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Taxonomy, Phylogeny and Resource Use of Glyptapanteles (Hymenoptera: Braconidae, Microgastrinae), Genus Highly Diversified in the Neotropics

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Taxonomy, Phylogeny and Resource Use of Glyptapanteles (Hymenoptera: Braconidae, Microgastrinae), Genus Highly Diversified in the Neotropics TAXONOMY, PHYLOGENY AND RESOURCE USE OF GLYPTAPANTELES (HYMENOPTERA: BRACONIDAE, MICROGASTRINAE), GENUS HIGHLY DIVERSIFIED IN THE NEOTROPICS BY DIANA CAROLINA ARIAS PENNA DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Entomology in the Graduate College of the University of Illinois at Urbana-Champaign, 2014 Urbana, Illinois Doctoral Committee: Professor James B. Whitfield, Chair, Director of Research Professor May R. Berenbaum Professor Sydney A. Cameron Dr. Marianne Alleyne Dr. Kevin P. Johnson ABSTRACT Among hymenopteran parasitoid wasps, Ichneumonoidea is one of the superfamilies with the highest number of species and includes the highly diverse Microgastrinae subfamily. Microgastrinae wasps are very abundant and can be collected in many different terrestrial habitats. A considerable number of species have been used in successful biological pest control programs, making it one of the most important insect groups. Glyptapanteles is one of the larger genera within Microgastrinae, which was segregated after several attempts to subdivide the gigantic genus Apanteles Foerster 1862. To date, 122 species have been described worldwide, of which only six are Neotropical, despite unpublished evidence that this genus is one of the largest in the Neotropics. Glyptapanteles are diminutive parasitoid wasps, which are free-living as adults, but as immatures, they attack exclusively larvae of Lepidoptera as a food resource for their developing larvae. These parasitoid wasps play a preponderant role in regulating their lepidopteran host populations and in maintaining high biological diversity in terrestrial ecosystems. A reliable revision for the Neotropics has not yet been attempted and many Glyptapanteles species remain undescribed. The scarcity of both taxon sampling and biological information is no longer standard for some Neotropical groups of insects. In the case of Glyptapanteles, the increasing accumulation of information, during the last four decades, derives from two independent long-term rearing projects: the caterpillar and parasitoid inventory of the Área de Conservación en Guanacaste (ACG) in Northwestern Costa Rica and the project Caterpillars and Parasitoids of the Eastern Andes (CAPEA) in Ecuador. This massive microgastrine material is available in Dr. James Whitfield’s laboratory at the University of Illinois, Urbana-Champaign (UIUC) and was the fundamental for my research. Chapter 1 is focused on the first taxonomic revision of Neotropical Glyptapanteles species from Costa Rica and Ecuador. Here, I describe 137 new species, 78 from Costa Rica and 59 from Ecuador. The taxonomic revision includes an extensive morphological image library for each of the species described and consists of about 2,331 high-resolution images which were used to create 223 plates. The pictures were obtained by both scanning electron microscope (SEM) and Z-stacked images merging different focus positions. The reference collection for this study comprises a total of 16,663 specimens, of which 13,540 are preserved in 100% ethanol and 3,123 are point mounted. Most of the species described (91 spp.) are completely gregarious while 28 ii are exclusively solitary, nine species exhibited both solitary and gregarious lifestyles and the remaining nine species were collected by Malaise traps. Three different sets of data (morphology, host records and DNA barcoding) were integrated in order to generate accurate boundaries between species. In Chapter 2, the first Glyptapanteles phylogeny based on morphological and molecular data from fragments of four genes is presented. The genes include mitochondrial COI (cytochrome c oxidase subunit 1) and three nuclear genes: Alpha-spectrin; long-wavelength opsin (LW Rh) and wg (wingless). All the Costa Rican material had associated COI, sequences generated partly by the collaborators in the Biodiversity Institute of Ontario, University of Guelph, Canada and partly by the Keck Center, UIUC. In contrast, COI sequences for Ecuador material and all nuclear genes were generated at UIUC. Phylogeny estimation included maximum likelihood and Bayesian inference. The most well supported phylogenetic reconstruction revealed two discrete clades, and although support was low at basal nodes, relationships at intermediate and terminal nodes were resolved with high support. The majority of the parasitoid samples are endowed with information about their herbivore hosts as well as host plants, providing information across three trophic levels. Mapping this information onto the phylogeny revealed patterns of niche conservatism