ABSTRACT BATEMAN, MELANIE LYNN. Impact of Plant Suitability, Biogeography, and Ecological Factors on Associations between the Specialist Herbivore Heliothis subflexa G. (Lepidoptera: Noctuidae) and the Species in its Host Genus, Physalis L. (Solanaceae), in West-Central Mexico. (Under the direction of Fred Gould.) Caterpillars of the moth species Heliothis subflexa G. (Lepidoptera: Noctuidae) are known to feed exclusively on fruits of plants in the genus Physalis L. (Solanaceae). However, data were lacking on whether H. subflexa is constrained to feeding on a subset of the approximately 90 species in this plant genus. The purpose of this research has been to determine which Physalis species are utilized by H. subflexa and to assess the relative importance of plant nutritional suitability, biogeography, and ecological factors in shaping the realized host range of H. subflexa. This was accomplished through a combination of field observations of plants of 17 Physalis species occurring at 76 field sites in West-Central Mexico, a common garden study, and laboratory bioassays. Variation among Physalis species in their biogeography, life history, fruit traits, and concentrations of essential fatty acids were characterized to determine if these factors impact H. subflexa host use. The realized host range of this specialized herbivore proved to be constrained to thirteen of the seventeen Physalis species examined in this study. Heliothis subflexa varied with respect to the frequency and the intensity with which it infested these thirteen host species. Although H. subflexa’s potential host range included species that it did not infest in the field, some of the potential hosts were suboptimal for larval development, and survivorship on these Physalis species did not differ from survivorship on fruits of a non-Physalis species, Nicandra physalodes, which is not infested by H. subflexa. Positive correlations found between patterns of host use in the field, the common garden, and the laboratory bioassays indicates that plant suitability to larvae and attractiveness to ovipositing females are important determinants of H. subflexa’s realized host range. Heliothis subflexa associations with Physalis species are also influenced by biogeographical factors. Differences in host associations at low versus high elevations may be associated with contemporary population isolation and differentiation. IMPACT OF PLANT SUITABILITY, BIOGEOGRAPHY, AND ECOLOGICAL FACTORS ON ASSOCIATIONS BETWEEN THE SPECIALIST HERBIVORE HELIOTHIS SUBFLEXA G. (LEPIDOPTERA: NOCTUIDAE) AND THE SPECIES IN ITS HOST GENUS, PHYSALIS L. (SOLANACEAE), IN WEST-CENTRAL MEXICO by Melanie Lynn Bateman A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy ENTOMOLOGY 2006 APPROVED BY: ________________________________ _________________________________ _________________________________ ________________________________ Chair of Advisory Committee BIOGRAPHY Melanie Bateman comes from a long line of outdoor enthusiasts and gardeners. Her grandparents on both sides of her family would have made excellent botanists and field biologists. Enthusiasm for plants and the outdoors did not skip a generation. Melanie’s parents took her and her brother on camping and hiking trips throughout their childhoods. She has fond memories of collecting plant material for her parents’ wildflower garden. Her first job was at a plant nursery. Given her lineage and the environment in which she was raised, Melanie’s subsequent career path in biology came naturally to her. Melanie earned a B.S. in Biology from Duke University. During her undergraduate studies, she carried out independent study projects in the laboratories of Drs. Mark Rausher, Paul Manos, and Janis Antonovics with the guidance of Nora Underwood and Matt Olson. Through a summer program at the Rocky Mountain Research Laboratory in Gothic, Colorado, she had the opportunity to fly in an airplane for the first time and to get to know the American West. She also spent a semester abroad studying ecology and culture in Venezuela. After college, she worked as a research assistant for Drs. Phyllis Coley and Tom Kursar at the Smithsonian Tropical Research Station on Barro Colorado Island, Panama. During her Ph. D. studies, Melanie moved over ten times. Each time that she packed her bags, she set off on another exciting international research opportunity. The bulk of her Ph. D. research was conducted over three years in Jalisco, Mexico. During her first two years of study in Mexico, she got a taste of big city life by living in apartments in Guadalajara. In those first two years of the project, her home base was the Centro de Ciencias Biologicas y Agropecuarias of the Universidad de Guadalajara. In her third year of study in Mexico, she was based at the Estación de Biología Chamela, UNAM, on the Pacific Coast of Jalisco. Following her last year of study in Mexico, she received a scholarship from the Toepfer Foundation which allowed her to conduct research on the fatty acid concentrations in the fruits of Physalis at the Max