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Tritrophic Interactions on Cultivated Maize and Its Wild Ancestor, Teosinte

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Tritrophic Interactions on Cultivated Maize and Its Wild Ancestor, Teosinte Tritrophic interactions on cultivated maize and its wild ancestor, teosinte PhD thesis presented by Elvira S. de Lange University of Neuchâtel, Switzerland September 13th 2013 Thesis director Prof. Ted C.J. Turlings Tritrophic interactions on cultivated maize and its wild ancestor, teosinte Dissertation submitted to the University of Neuchâtel for the Degree of Doctor in Natural Sciences by Elvira S. de Lange Faculty of Science, Institute of Biology Laboratory of Fundamental and Applied Research in Chemical Ecology University of Neuchâtel Accepted by recommendation of the thesis committee: Prof. Ted C.J. Turlings, University of Neuchâtel, Switzerland (thesis director) Dr. Christophe J. Praz, University of Neuchâtel, Switzerland Prof. Florian P. Schiestl, University of Zürich, Switzerland Dr. Alisa Huffaker, USDA‐ARS, United States of America Defended on September 13th, 2013 University of Neuchâtel 2014 Faculté des sciences Secrétariat-décanat de Faculté Rue Emile-Argand 11 2000 Neuchâtel - Suisse Tél: + 41 (0)32 718 2100 E-mail: [email protected] IMPRIMATUR POUR THESE DE DOCTORAT La Faculté des sciences de l'Université de Neuchâtel autorise l'impression de la présente thèse soutenue par Madame Elvira DE LANGE Titre: Tritrophic interactions on cultivated maize and its wild ancestor « teosinte » sur le rapport des membres du jury composé comme suit: • Prof. Ted Turlings, Université de Neuchâtel, directeur de thèse • Dr Christophe Praz, Université de Neuchâtel • Prof. Florian Schiestl, Université de Zürich • Dr Alisa Huffaker, USDA-ARS, Center for medical, Agricultural and veterinary Entomology, Gainesville, FL, USA Neuchâtel, le 13 janvier 2014 Le Doyen, Prof. P. Kropf Imprimatur pour thèse de doctorat www.unine.ch/sciences Key words / Mots clés Key words Campoletis sonorensis, Chemical ecology, Cotesia marginiventris, Corn, Domestication, Fall armyworm, Green leaf volatiles, Herbivore‐induced plant volatiles, Host plant, Insect herbivore, Maize pest, Mexico, Natural enemy, Parasitoid wasp, Plant defense, Spodoptera frugiperda, Teosinte, Tritrophic interactions, Volatile organic compounds, Zea mays Mots clés Campoletis sonorensis, Écologie Chimique, Cotesia marginiventris, Maïs, Domestication, Légionnaire d'automne, Green leaf volatiles, Odeurs induites, Plante hôte, Insecte herbivore, Ravageur du maïs, Mexique, Ennemi naturel, Guêpe parasitoïde, Défense des plantes, Spodoptera frugiperda, Téosinte, Interactions tritrophiques, Composés organiques volatils, Zea mays Contents Contents Abstract ..................................................................................................................................... 7 Résumé ...................................................................................................................................... 9 Resumen .................................................................................................................................. 13 Zusammenfassung ................................................................................................................... 15 Samenvatting ........................................................................................................................... 19 General introduction ............................................................................................................... 23 Chapter 1 Insect and pathogen resistance in cultivated maize and its wild ancestor, teosinte ............................................................................................ 39 Chapter 2 Natural presence of insect pests on teosinte, the ancestor of maize, in Mexico .............................................................................................. 59 Chapter 3 Has maize lost some of its ability to attract parasitoids during domestication? ................................................................................................ 75 Chapter 4 Behavior and performance of fall armyworm and its parasitoids on cultivated maize and its wild ancestor, teosinte ............................................. 93 Chapter 5 Parasitic wasps can reduce mortality among caterpillar‐infested teosinte plants ............................................................................................... 115 Chapter 6 Are green leaf volatiles important for parasitoid wasp attraction in the field? ........................................................................................................ 137 General discussion................................................................................................................. 