The Nature of Defense: Coevolutionary Studies, Ecological Interaction, and the Evolution of 'Natural Insecticides,' 1959-1983 A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY Rachel Natalie Mason Dentinger IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Mark Borrello December 2009 © Rachel Natalie Mason Dentinger 2009 Acknowledgements My first thanks must go to my advisor, Mark Borrello. Mark was hired during my first year of graduate school, and it has been my pleasure and privilege to be his first graduate student. He long granted me a measure of credit and respect that has helped me to develop confidence in myself as a scholar, while, at the same time, providing incisive criticism and invaluable suggestions that improved the quality of my work and helped me to greatly expand its scope. My committee members, Sally Gregory Kohlstedt, Susan Jones, Ken Waters, and George Weiblen all provided valuable insights into my dissertation, which will help me to further develop my own work in the future. Susan has given me useful advice on teaching and grant applications at pivotal points in my graduate career. Sally served as my advisor when I first entered graduate school and has continued as my mentor, reading nearly as much of my work as my own advisor. She never fails to be responsive, thoughtful, and generous with her attention and assistance. My fellow graduate students at Minnesota, both past and present, have been a huge source of encouragement, academic support, and fun. Even after I moved away from Minneapolis, I continued to feel a part of this lively and cohesive group of colleagues. The sense of camaraderie created by the Minnesota connection is undeniable, and I anticipate many more years of intellectual exchange and friendship with these colleagues, especially Georgina Montgomery, Christine Manganaro, and Nathan Crowe. Most importantly, I thank my lucky stars that I entered the history of science and technology program in the same cohort as Gina Rumore. I can't even imagine what i graduate school would have been like without her. I am proud to have shared these years with this great historian, role model for balancing motherhood and scholarship, and dear friend. Support for my graduate work has come from the Program in the History of Science and Technology, which employed me as a teaching assistant for three years. This support was much more than financial—in particular, my experiences as a teaching assistant for Sally Gregory Kohlstedt, Susan Jones, and Mark Borrello enriched me as a scholar and as a teacher. Further financial support for both living and research expenses came from the University of Minnesota Graduate School. My graduate program and the Graduate School, in addition to the National Science Foundation (Doctoral Dissertation Research Improvement Grant #0724244), all provided the funds that enabled me travel to various corners of the United States, visiting archives and conducting oral history interviews. The generosity of my interview subjects, in taking time out of their invariably busy schedules to share their experiences and insight with me, can't be underestimated. Thank you, May Berenbaum, Paul Ehrlich, Paul Feeny, Dan Janzen, and Peter Raven. In addition, the archivists and librarians in charge of many collections have been extremely helpful—but none more so than Laurie Hannah of the C.H. Muller Library in the Cheadle Center for Biodiversity and Ecological Restoration, who opened the C.H. Muller collection and her own home to me when I traveled to Santa Barbara for the first leg of my dissertation research in 2007. Both she and Jennifer Thorsch made this one of the most satisfying and useful archival trips of my graduate research. ii My friends and family deserve much credit for their unfailing support of my academic pursuits, even when the purpose of spending so much time in school may not have always seem entirely clear to them! I often feel unworthy of the faith that these loved ones bestow on me. I sorely wish that I could have shared this success with my deeply missed grandmother, Lee. Nevertheless, her presence at my dissertation defense could be felt with the amazing showing that my fantastic family made in support of my work. Thanks for coming and cheering me on. My in-laws, the Dentingers, and my oldest and dearest friends, especially Angela and Beth, are living proof that the love of true family need not emerge from shared ancestry. Ever important, since the very beginning of my academic career almost three decades ago, has been my mother's steadfast emotional, intellectual, and technical support. Nothing seems to deplete her ability to give generously of her love and assistance—even when I call her with a desperate last-minute proofreading request! Together, her certainty of my success and her very practical help and advice have provided the firm foundation from which I still work today. There is no question that the years of my graduate work have been most profoundly