Veilleux 2012 Dissertation FIN
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Copyright by Carrie Cecilia Veilleux 2012 The Dissertation Committee for Carrie Cecilia Veilleux Certifies that this is the approved version of the following dissertation: Effects of Light Environments on the Evolution of Primate Visual Systems Committee: E. Christopher Kirk, Supervisor Deborah A. Bolnick Molly E. Cummings Rebecca J. Lewis Liza J. Shapiro Effects of Light Environments on the Evolution of Primate Visual Systems by Carrie Cecilia Veilleux, B.A.; M.A. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin May 2012 Dedication For Drew, who gives me the strength to chase the moon, and Natalie, with whom I want to share it. Acknowledgements Like all dissertations, this one has been an incredibly collaborative effort. As I worked to unite such diverse research methodologies, I received substantial support and advice from experts in each area. First and foremost, I would like to thank my advisor Chris Kirk for all of the advice, support, comments, criticisms, and general awesomeness that he has provided over the past eight years. It’s been fun to watch my writing style, presentation style, and general concept of science (go comparative method!) evolve through my interactions with Chris, and I feel that he is responsible for most of my development into an actual primate sensory ecologist from an eager undergraduate interested in fossil functional morphology. While Chris has not entirely broken me of my love of long sentences, I have to say, I don’t think you’ll find one inappropriately used semi-colon in this dissertation. I would also like to offer my eternal gratitude to Deborah Bolnick, who has gone above and beyond the role of “committee member” as she helped me on my quest to become a primate geneticist. She has been incredibly patient and generous as I navigated the complex world of cloning, selection tests, and weird results. Through this experience, I’ve come to think of Deborah as a second advisor. I am also very grateful for the assistance and advice of the other wonderful members of my committee. I think I lucked out in constructing such an amazing and helpful dissertation committee. Becca Lewis introduced me to the wonders of Madagascar and has been a source of inspiration and ideas during the development of this project and interpreting its results. Her advice and support, particularly while we were in the field at Kirindy Mitea, were crucial as I adapted methodology to the situation on the ground, so to speak. Molly Cummings was also instrumental in the development and v analysis of this project, particularly the field component. Molly generously shared her expensive light equipment for a project that required taking it by oxcart to a remote site in Madagascar. After I returned, she was incredibly helpful in interpreting the results and I think our regular meetings are entirely responsible for Chapter 3. I am also very thankful to Liza Shapiro for advice, support, and criticisms. Liza has a knack of getting to the heart of the matter and asking the hard questions. My interactions with her have trained me to think in terms of “so what, why should I care?” as I write and present my findings. Her courses firmly grounded me in scientific thought, and I will never forget the gubernaculum. I would also like to thank my undergraduate advisor, Leanne Nash, for advice and encouragement. Her work on nocturnal lemurs and moonlight was particularly inspiring for the development of this project. This dissertation would have been impossible without the assistance and advice of the many people that helped me get to and work in Madagascar. I am very grateful for the support of the Leakey Foundation, the Wenner Gren Foundation, the American Society of Mammalogists, and the Lewis and Clark Fund for Exploration and Field Research. The officials at the Institute for Conservation of Tropical Environments (ICTE), MICET (particularly Benjamin Andriamihaja), and Madagascar National Parks were instrumental in facilitating my research. I am grateful for the support and advice of Pat Wright, Sarah Zohdy, and Rachel Jacobs, as well as the staff at Centre ValBio during my time at Ranomafana National Park. I am also grateful for the support of Becca Lewis, Desperat, and the crew that supported my work at Kirindy Mitea National Park. This research would not have been possible without the assistance of RAKOTOSOLOFO Andrianandrasanarivelo, Reziky Clement, Birevotra Faharoy, Géorges RAZAFINDRAKOTO, AimeNoel NDRIATAHINA, and Jean Baptiste VELONTSARA. vi Solofo and Reziky in particular helped make our nocturnal research into fun adventures in learning Malagasy, and our days into endless Uno games. The genetics component of this dissertation would not have been possible without the generosity of Ed Louis and staff at the Henry Doorly Zoo in Omaha. They welcomed me into their lab and shared genomic samples for my analyses. These analyses were supported by