157 References ............................................................................................................................. 163 Acknowledgements ............................................................................................................... 183 Annex 1 ....................................................................................................................................... I Annex 2 ...................................................................................................................................... V Curriculum vitae ..................................................................................................................... XIX Front cover pictures: A female parasitoid wasp, Campoletis sonorensis, localizes and parasitizes her lepidopteran host, Spodoptera frugiperda, while the latter is feeding on a maize plant. Pictures: Matthias Held 5 Abstract Abstract Modern maize plants (Zea mays ssp. mays, Poaceae) are characterized by large cobs that contain juicy grains, although they have not always had these characteristics. Approximately 9000 years ago, maize was domesticated from teosinte (Z. mays ssp. parviglumis), its wild ancestor, which produces much less and much smaller seeds. Teosinte still grows in the wild in southern Mexico, while cultivated maize is produced all over the world. Continuous selection for improved yield and quality has had a cost for the plant in terms of the loss or alteration of other potentially useful traits, such as resistance to pathogens and herbivorous insects (reviewed in Chapter 1). This thesis focuses on the resistance of maize and teosinte against insect pests, in particular with respect to the emission of herbivore‐induced volatiles. This feature is considered an indirect defense trait, as the volatiles can betray the presence of prey or hosts to predators and parasitoids, natural enemies of herbivorous insects. Among these natural enemies are parasitoid wasps, of which females have an ovipositor with which they can lay single or multiple eggs in individual hosts. When the wasp larvae develop inside the host they will eventually kill it, potentially benefitting the plant. At first, we assessed in nature which insect pests occur on teosinte (Chapter 2). Fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), is reported as one of the main maize pests in the Americas, and is frequently attacked by many species of parasitoids. However, little is known about the presence of this herbivore and its associated parasitoids on teosinte. In a laboratory setting, we then assessed whether maize and teosinte emit a similar blend of volatiles when induced by lepidopteran herbivores. We also evaluated the attractiveness of the odor blends to females of two species of solitary koinobiont endoparasitoid wasps, Campoletis sonorensis (Hymenoptera: Ichneumonidae) and Cotesia marginiventris (Hymenoptera: Braconidae). Although the odor blends appeared similar upon gas chromatography analysis, the foraging parasitoids responded differentially to them. C. sonorensis did not distinguish between the odors, whereas C. marginiventris showed a preference for the odors of teosinte over those of maize (Chapters 3, 4). We obtained similar results when testing real plants and extracts of collected odors (Chapter 3) indicating that these extracts can be used to identify the key compounds that are responsible for parasitoid wasp attraction. Interestingly, we observed that the host plant, i.e. cultivated maize or wild teosinte, can have an effect on the development of parasitoid larvae within their host. While C. marginiventris developed equally well when their host, S. frugiperda, had been feeding on maize or teosinte, C. sonorensis cocoons were larger when their host had fed on maize plants. Since C. marginiventris wasps preferred the odors of teosinte, and C. sonorensis wasps did not display a preference for the odors of teosinte or maize, these results indicate that the parasitoids were not necessarily attracted to the plants that were best suited for the development of their offspring (Chapter 4). 7 Abstract There is surprisingly little field evidence for fitness benefits for plants due to the action of natural enemies. This is still an important point in the discussion on the possible indirect defense role of inducible plant volatiles, especially in the case of parasitoid wasps that, unlike predators, do not directly kill their hosts. Therefore, we evaluated how parasitoid wasps can affect plant performance in a semi‐natural setting in Morelia, Mexico. Our tritrophic system comprised teosinte, devoid of the pleiotropic effects of artificial selection, the herbivore S. frugiperda and the wasp C. sonorensis, all organisms that co‐occur in nature. Teosinte was planted in large screen tents, which allowed us to assess how the herbivore, in the absence or in the presence of parasitoid wasps,
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