preferences evolve both across populations within a species and across species. ‘Sensory bias’ predicts that the traits involved in mate choice will co-evolve with the tuning of the sensory systems responsible for detecting such traits. The family Poeciliidae is a classic system for studies of mate choice and provides an excellent opportunity to examine the co-evolution of preference for colour traits and the sensory system detecting such traits: colour vision. In this dissertation, I present a body of work investigating how colour vision differs across species and populations, thus exploring the potential role sensory systems have in shaping mate preferences. To do this, I focus on the opsin genes, which play a predominant role in tuning the wavelength sensitivity of cone cells – the detectors for colour vision. I found the Long Wavelength Sensitive opsins (detecting red/orange colours) experience high rates of gene conversion due to their genomic architecture. The effects of conversion may be influenced by the importance of red/orange in mate choice decisions. While traditional models of duplication and divergence suggest sensory repertoire expansion occurs slowly, I found hybridization can expand sensory repertoires in one generation. I have termed this process: Hybrid Sensory Expansion. I then focus on one species to show that differences in visual tuning (gene expression and allele frequency) co-vary with mate preferences across populations in a manner that is consistent with the Sensory Exploitation (SE) model for the evolution of female mate preferences. However, I go on to find that closely related, highly sympatric species differ in colour vision more across populations than across species within populations on mainland South America. This suggests that while SE could explain differences in mate preference across populations, it may not scale up to explain species level differences as generally assumed. Taken together, these results show that the evolution of visual tuning may not always evolve through traditional mutation-selection models and that visual systems are far more variable across populations within species than generally assumed. Keywords: Opsin; Sensory System; Ecological Genetics; Sensory Bias; Sensory Exploitation; Sexual Selection iv Dedication For family, friends, fish and fun v Acknowledgements As this thesis is a result of lifelong learning both in the classroom and out, I owe a great deal to a great many people that have touched my life over the years. Specifically, I am tremendously thankful for the wonderful guidance and support of my advisor Dr. Felix Breden who always went along with my crazy plans for projects in both the lab and field- even when it meant exhausting fieldwork. Felix has been not only an excellent mentor but also a great friend and role model. It is impossible to express my gratitude to my wife, Dr. Nora Prior, for her boundless support, insightful intellectual contributions and her uncanny ability to keep us moving forward. I thank our daughter, Ardea Sandkam, for keeping me active and sharing a love of the outdoors. I am also incredibly thankful for the amazing support of my in-laws, Dr. Julie Hengst and Dr. Paul Prior for their amazing patience, support and guidance into the world of academia. Thank you also to my close friend Matt Taves, for excellent scientific discussions while exploring nature on and under the water. I thank my parents, Tracy and Jeff Sandkam, for their support and kindling a lifelong love of the natural world. I owe a great deal to all members of the Breden and FAB* labs past and present, specifically: Drs. Mike Hart, Arne Mooers, Bernie Crespi, Corey Watson, Jeff Joy, Will Stein, Mika Mokkonen, Kristen Gorman, and Iva Popovic, for insightful feedback, training, and excellent camaraderie. Megan Young and Kristina Pohl were invaluable to my ability to work off campus and I am very grateful for their patience and assistance. A big thank you to my committee members, Drs. Kim Hughes and Wendy Palen, for the great feedback and understanding while my thesis morphed into what it has become. Thank you also to Dr. Karen Carleton for graciously taking the time to provide outside perspective as my external examiner. While not directly involved with the work of this thesis, I am incredibly grateful to Dr. Isabelle Côté for training in scientific SCUBA diving, and inspirational enthusiasm for all things aquatic. Thank you also, to my undergraduate advisor, Dr. Becky Fuller, for the opportunities, advice and support that has continued even long after leaving her lab. vi Table of Contents Approval ............................................................................................................................. ii Ethics Statement ............................................................................................................... iii Abstract ............................................................................................................................. iv Dedication .......................................................................................................................... v Acknowledgements ........................................................................................................... vi Table of Contents ............................................................................................................. vii List of Tables ...................................................................................................................... x List of Figures .................................................................................................................. xii Introductory Image .......................................................................................................... xiv Chapter 1. Introduction ............................................................................................... 1 The Family Poeciliidae ............................................................................................. 2 Mate Choice Evolution ............................................................................................. 3 Colour Vision ............................................................................................................ 5 Objectives ................................................................................................................ 7 References ........................................................................................................................ 9 Chapter 2. The impact of genomic environment on the evolution of colour vision in the family Poeciliidae, a model for visually based sexual selection ...................................................................................... 16 Publication and Contributions ................................................................................ 16 2.1. Abstract .................................................................................................................. 16 2.2. Introduction ............................................................................................................ 17 2.3. Materials and Methods ........................................................................................... 19 2.3.1. Sequencing ............................................................................................... 19 2.3.2. Tree Building ............................................................................................. 20 2.3.3. Gene Conversion Analyses in LWS Opsins .............................................. 21 2.3.4. Identifying Sites Under Selection in Non-LWS Genes .............................. 22 2.4. Results ................................................................................................................... 22 2.4.1. Data Set and Alignment ............................................................................ 22 2.4.2. Phylogenetic Analyses .............................................................................. 23 2.4.3. Gene Conversion Analyses ....................................................................... 23 2.4.4. Identifying Sites Under Selection in Non-LWS Genes .............................. 23 2.5. Discussion .............................................................................................................
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