the National Science Foundation, Sigma Xi, and the University of Texas at Austin. I am also grateful for all of the wonderful undergraduates who poured and visualized gels and purified PCR products over the years, including Kelly Chapman, Elissa Ludeman, Maeve Cavanagh, Maggie Mitchell, Jenna Strawbridge, and Jonathan Kincaid. Additionally, I am really grateful to my fellow grad students Jaime Mata- Miguez and Rick Smith in anthropology and Lisa Snowberg and Will Stutz in biology for all of their advice on R, statistical analyses, genetic troubleshooting, and cloning. I’d also like to thank Holly Bonine for all of the fun times in the lab running PCRs and purifying samples. Finally, PJ Perry has been incredibly generous with advice and support in genetic analysis methods. UT Austin’s physical anthropology department has a really close-knit and amazing group of graduate students and postdocs. I’m grateful for all of the time and support these awesome people have donated in reading my manuscripts, critiquing my presentations, celebrating my achievements, and being sounding boards for my ideas. So I’d like to thank Angel Zeininger, Andrew Barr, Laurel Carnes, Amy Whitaker, Matt Killberger, Carl Toborowsky, Brett Nachman, Gabrielle Russo, Amber Heard Booth, Jesse Young, Jaime Mata-Miguez, Rick Smith, Kat Bannar-Martin, Kelsey Ellis, and Krista Church for all of their support. Additionally, discussions with the students and faculty at the Lund University Sensory Ecology Course really contributed to the sensory ecological theory underlying this dissertation. Finally, I’d like to thank my partners in vii crime—people who have been my writing buddies at all stages of this dissertation, including Clara Scarry, Beth Dawson, Jenny Carlson, Tessa Farmer, Carla Klehm, and Robyn Dodge. On a lighter note, I’d like to thank Bill, Kristin, Austin, and the rest of the staff at Bennu Coffee, who kept me dosed up in soy Don Quixotes, sometimes on their tabs. Additionally, this dissertation would not be complete without acknowledging the cast, crew, and writers of Battlestar Galactica for providing me with a productive and thought- provoking reward after long difficult days. Finally, I’d not be finishing this dissertation without the support of my family. My parents encouraged me in pursuing my dreams and are a constant source of advice and support. Drew is the best boy a girl could have- he’s been incredibly supportive throughout this journey. He’s read grant and manuscript drafts, listened to practice talks, cooked for me, brought me coffee, and probably can describe my dissertation nearly as well as I can. My dogs Mendel and Darwin kept me company on the long days and nights I’d be writing, making sure I get sunlight at least sometimes. And lastly, Natalie has taught me how to effectively manage my time, showing me that a toddler and a dissertation can actually coexist and grow together. viii Effects of Light Environments on the Evolution of Primate Visual Systems Carrie Cecilia Veilleux, Ph.D. The University of Texas at Austin, 2012 Supervisor: E. Christopher Kirk Primate habitats differ dramatically in the intensity and spectral quality (color) of ambient light. However, little research has explored the effects of habitat variation in ambient light on primate and mammalian visual systems. An understanding of variation in nocturnal light environments is particularly lacking, considering the significance of nocturnality and vision in primate evolutionary hypotheses. In this dissertation, I explored effects of habitat variation in light environments on primate visual evolution in three studies. First, I examined how variation in ambient light intensity influenced visual morphology in 209 mammals. Second, I analyzed effects of variation in nocturnal light environments on color vision in nocturnal primates and mammals. For this second objective, I first identified factors influencing variation in nocturnal light environments within and between habitats in Madagascar and explored how nocturnal light spectral quality has influenced mammalian visual pigment spectral tuning. I then analyzed selection acting on the SWS1 opsin gene (coding for blue-sensitive cone visual pigments) between nocturnal lemurs from different habitat types to explore whether nocturnal light environments affect selection for dichromatic color vision. The results of all three studies suggest that habitat variation in light environments has had a significant influence on primate and mammalian visual evolution. In the first ix study, I found that day-active mammals from forested habitats exhibited larger relative cornea size compared to species from open habitats, reflecting an adaptation to increase visual sensitivity in diurnal forests. The results of the second study revealed that forest and woodland habitats share a yellow-green dominant nocturnal light environment and that nocturnal vertebrates exhibit visual pigments tuned to maximize photon absorption in these environments.