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Phylogeny and Host Relationships of the Australian Gall-Inducing Fly Fergusonina Malloch (Diptera: Fergusoninidae)

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Phylogeny and Host Relationships of the Australian Gall-Inducing Fly Fergusonina Malloch (Diptera: Fergusoninidae) Phylogeny and host relationships of the Australian gall-inducing fly Fergusonina Malloch (Diptera: Fergusoninidae) Michaela Fay Elizabeth Purcell December 2017 A thesis submitted for the degree of Doctor of Philosophy of the Australian National University © Copyright by Michaela Fay Elizabeth Purcell 2017 All Rights Reserved. DECLARATION I, Michaela Fay Elizabeth Purcell, declare that this thesis is my own original work, except for the Eucalyptus phylogenies in Chapter 3 contributed by Andrew H. Thornhill. This thesis has not been submitted for consideration at any other academic institution. Michaela Fay Elizabeth Purcell December 2017 Word count: 32,178 i ACKNOWLEDGEMENTS First and foremost, of course, my greatest thanks go to my supervisors, David Yeates and Dave Rowell, who provided encouragement, patience, support, laughs, time, advice, kindness and wisdom throughout my project with unstinting good humour. I always knew they had my back. It was David Yeates who introduced me to the many unsolved mysteries of the Fergusonina/ Fergusobia system when I was looking for a special topics project as an undergraduate, igniting my curiosity and affection for this small, strange, gall-dwelling fly. Dave Rowell, as well as assiduously checking to ensure I was happy, making progress and travelling in the right direction, employed me when my scholarship ran out, which not only prevented starvation but also give me the chance to explore the habits of other animals such as spiders, scorpions, velvet worms and invertebrate zoology students. Together, with their varied areas of experience, interest and expertise, the two Davids offered a very special supervisory combination, and I hope they know how much I appreciate their guidance. It’s impossible to give enough thanks to my friend and stalwart companion in adventure Thomas Wallenius, whose unflagging enthusiasm, hard work and genuine interest in the project turned gall collecting outings into hilarious and joyous expeditions. His contribution in the field was invaluable and his gall finding skills unparalleled, and I know this project would have been much harder and a lot less fun without him. An unexpected bonus of this project was developing a great appreciation and fondness for the eucalypts, frustrating as they can be. Thanks to everyone who provided ii generous help with plant identifications or offered useful information about host plants and gall hunting sites: Doug Benson, Max Beukers, Meredith Cosgrove, Penny Mills, Andrew Thornhill, and particularly Mike Crisp. Very special thanks are due to Leigh Nelson, who took me up Black Mountain on my first gall-hunting trip and cheerfully provided a great deal of help when I was a Fergusonina novice, and to Andreas Zwick, Diane Hartley and Bruce Halliday for giving up their time to offer practical help and expert advice. Heartfelt thanks (and apologies) to my dear son Ciaran for coping with flies in the fridge, despite the fact that he really hates flies, and to Sean Hannigan for pulling up stakes and moving to Canberra so I could do this thing, which he never doubted that I was capable of. Thanks, of course, to my fellow dipterist PhD students Xuankun Li and James Lumbers, being two of the few people I know who could sympathise with the consternation that can be caused by fly hairs, and to the lovely fellow researchers who welcomed me warmly into the arcane world of Fergusonina and Fergusobia: Kerrie Davies, Jeff Makinson, Gary Taylor, and the other MF Purcell, Matt. The MicroCT imaging was achieved thanks to Paul Cooper the ANU Research School of Biology, and Holger Averdunk, Tim Senden and Michael Turner, from the Research School of Physics & Engineering. Dr Ajay Limaye, VizLab, ANU Supercomputer Facility (ANUSF) compiled the raw data into beautiful 3D images using Drishti. iii Finally, thanks to everyone who ever came scouring the scrub for galls with me, or presented me with a lump on a stick and asked “is this one of yours?”: Keith Bayless, Max Beukers, Sarah Buchan, Bokyung Choi, David Coates, Lyn Cook, Jack Couch, Mike Crisp, Roger Farrow, Penny Gullan, Colin Handley, Carsten Kulheim, Andrew Leo, Bryan Lessard, Xuankun Li, James Lumbers, Penny Mills, Susanne Moor, Leigh Nelson, Sandra Schachat, Andrew Thornhill, Marco Wallenius and Mark Wong. This research was facilitated by funding from the Schlinger Trust endowment to the Australian National Insect Collection, and was supported by an Australian Government Research Training Program (RTP) Scholarship. iv ABSTRACT Fergusoninidae is a monogeneric family of mainly Australian flies. In a unique obligate mutualism with a nematode, these flies induce galls