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Assessing the Drivers of Adaptive Radiation in a Complex of Gall Midges: a Multitrophic Perspective on Ecological Speciation

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Assessing the Drivers of Adaptive Radiation in a Complex of Gall Midges: a Multitrophic Perspective on Ecological Speciation ASSESSING THE DRIVERS OF ADAPTIVE RADIATION IN A COMPLEX OF GALL MIDGES: A MULTITROPHIC PERSPECTIVE ON ECOLOGICAL SPECIATION A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy By Jeremy J. Heath M.S. Entomology, Ohio State University, 2001 B.S.(H) Environmental Science, Acadia University, 1996 ____________________________________________ 2012 Wright State University COPYRIGHT BY JEREMY J. HEATH 2012 WRIGHT STATE UNIVERSITY GRADUATE SCHOOL 12 December 2012 I HEREBY RECOMMEND THAT THE DISSERTATION PREPARED UNDER MY SUPERVISION BY Jeremy J. Heath ENTITLED Assessing the drivers of adaptive radiation in a complex of gall midges: A multitrophic perspective on ecological speciation BE ACCEPTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF Doctor of Philosophy. ______________________________ John O. Stireman III, Ph.D. Dissertation Director Associate Professor, Environmental Sciences Ph.D. Program ______________________________ Don Cipollini, Ph.D. Director, Environmental Sciences Ph.D. Program ______________________________ Andrew Hsu, Ph.D. Dean, Graduate School Committee on final examination ______________________________ John O. Stireman III, Ph.D. ______________________________ Don Cipollini, Ph.D. ______________________________ Tom Rooney, Ph.D. ______________________________ Thaddeus Tarpey, Ph.D. ______________________________ P. Douglas Abbot, Ph.D. ABSTRACT Heath, Jeremy J. Ph.D. Environmental Sciences Ph.D. Program, Wright State University, 2012. Assessing the drivers of adaptive radiation in a complex of gall midges: A multitrophic perspective on ecological speciation. Natural enemies as selective forces maintaining and shaping morphological, physiological, and behavioral divergence in adaptive radiations have received very little attention. Until recently, the focus has been on primary resource competition as a major driver of trait divergence in adaptive radiations. Here I consider the role of natural enemies specifically in driving trait divergence in a complex of gall midges in the nominal species Asteromyia carbonifera (Diptera: Cecidomyiidae), which appears to be in the throes of an incipient adaptive radiation on its host plant, goldenrod (Solidago). This galler uses a symbiotic fungus (Botryosphaeria dothidae) as a food source and as the major structural component of its gall. Use of this symbiont may be the key innovation that allowed colonization of its host plant and began the process of adaptive radiation in this system. Overall, I find strong evidence that the extended phenotype of these gall midges (i.e., the gall) is experiencing stabilizing, directional, and diversifying selection imposed by natural enemies. I also find that natural enemies appear to be driving divergence in an ovipositional phenotype that may represent a major split in the evolution of these lineages. Furthermore, sequestration or de novo biosynthesis of carotenoids by these midges may provide the precursors that allow gall proliferation, but may also be costly because of the potential attraction of natural enemies. Finally, I find that the host plant has little effect on gall traits, but host plant defenses (e.g., sesquiterpenoids) may limit the general density of galling insects. I conclude that divergence in gall iv morphology and ovipositional behaviors are, at least in part, determined by natural selection imposed by natural enemies and that these forces may help explain the diversity of gall morphologies and habits found in nature. v TABLE OF CONTENTS 1 Introduction ................................................................................................................. 1 1.1 Adaptive radiation and ecological speciation....................................................... 1 1.2 The study system .................................................................................................. 6 1.3 Outline and objectives .......................................................................................... 9 1.4 References .......................................................................................................... 11 2 Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea ..................................................................... 17 2.1 Abstract .............................................................................................................. 17 2.2 Introduction ........................................................................................................ 18 2.2.1 Study system ............................................................................................... 20 2.3 Materials and methods ....................................................................................... 21 2.3.1 Biology and life history traits ..................................................................... 21 2.3.2 Nature of the midge-fungus interaction ...................................................... 22 2.3.3 Asteromyia eclosion behaviour ................................................................... 25 2.3.4 Conidia morphology ................................................................................... 25 2.3.5 Gall initiation in field plots ......................................................................... 26 2.3.6 Gall initiation in screen tents ...................................................................... 28 2.4 Results ................................................................................................................ 29 2.4.1 Biology and life history .............................................................................. 29 2.4.2 Asteromyia-fungus interdependency ........................................................... 31 2.4.3 Adult behaviour .......................................................................................... 32 2.4.4 Fungal acquisition and gall initiation .......................................................... 33 2.5 Discussion .......................................................................................................... 34 vi 2.5.1 Time required for appearance of fungus ..................................................... 34 2.5.2 The nature of the Asteromyia-Botryosphaeria symbiosis ........................... 35 2.5.3 Gall initiation, conidia collection, and eclosion behaviour ......................... 37 2.6 References .......................................................................................................... 42 3 Carnivores and carotenoids are associated with an adaptive behavioural phenotype in a radiation of gall midges. ................................................................................................. 59 3.1 Abstract .............................................................................................................. 59 3.2 Introduction ........................................................................................................ 60 3.2.1 System background ..................................................................................... 61 3.2.2 Within-host preference and performance .................................................... 62 3.2.3 Variation in carotenoids among gall morphs and its consequences ........... 63 3.3 Materials and Methods ....................................................................................... 65 3.3.1 Testing for differences in ovipositional phenotype .................................... 65 3.3.2 Assessing variation in parasitoid attack ...................................................... 67 3.3.3 Testing suitability of the oviposition site .................................................... 68 3.3.4 Characterizing carotenoid profiles in accessory glands .............................. 69 3.3.5 Associating carotenoid quantity and parasitoid attack ................................ 70 3.3.6 Determining the presence of abscisic acid in the salivary glands ............... 70 3.4 Results ................................................................................................................ 72 3.4.1 Ovipositional phenotype ............................................................................. 72 3.4.2 Parasitoid attack .......................................................................................... 73 3.4.3 Egg transplants and crescent failure rates ................................................... 73 3.4.4 Carotenoid profiles...................................................................................... 74 3.4.5 Relationship between carotenoids and Platygaster attack .......................... 74 3.4.6 ABA in the SGs .......................................................................................... 75 vii 3.5 Discussion .......................................................................................................... 75 3.6 Conclusions ........................................................................................................ 79 3.7 References .......................................................................................................... 81 4 The role of carotenoids and their derivatives in mediating interactions between insects and their environment ......................................................................................... 102 4.1 Abstract ............................................................................................................ 102
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