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Behavioural Innovation and the Evolution of Cognition in Birds

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Behavioural Innovation and the Evolution of Cognition in Birds BEHAVIOURAL INNOVATION AND THE EVOLUTION OF COGNITION IN BIRDS Sarah Elizabeth Overington Department of Biology McGill University, Montreal September 2010 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctor of Philosophy. © Copyright: Sarah E. Overington, 2010 DEDICATION For my son and my father, who crossed paths for a few short months this year: Kai James, born February 18, and Murray James, died April 10. 2 ACKNOWLEDGEMENTS The insight, creativity and humour of my PhD supervisor, Louis Lefebvre, is behind all of the work in this thesis, and I thank him immensely for his role in shaping me into the researcher I am today. He encouraged me to develop strong hypotheses and predictions, but also to pay attention to the cues of my stubborn experimental subjects in Barbados and to adjust my work to make it feasible. Louis allowed me the freedom to collaborate with researchers at many other institutions, thus satisfying my urge to approach a very broad thesis question using as many relevant techniques as possible. Neeltje Boogert has been my foremost collaborator and a great friend from the start of this degree. My thesis would not exist were it not for her discussions, comments, very thorough editing and laughter throughout the process. She also contributed data to this thesis, from catching birds in Barbados and measuring skulls in museum collections to conducting analyses. She is a great teacher and scientist, and I look forward to our continued collaboration. Julie Morand-Ferron acted as a mentor and friend, guiding me through my PhD and providing great ideas and discussions. She has continued to be a valued McGill lab-mate even as she pursues postdoctoral work at Oxford. I thank my supervisory committee members, Rüdiger Krahe and Karim Nader. Their enthusiasm for my research made committee meetings enjoyable and productive. Rüdiger and Karim both provided thoughtful comments throughout the thesis, and their suggestions led to some important changes in my experimental design in Chapters 5 and 6. None of the work with grackles would have happened without the enthusiastic contributions of Laure Cauchard and Kimberly-Ann Côté. I thank them for their long hours of research in the field, for their positive attitude toward stubborn birds, and for their friendship in Barbados and beyond. Thanks also to Laure for translating several iterations of my thesis abstract. I am grateful to the staff at Bellairs Research Institute in St James, Barbados, for all of their support while I carried out research there. 3 Many thanks to Luisa Sabaz, Linda Morai, Zabrina Kadkhodayan and especially Susan Bocti in the Department of Biology who helped with all things practical and administrative. Susan made sure everything happened on time during my degree, and facilitated both my stint as a visiting student at Yale and my maternity leave. She is the ideal graduate program administrator and I will always appreciate the support and guidance she provided during my PhD. The Behavioural Ecology Discussion Group provided many good discussions and ideas for this thesis. In particular Patrick Leighton, Don Kramer, Katrine Turgeon, Richard Feldman, Aerin Jacob, Xoxo O’Farrill, and Steffi Lazerte contributed to discussions at various stages of my PhD research. I was fortunate to spend 2008-2009 as a visiting student in the Department of Ecology and Evolutionary Biology at Yale. I thank the ornithology group for an intellectually stimulating and productive year: Professor Rick Prum, for providing space and ideas, Kristof Zyskowzky, Vinod Saranathan, Patricia Brennan, and Jake Musser. While at Yale I took a course on phylogenetics taught by Thomas Near that was invaluable to the research in Chapter 2. I thank Ehab Abouheif for jointly supervising the course from McGill. I thank Lenore Fahrig and the Geomatics and Landscape Ecology Lab at Carleton for generously providing me with writing space and helpful discussions during my final year of thesis writing. Given the breadth of techniques used in my thesis, I relied heavily on the generosity of many researchers who shared their expertise. Simon Reader (University of Utrecht) provided helpful comments on several chapters of this thesis. Daniel Sol (Universitat Autònoma de Barcelona) introduced me to the comparative method, and confirmed the analyses in Chapter 1. Andrea Griffin (University of Newcastle, Australia) provided ideas about the ecological costs of innovation in Chapter 1. Andrew Iwaniuk (University of Lethbridge, Alberta) provided crucial methodological details for the endocranial measurements in Chapter 2, and shared data relevant to my project. Muir Eaton (Drake University, Iowa) shared his data on niche evolution in grackles and allies, and also provided an ornithologists’ insight into the factors driving brain size differences in this 4 clade. Scott Lanyon (University of Minnesota) allowed me to use his most recent Icteridae phylogeny, and provided useful feedback following my talk at the American Ornithologists’ Union Meeting in Philadelphia last year. Frédérique Dubois (Université de Montréal) introduced me to game theory and was an enthusiastic collaborator on Chapter 4. Chapters 3, 4, 5 and Appendix 2 have all been published, and I thank the anonymous referees whose comments improved all of these works tremendously. The research in this thesis was supported by grants to Louis Lefebvre from NSERC and FQRNT. I am grateful for CGS-M and PGS-D scholarships from NSERC (2005-2010) and a doctoral fellowship from FQRNT (2010) that supported me throughout my PhD. Thanks also to NSERC for recognizing the challenges of raising children while doing research and providing me with a much-needed four-month leave this winter after my son was born. As in all of my endeavours, my family provided great support through this degree. Thank you to my parents, Nancy and Murray, my brother Jeff, and especially to my sister Louise. Louise helped directly with several parts of this thesis (video coding, formatting references, many hours of proof-reading) and her ability to say the right thing in moments of doubt gave me the confidence I needed in the final years of graduate work. Thanks to my grandmother, Val, and my grandfather, Roy for their constant enthusiasm about my research. Thanks also to my mother- and father-in-law, Sari and Neil Tudiver, who encouraged me and gave excellent advice, having gone through the joys and pains of PhD research themselves. Finally, thank you to my husband and greatest supporter, Simon. My partner in everything, his contributions to this thesis are both measurable (assistance in the field, help in formulating ideas and hypotheses, preparation of papers and presentations, thorough editing and formatting of this thesis) and immeasurable. 5 ABSTRACT Cognition shapes the interactions of an animal with its environment. Species vary greatly in all aspects of cognition, and studying the relationship between this variation and ecology is crucial for understanding how intelligence has evolved. In this thesis, I approach questions about the ecology and evolution of cognition that are often ignored because cognition is difficult to quantify. I use innovation rate as an operational measure and residual brain size as a correlate of general cognition in birds. I first examine the link between cognition and ecology through comparative analyses of the relationships between residual brain size, innovativeness, and measures of ecological generalism across a broad sample of the avian phylogeny, and within a single clade (Icteridae). I find that innovation is positively correlated with habitat breadth but not diet generalism, and that neither measure of generalism is associated with residual brain size. Although residual brain size and innovation rate are strongly correlated with one another, they each appear to have different relationships to a species’ ecology. Further analysis finds that the relationship between innovativeness and residual brain size is driven by innovations that involve the use of novel foraging techniques and not the ingestion of new food items. Comparative studies use the traits of extant species to infer their evolutionary history, but can only speculate on the forces driving changes in a trait. The latter half of my thesis focuses on these underlying forces and behavioural mechanisms. Using a game theory model, I show that unpredictable food availability might drive both behavioural flexibility and sociality, two traits strongly associated with cognitive complexity. Finally, I focus on innovativeness at the intraspecific level and examine foraging innovation in a large-brained grackle species, Quiscalus lugubris. I find that this gregarious species is slower to innovate when conspecifics are nearby, and that individuals differ in their ability to solve novel problems. I use these differences to describe the process of innovation, and show that novelty responses, attention, persistence, and flexibility are all important factors underlying individual variation in the ability to innovate. 6 RÉSUMÉ La cognition dirige les interactions d’un animal avec son environnement. Les espèces varient énormément dans tous les aspects de la cognition, et étudier les relations entre ces variations, l’écologie et l’évolution est crucial pour comprendre comment l’intelligence a évolué. Dans cette thèse, j’aborde les questions de l’écologie et l'évolution de la cognition souvent ignorées, la cognition étant difficile à évaluer quantitativement. J’ai utilisé le taux d’innovation comme une mesure opérationnelle, et la taille résiduelle du cerveau comme un corrélat de la capacité cognitive générale des oiseaux. J’ai d’abord examiné le lien entre la cognition et l’écologie en procédant à des analyses comparatives des relations entre la taille résiduelle du cerveau, la capacité innovatrice, et des mesures du généralisme écologique à travers un large échantillon de la phylogénie aviaire, et dans un clade unique (Icteridae). J’ai trouvé que la capacité innovatrice est corrélée positivement avec l’étendue de l’habitat, mais non avec le régime généraliste, et qu’aucune mesure du généralisme n’est associée avec la taille résiduelle du cerveau.
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