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Evolution of Sexual Size Dimorphism in Squirrels by R. Nandini A

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Evolution of Sexual Size Dimorphism in Squirrels by R. Nandini A Evolution of Sexual Size Dimorphism in Squirrels by R. Nandini 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 December 12, 2011 Keywords: Sexual-size dimorphism, squirrels, evolution, gliding lifestyle, functional morphology Copyright 2011 by R. Nandini Approved by F. Stephen Dobson, Chair, Professor of Biological Sciences Geoffrey E. Hill, Professor of Biological Sciences Wendy R. Hood, Assistant Research Professor of Biological Sciences Richard Thorington Jr., Curator of Mammalogy, Smithsonian Institution, Washington D.C. Anindya Sinha, Professor of Biological Sciences, National Institute of Advanced Studies, India Abstract Difference between the sizes of the sexes in a species (sexual size dimorphism SSD) is a common phenomenon, and most mammals are male-biased in size. Female-biased size dimorphism (FBSD) is uncommon in mammals. Flying squirrels exhibit a unique lifestyle (gliding), which could require females to evolve larger size to attain functional or reproductive advantages. In this dissertation I examined the evolution of FBSD in flying squirrels using comparative approaches. I began by examining all squirrels and their patterns of dimorphism to determine if FBSD evolved in association with gliding. FBSD was seen to evolve multiple times across squirrels, and the ancestor to flying squirrels was male- biased, implying that FBSD evolved in association with a gliding lifestyle. An analysis of ecological predictor variables revealed that FBSD was predicted by arboreal habits, nocturnality and tropical latitudes, and that extreme MBSD was predicted by open habitats and sociality. In a second analyses, I examined body size partitioning across two sympatric squirrel communities, temporal and diurnal, in Borneo. Species and sexes partitioned themselves along a non-overlapping size spectrum, implying that species evolved specific sizes to minimize competition. SSD does not seem to enhance partitioning of resources. Finally, I examined patterns of scaling (Rensch’s rule) of FBSD across 27 flying squirrel species based on morphometric measurements from museum specimens. Flying squirrels were seen to scale in accordance with Rensch’s rule, which predicts that FBSD decreases with increasing body size across related species. Females had relatively longer tails and larger heads than males, indicating that selection for enhanced gliding ability may have resulted in FBSD. Within flying squirrels, small-bodied gliders with reduced patagia had more compensatory morphological adaptations than large bodied gliders with extended patagia. Comparative phylogenetic analyses revealed that patterns of gliding morphostructure and dimorphism are deeply rooted within the phylogenetic history of this tribe. ii Acknowledgements My advisor, Steve Dobson, gave me a long enough rope to travel around the world and find my way back, and his constant support and confidence in me allowed me to pursue independent work. Over the years our numerous discussions have moulded my curiosity into a scientific framework, and I consider these interactions the most important and enjoyable experiences of my graduate career. Geoff Hill has been a steady source of encouragement, critique and practical advice throughout my PhD, and being an ‘adopted’ member of his lab has been energizing. I owe a lot to Anindya ‘Rana’ Sinha, who welcomed me into his group at NIAS, Bangalore, and his counsel and patronage have shaped me both as a professional and as a person. Wendy Hood has played a positive role in my committee, and I thank her for discussions and the quick turnaround of comments on drafts. I am grateful to Richard Thorington for his interest in my work, and for first introducing me to museums and protocol, perhaps inadvertently sparking what has turned out to be an enduring fascination. Craig Guyer played an important role in discussing ideas that shaped the proposal early on in the program. At Auburn, Jack Feminella, Mary Mendonca and the staff in the Biology Department have been very supportive in tough situations, as were several people in the Graduate and International Schools. My friends in Biology have made many semesters at Auburn enjoyable, and I would like to thank Michelle Gilley, Lesley de Souza, Jessica Stephens, Amy Skibiel, Shobnam Ferdous, Courtney Holt, David Broussard, Lynn Siefferman, and members of the Dobson and Hill labs for all their good humor and companionship. Julia Kjelgaard has been extremely hospitable numerous times over the years, and I am grateful for her generosity. A large part of my PhD duration was spent in India, developing a field project to test iii some of the predictions presented here. NIAS has been a great base to work out of, and I thank the administration, particularly Srinivas Aithal. Numerous friends and colleagues helped me during this time in India, and I name a few: Divya Mudappa, T.R. Shankar Raman, Kakoli Mukhopadhyay, Kartik Shanker, Sanjay Sane, Uma Ramakrishnan, M. Ananda Kumar, Bharath Sundaram, Dilip P. Venugopal, Sindhu Radhakrishnan, Kavita Isvaran, Subhankar Chakraborty, Narayan Sharma, Shomita Mukherjee, Devcharan Jathanna, Arundhati Das, Rishi Kumar, Mayukh Chatterjee. Many people assisted me with field work in the Western Ghats, and I thank Julien Cornut, Joan Cassanelles, and my field assistants Karupuswamy, Katturaja, Loganathan, Ramesh and Sendhil for countless hours of watching flying squirrels, climbing trees and measuring plants (none of which finally figures in the following pages). Much of the data in this dissertation was collected from museums, and I thank the Curators at the Auburn University Museum, American Museum of Natural History, Bombay Natural History Society, Natural History Museum-London, Smithsonian Institution, Berlin Museum of Natural History, Senckenberg Museum of Natural History and the Zoological Survey of India for allowing me to use the collections. My field work in India and travel to museums was funded by the Ministry of Environment and Forests-Government of India, Muthoot Environment Research Foundation, Dorabji Tata Fund, AU Graduate Research Fellowships, AU Travel Awards, AU COSAM Travel Award and the Critical Ecosystem Partnership Fund. My parents, S. Rajamani and Jayashree Rajamani, and brother R. Shyam Sundar, have championed me on, even when things were bleak, and I dedicate this thesis to them. My parents-in-law, V.S. Vijayan and Lalitha Vijayan, have been a constant source of support and understanding. Urmila Lakshmanan (and her many friends), Shivkumar Kannan, Divakar Shekar, Ayshwarya Ravi, Vaishnavi Shekar, and Mitra Nataraj have hosted me innumerable times, and kept me connected to the real world with gossip and dark humour. And as I come to the end of this long process (and list), I thank most of all Robin Vijayan, for being my closest friend and companion, and sharing the excitements and frustrations of these many years. Without him much of this journey would have been incomplete. iv Table of Contents Abstract ....................................................................................................................................ii Acknowledgments ...................................................................................................................iii List of Tables ..........................................................................................................................vii List of Figures ........................................................................................................................viii Chapter 1 An Introduction to Sexual Size Dimorphism .........................................................1 Chapter 2 Origins andEcological Correlates of Sexual Size Dimorphism in Squirrels ........14 Introduction ..............................................................................................................14 Methods .....................................................................................................................18 Results ....................................................................................................................... 26 Discussion .................................................................................................................38 Literature cited .........................................................................................................42 Chapter 3 Character Displacement in Species and Sexes of Sympatric Squirrels ...............51 Introduction ..............................................................................................................51 Methods ....................................................................................................................53 Results .......................................................................................................................57 Discussion .................................................................................................................66 Literature cited .........................................................................................................69 Chapter 4 Flying Squirrels Follow Rensch’s Rule ................................................................73 Introduction ..............................................................................................................73 Methods .....................................................................................................................75
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