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EMJ Dissertation 2010 Final Good THE EVOLUTIONARY ECOLOGY OF AN INSECT-FUNGUS INTERACTION: BOTRYOSPHAERIA DOTHIDEA , SYMBIOTIC WITH THE GOLDENROD-GALLING MIDGE ASTEROMYIA CARBONIFERA (DIPTERA: CECIDOMYIIDAE) By Eric Michael Janson Dissertation Submitted to the Faculty of the Graduate School of Vanderbilt University in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSPHY in Biological Sciences August, 2010 Nashville, Tennessee Approved: Professor Patrick Abbot Professor Daniel J. Funk Professor David E. McCauley Professor John O. Stireman III To my family, Michael, Carol, and Erin Janson. I will never be able to thank you enough. ii ACKNOWLEDGEMENTS They say that science is a collaborative pursuit, and in coming to the end of my current journey, I fully understand why. This dissertation (and various side projects) could not have been completed without the intellectual, logistical, and emotional support from friends, colleagues, and friendly colleagues. Foremost among them include Betsy Arnold, Spence Behmer, Chris Brown, Vikram Chhatre, Hilary Devlin, Dan Duran, Jennifer Mandel, Scott Egan, Dan Funk, John Gibbons, Bob Grebenok, Jeremy Heath, Jessica Mezzanote, Emily Peeden, Antonis Rokas, John Stireman, and Mike Singer. All of you gave of yourselves and I am better scientist, and person, because of it. You have my deepest gratitude and I hope to repay you in time. I would like to give special thanks to Cris Hochwender. You saw something in me that I doubt I would have ever seen in myself. I don’t know that any of this would have happened without your support and guidance. The most supportive one of all, though, despite my best attempts to drive her insane, is Kathryn Haley. When the going got tough, she told me to get going and I will never be able to thank her enough. I love you, Kate. I thank Dave McCauley for being a patient, understanding, and fair committee chair, and a scientific role model. I would like to give special thanks to my academic advisor, Patrick Abbot. The road was rocky, but you kept me on the path. You taught me some important lessons about myself, the less glamorous aspects of modern science, and helped solidify my scientific philosophies. And finally, to those not mentioned here: you are not forgotten. This dissertation was supported by National Science Foundation grant DEB 0614433 and Vanderbilt University. “We might not be the best people...” - Jack Donaghy “But we're not the worst...” - Liz Lemon “Graduate students are the worst.” - Liz and Jack in unison -30 Rock, National Broadcasting Company- iii TABLE OF CONTENTS Page DEDICATION………………………………………………………………………... ii ACKNOWLEDGEMENTS………………………………………………………….. iii LIST OF TABLES………………………………………………………………….... vii LIST OF FIGURES………………………………………………………………….. ix Chapter I. INTRODUCTION…………………………………………………..... 1 II. PHYTOPHAGOUS INSECT-MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION.............................................. 11 Abstract.................................................................................................... 12 Introduction............................................................................................. 13 Prevalence of phytophagous insect–microbe mutualisms and the benefits conferred by microbial mutualists to their insect hosts........................... 15 Impact of microbial mutualists on adaptive evolutionary diversification in phytophagous insects............................................................................... 18 Modification of ecological opportunity by microbial mutualists: facilitative and inhibitory effects on diversification................... 21 Facilitative effects: environmental buffering through microbial mutualists........................................................ 21 Facilitative effects: reduction of insect genetic constraints by microbial mutualists................................................... 26 Inhibitory effects: microbial mutualist imposed limits on ecological opportunity..................................................... 28 Modification of host plant-associated natural selection by microbial mutualists: facilitative and inhibitory effects on diversification.............................................................................. 29 Facilitative effects: microbial mutualist promotion of host-plant specialization.................................................. 29 Inhibitory effects: reduction in host plant (ecological) specialization through microbial mutualists................... 34 Insect–microbe mutualisms in a tri-trophic context: facilitative and inhibitory effects on diversification............................................. 35 Conclusions and future directions........................................................... 