Planck Institute in Jena, Germany. Now she awaits her next adventure. ii ACKNOWLEDGEMENTS First and foremost, I would like to thank my family: my parents for their support, their unwavering faith in me, and phone conversations that transcend the distances that separate us; my brother for his incisiveness and his intellect; and my grandparents for being a source of inspiration. I would like to express my gratitude to CC Maurer, Shawn Fitzpatrick, Newton Fitzpatrick, and Annika Schauer for being excellent roommates and forces of good in my life. I give my love and appreciation to old friends from Duke. To Kasane, Emmy, Jessica, John and Ginna: you are my fresh air and you help me to always remember who I am. New friends in Raleigh have also been invaluable. Stef, JB, Beth T., Beth M., Maria, Jeff, Skip, Chris, and Josh helped make Raleigh feel like “my town”. I am grateful to Fred Gould for all that he has given me over the years: his support, advice, access to opportunities, and patience. Likewise, Cavell Brownie helped me throughout with advice on statistical analyses. I would like to thank my committee members Trudy Mackay, Nick Haddad, and George Kennedy for their insights. All of the members of the Gould lab have been valuable sources of constructive criticism. Molly Puente is an exemplary editor. I feel lucky to have collaborated with Nicole Benda, who makes everything more fun. In general, the Bug Lab (as christened by Amanda) has been a source of companionship and commiseration. In particular, I am grateful for the friendship of Nicole, Molly, Astrid Groot, and Maria Simms. I would also like to give my heartfelt appreciation to Ofelia Vargas Ponce and Mollie Harker. Without their advice, their help, and their friendship, I would have been unable to carry out my Ph. D. research in Mexico. Mollie gave me shelter, sympathy when I was sick, rides to the university, oranges from her tree, and countless other kindnesses. Ofelia introduced me to Physalis and formal/polite communication in Spanish. I would like to express my gratitude to the researchers with whom I collaborated at the Max Planck Institute for Chemical Ecology in Jena, Germany. Birigt Schulze is a wonderful person who has an impressive ability to convey information. Through the example of Jan Schiers and David Heckel, I learned how to work in an integrated team. I can only hope to immulate their work ethic and their incisive approach. Finally, I am indebted to my sources of funding. Without support from the National Science Foundation Pre-doctoral Fellowship, the EPA NCER’s P3 Student Design Competition, the Keck Foundation, or the Toepfer Foundation, none of this research would have been possible. In particular, the Keck Center for Behavioral Biology, the P3 Student Design Competition, and the Toepfer Foundation each gave me access to unique experiences that were meaningful in ways beyond mere monetary support. Interactions associated with each of these organizations inspired me in unanticipated ways. iii TABLE OF CONTENTS Page LIST OF TABLES . vi LIST OF FIGURES . viii 1. INTRODUCTION . 1 Why are there so many species? . 1 How is herbivore host range constrained? . 2 Case studies as a tool for the study of plant-herbivore interactions . .. 3 Heliothis subflexa & Physalis, a case study . 5 References . 8 2. IMPACT OF PLANT SUITABILITY, BIOGEOGRAPHY, AND ECOLOGICAL FACTORS ON ASSOCIATIONS BETWEEN THE SPECIALIST HERBIVORE Heliothis subflexa G. (Lepidoptera: Noctuidae) AND PLANTS IN THE GENUS Physalis L. (Solanaceae) . 14 Abstract . 15 Introduction . 16 Methods . 18 Results . 28 Discussion . 33 Acknowledgements . 35 References . 35 Tables and Figures . 42 3. BIOGEOGRAPHICAL PATTERNS OF PHYSALIS (SOLANACEAE) DISTRIBUTION IN WEST-CENTRAL MEXICO . 54 Abstract . 55 Introduction . 56 Methods . 58 Results . 63 Discussion . 66 Acknowledgements . 69 References . 69 Tables and figures . 74 4. VARIATION AMONG ELEVEN SPECIES OF PHYSALIS (SOLANACEAE) IN LIFE HISTORY . 81 Abstract . 82 Introduction . 83 Methods . 85 iv Results . 91 Discussion . 93 Acknowledgements . 94 References . 94 Table and figures . 98 5. VARIATION IN ESSENTIAL FATTY ACID CONCENTRATIONS IN THE FRUITS OF NINE PHYSALIS SPECIES & ITS RELATIONSHIP TO HERBIVORE DEFENSE . 109 Abstract . 110 Introduction . 110 Methods . 112 Results . 116 Discussion . 117 Acknowledgements . 118 References . 118 Tables and figures . 122 6. Appendices . 129 A. Description of the field sites in West-Central Mexico, 2002-2004 . 130 B. Insects found in association with Physalis plants in the field and in the common gardens in West-Central Mexico . 134 C. SAS codes for some key statistical tests . 135 v LIST OF TABLES TABLE 2.1. Description of the 17 Physalis species examined in this study . 42 TABLE 2.2. Time period of data collection in the field in each year of the study . 44 TABLE 2.3. Description of the H.subflexa laboratory colonies that were used in the bioassays and the conditions under which they were maintained . 44 TABLE 2.4. Results of logistic regression on the percentage of plants with H.