on plants in the family Myrtaceae, and have been recorded on seven genera of host plants, most commonly on the eucalypts. Most host plants are associated with multiple species of Fergusonina, usually galling different sites on the plant. Despite the abundance and diversity of Fergusoninidae and its tight association with Australia’s most iconic flora, the host specificity and coevolutionary relationships of Fergusonina with its plant hosts have not previously been examined in depth. I used a phylogenetic approach based on mitochondrial COI to examine the evolutionary relationships between Fergusonina species and their plant hosts, initially performing a Bayesian analysis of 41 putative species on flies from Eucalyptus plant hosts. This analysis revealed well-supported lineages of flies characterised by larval morphology and gall type, usually from the same plant host subgenus. The deeper phylogenetic relationships between groups of species remained unclear, so I performed a further analysis of an expanded dataset including flies from four host genera, using separate and concatenated COI and nuclear CAD sequences. Having disparate evolutionary time scales, Fergusonina and their hosts cannot have codiverged early in the history of Myrtaceae, but current fly-plant host specificity suggested that there may be cospeciation at finer taxonomic levels. A fine-scale analysis of v flies collected from a clade of ten Eucalyptus species explored the plant-fly coevolutionary relationships in three clades of flies from different sites of the host plant: flower buds, leaf blades and vegetative shoot buds. The degree of host specificity displayed by the three fly groups varied markedly, with flower bud gallers exhibiting the most cophylogenetic history, and leaf blade gallers the least. These results suggest that host switching occurred often in the history of Fergusonina and Myrtaceae. I compared molecular, morphological and ecological criteria for determining species limits, including a number of molecular species delimitation models. Delimiting species using a 2% pairwise distance was most consistent with other data such as larval and adult morphology, host and gall site. However, molecular methods were not adequate to clarify some ambiguous species limits, highlighting the need to integrate multiple criteria when identifying species in this group. Over the course of the study, I discovered around 95 unrecorded host plant/gall site associations, indicating that the potential number of species in this family is very large. The definable morphological and ecological differences among the lineages of Fergusonina, supported by molecular evidence, argue for a revision of the genus along these lines. The type species for Fergusonina, collected in Sydney in 1924, is in poor condition and is not identifiable; there are no records of its host, gall type or larval morphology, and I could not extract and DNA from it. A neotype will need to replace the existing holotype, or the type species assigned to a probable group. After a comparison of morphological characters I concluded that the type species is likely to belong to a group associated with the host genus Corymbia. vi TABLE OF CONTENTS Declaration…………………………………………………………………………………………………..……………………………….i Acknowledgements………………………………………………………………………………………………………………………ii Abstract………………………………………………………………………………………………………………………………………..v Table of contents…………………………………………………………………………………..……………………………………vii List of tables…………………………………………………………………………….……………………………………………………x List of figures……………………………………………………………………………………………………………………………….xi Chapter 1: General introduction ......................................................................................................... 1 1.1 Overview of Fergusoninidae ...................................................................................................... 1 1.2 Aims……………………………………………………………………………………………………………………………………..1 1.3 The Fergusonina/Fergusobia system ......................................................................................... 3 1.3.1 Taxonomy, morphology and diversity……………………………………………………………………….4 1.3.2 Fergusonina life cycle………………………………………………………………………………………...…....6 1.3.3 Gall initiation……………………………………………………………………………………….……….…………10 1.3.4 Gall types…………………………………………………………………………………..……………………………11 1.3.5 Fergusobia life cycle…………………………………………………………………….………………………….12 1.3.6 Natural enemies……………………………………………………………………………………………………..14 1.4 Materials and methods – collection of specimens………………………………………………………………16 1.5 Publication of chapters from this thesis………………………………………………………………………………17 Chapter 2: Relationship between larval dorsal shield morphology and gall type .......................... 18 2.1 Abstract .................................................................................................................................... 18 2.2 Introduction………………………………………………………………………………………………………………………..18
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