38 iv Acknowledgements................................................................................. 41 III. SAME HOST-PLANT, DIFFERENT STEROLS: VARIATION IN STEROL METABOLISM IN AN INSECT HERBIVORE COMMUNITY….... 42 Abtract………………………………………………………………. 43 Introduction…………………………………………………………... 45 Medthods and Materials…………………………………………….... 50 Collection sites……………………………………………….. 50 Study taxa…………………………………………………...... 51 The plant……………………………………………..... 51 The insects…………………………………………..... 51 The fungus…………………………………………..... 54 Tissue collection for sterol analysis………………………...... 54 Sterol extraction and analysis………………………………... 56 Results………………………………………………………………... 60 Solidago leaf sterol profile………………………………….... 60 Externally feeding insects’ sterol profiles…………………..... 60 Fungus sterol profile.................................................................... 64 Internally feeding insects’ sterol profiles.................................... 66 Discussion................................................................................................ 66 Acknowledgements.................................................................................. 73 IV. EVOLUTIONARY PATTERNS IN THE FUNGAL ECTOSYMBIONT OF THE GOLDENROD GALL MIDGE ASTEROMYIA CARBONIFERA (DIPTERA: CECIDOMYIIDAE) REVEALS SYMBIONT-MEDIATED PHENOTYPIC VARIATION WITHOUT COEVOLUTION……………………….... 75 Abstract……………………………………………………………..... 76 Introduction…………………………………………………………... 77 Methods and Materials……………………………………………….. 80 Study organism……………………………………………...... 81 Fungus isolation……………………………………................. 83 Genomic DNA extraction and amplification fot cloning and sequencing AFLPs……….......................................................... 85 Phylogenetic reconstruction and analysis of DNA sequence data……………………………………….................................. 86 Genomic DNA extraction and amplification for AFLP analysis....................................................................................... 89 Amplified fragment length polymorphism AFLP genotyping and analysis.................................................................................. 90 Culture-based assays.................................................................... 92 Results………………………………………………………………... 93 Fungal identity, phylogenetic reconstruction, and other evolutionary metrics.................................................................... 93 v AFLP population genetics and phylogenetics………............... 102 Culture-based assays……………………………….................. 107 Discussion…………………………………………………………..... 110 Botryosphaeria dothidea as a source of phenotypic variation and its influence on evolutionary divergence for Asteromyia carbonifera …………………………………………………... 111 Implications for the evolution of gall midge-fungus associations…………………………………………………... 112 Comparisons to other microbial symbioses................................ 117 Acknowledgements…………………………………………………... 119 V. CONCLUSIONS……………………………………………………... 120 REFERENCES……………………………………………………………………...... 127 vi LIST OF TABLES Table Page 1. Identity and the relatitive percentages of sterols detected in the leaf tissue of Solidago altissima ………………………………………………………....... 61 2. Identity and relative percentages of sterols detected in externally feeding insects collected on Solidago altissima ………………………………………………. 62 3. Identity and relative percentages of sterols detected in two internally feeding insects and one insect-associated fungal symbiont collected on Solidago altissima … 65 4. List of fungi isolated from Asteromyia carbonifera galls or detected through culture independent methods and their frequency of isolation………………………. 94 5. Mean percent nucleotide composition of four nuclear loci for non-insect associated and Asteromyia carbonifera -symbiotic isolates of Botryosphaeria dothidea ……………………………………………………………………………… 99 6. Results of Tajima’s relative rate test for three sequences for various gall midge-symbiotic, lichen symbiotic, and non-insect symbiotic fungal isolates…………………………..................................................................................... 100 7. Pairwise F ST and Nei’s genetic distances for Botryosphaera dothidea isolates of the four known gall morphs of Asteromyia carbonifera ………………………….. 104 8. Summary of analysis of molecular variance (AMOVA) of amplified fragment length polymorphisms (AFLPs) based on Euclidian genetic distances for Asteromyia -symbiotic Botryosphaeria dothidea ……………………………………………………………... 105 9. Summary of index of association tests for asexuality for Asteromyia carbonifera - symbiotic Botryosphaeria dothidea ………………………………………………….. 106 vii 10. Pairwise correlations of growth rates for individual Botryosphaeria dothidea isolates across different growth rate experiments…………………………………………….. 108 viii LIST
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