in one of the clades. It was revealed that host preferences of Glyptapanteles are concentrated primarily in exposed feeding Macrolepidoptera, although ancestrally they explored Microlepidoptera. iii ACKNOWLEDGMENTS I would like to give sincere gratitude to my advisor Dr. James B. Whitfield for believing in me, giving me the opportunity to come from Colombia to the United States and permitting me to be part of his Microgastrinae lab family. I am really indebted to him for his continued support and encouragement. I hope we can continue our collaboration as colleagues. To Dr. Michael J. Sharkey (Kentucky University, USA), Dr. Thomas Pape (Natural History Museum of Denmark) and Dr. Marc A.A. Pollet (Institute for the Promotion of Innovation through Science and Technology (IWT-Vlaanderen), Belgium) for taking the time to write on behalf of my graduate school application. I appreciate your support. To Dr. Josephine J. Rodriguez for her encouragement and guidance during my first days at the UIUC, and valuable input on my draft proposal. This research project would not have been possible without the support of many people. To Dr. Daniel Janzen, Dr. Winifred Hallwachs, and Dr. Lee Dyer, who provided tons of specimens which are the backbone of my dissertation. To Dr. Alexander L. Wild and Jaqueline M. O’Connor for their guidance and training during my first steps in molecular skills. A special thanks to my colleague Andrew H. Debevec who enlightened me during my technical difficulties running phylogenetics programs. I would like to give very special thanks to Brielle Fischman and Dr. Felipe Soto-Adames for their prompt collaboration and valuable assistance with alignment of sequences critical for my molecular analysis. I am thankful to Yali Zhang for her assistance in preparing wasps for dry collection during the initial steps of this project. To Scott J. Robinson, and Catherine L. Wallace from the microscopy suite, imaging technology group, Beckman Institute for their help in taking SEM images. To Dr. Andrew Suarez for giving me access to his laboratory equipment and allowing me to take the digital images. A special thanks goes to Kyle Parks, Dr. Sydney Cameron and all her lab members: Michelle Duennes, John Maddux, Charles Deans and those who exited some time ago searching for new challenges, Haw Chuan Lim and Jeff Lozier for their advice and useful comments to my proposal. iv To my friends and colleagues Tolu, Marsha, Juma, Ling-Hsiu, Doris, Mami, Sindu, Tania, Nathalie and Rafa who were my companions. People, you made me feel at home. I thank you for the moments I spent with each of you. I am grateful to all of my family for their endless support. My mom, Amanda Penna, my sisters Tania Arias and Sofía Arias as well as my brother-in-law Thibaut Delsinne. One special and deepest thanks to my husband, Peter Marz, who accepted to be my travel companion in this long voyage, for his unconditional support, patience and taking care of me during the most critical stages of my research. Also, to my son Andrés, for bringing great joy and happiness to our lives. I would like to thank members of my dissertation committee, professors from the Entomology department and graduate students who contributed to my academic development, learning opportunities and life experience. v TABLE OF CONTENTS CHAPTER 1: A TAXONOMIC REVISION OF THE GLYPTAPANTELES SPECIES (HYMENOPTERA: BRACONIDAE, MICROGASTRINAE) WITH EMPHASIS UPON REARED MATERIAL FROM COSTA RICA AND ECUADOR……………………………… 1 Abstract …………………………………………………………………...……..……………1 Introduction……………………………………………………………………..……………. 2 Materials and Methods……………………………………………………..…………..….…. 6 Results…………………………………………..……………………………………………12 Acknowledgments……………….……..…………….……..…………….………….……. 516 References……………….……..…………….……..…………….……………….………. 518 CHAPTER 2: MOLECULAR PHYLOGENY OF GLYPTAPANTELES (HYMENOPTERA: BRACONIDAE, MICROGASTRINAE) AND HERBIVORE HOST USE IN A SPECIES-RICH NEOTROPICAL GROUP OF PARASITOID WASPS ……………………………………… 529 Abstract …………….……………….…………………………………..……………….…529 Introduction……………….……………….…………………………………..……………529 Materials and Methods ……………….……………………………………….…..….…… 534 Results………….……………………………………………………..………………..….. 541 Conclusions ……………………………………………………..….…………….……..… 550 Acknowledgments ……………………………………………………..………………..… 552 References ………………………………...………………..…..…………….…………… 553 APPENDIX A: MATERIAL EXAMINED …………………………………………..……… 561 APPENDIX B: FIGURES……………………………………………………………..……… 562 APPENDIX C: HOLOTYPES …………………………………………………...…………… 563 APPENDIX D: PARASITOIDS, HERBIVORES AND PLANT HOSTS …………..………. 564 vi APPENDIX E: CYTOCHROME OXIDASE I, (COI) FROM COSTA RICA AND ECUADOR …………………………………………………………………………………………………. 565 APPENDIX F: MORPHOLOGICAL CHARACTER LIST OF GLYPTAPANTELES ………. 566 APPENDIX G: GLYPTAPANTELES DNA EXTRACTION …………………..…………….. 567 APPENDIX H: MOLECULAR DATASETS…………………………………………..……. 568 vii CHAPTER 1 A Taxonomic Revision of
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