shaped and fueled by the love and partnership of my husband, Bryn. A graduate student himself when we first met, he knew just how to encourage me at those moments when I was pretty sure that I was not going to make it past the next milestone. His understanding of my work in the history of science, as well as his own experiences as a scientist, have provided a wellspring of knowledge for me to draw on throughout my dissertation work. For both of us, graduate school was a test of our confidence and our iii resolve, and in facing these challenges jointly, we built our relationship with the mutual confidence and resolve that now carries us into the next phase of our life together. I think that Bryn will agree, though, that in the final stretch of this dissertation, the person most responsible for urging me on to completion was one that I have yet to meet—the baby in my belly, whose due date fast approaches now. Thank you, both Baby and Bryn, for helping me keep things in perspective during those times when it's been all too easy to become overwhelmed by the work at hand. iv This dissertation is dedicated to Bryn and to Baby M.D., whom we can't wait to meet! v Table of Contents iv List of Figures 1 Introduction 13 Chapter One: Molecularizing Plant Compounds, Evolutionizing Insect-Plant Relationships: Gottfried S. Fraenkel and the physiological study of insect feeding in the 1950s 56 Chapter Two: Selection, Natural or Unnatural: The evolution of insecticide resistance and the emergence of coevolutionary theory in the 1960s 96 Chapter Three: Biochemical interactions as adaptations: Closing the gap between evolution and ecology with coevolutionary research 148 Chapter Four: Collaboration and Conflict Where Plants and Insects Meet: Professional meetings and persuasive metaphors bring together botany and entomology 194 Chapter Five: "When is it coevolution?": Expansion and reform in coevolutionary theory from the 1970s onward 247 Conclusion 254 Bibliography vi List of Figures 19 Figure 1: Ligatured blowfly larva 35 Figure 2: "Larval growth of Tribolium confusum" 111 Figure 3: Beltian bodies and foliar nectaries of Acacia cornigera 179 Figure 4: Aerial photo of chaparral 235 Figure 5: Cluster analyses relating plant species and their chemistry vii Introduction This dissertation is a historical account of one of the most compelling concepts in evolutionary biology in the last half of the 20th century: the notion that organisms of different species, and even different kingdoms, can evolve in close, reciprocal response to one another. At the same time, it is an examination of some of the ways that human action in the natural world can change how biologists understand nature. Coevolutionary theory has deep roots in the history of biology. Darwin himself was fascinated by what he called “coadaptation,” particularly between flowers and their insect pollinators. These intricately specialized adaptations provided him with evolutionary stories that continue to capture our imaginations in the present day. Yet the field of “coevolutionary studies” was something different. Becoming a vigorous domain of discovery in the 1960s, its practitioners were direct inheritors of the modern evolutionary synthesis of the 1940s. They were also direct inheritors of a natural environment that seemed increasingly on the decline, thanks primarily to the destructive actions of humans. Thus, in my account, knowing—the pursuit of knowledge about the natural world—is inextricably interwoven with doing—the practical business of interacting with and altering the natural world, for better or worse. While this dissertation falls solidly within the domain of the history of biology, it also draws significantly from the recent work of environmental historians, whose interrogation of the relationship between nature and human culture has proved an invaluable resource. Through his history of the Columbia River, Richard White writes of "knowing nature through labor," where the process of work, of exerting the human 1 presence upon nature, whether mediated by technology or not, not only teaches us what nature is, but also embeds human beings in the natural world "so thoroughly that they can never be disentangled."1 Similarly, Edmund Russell's work on the development of chemical warfare, against humans and against insect pests, shows how technology transformed our views of both nature and of ourselves. In the past, "we have seen war and interactions with nature as separate, even opposite endeavours," Russell writes, but "the control of nature expanded the scale of war, and war expanded the scale on which people controlled nature. More specifically, the control of nature formed one root of total war, and total war helped expand the control of nature to the scale rued by modern environmentalists."2 Critically, both Russell and White explore the multiplicity of meanings of "nature," revealing permeability in the supposedly reliable boundary between the natural and the technological.