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An Investigation of the Chemical and Visual Cues That Mediate Mate Recognition in Blowflies (Diptera: Calliphoridae)

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An Investigation of the Chemical and Visual Cues That Mediate Mate Recognition in Blowflies (Diptera: Calliphoridae) University of Wollongong Research Online University of Wollongong Thesis Collection 2017+ University of Wollongong Thesis Collections 2020 Love at first flight: an investigation of the chemical and visual cues that mediate mate recognition in blowflies (Diptera: Calliphoridae) Nathan Butterworth University of Wollongong Follow this and additional works at: https://ro.uow.edu.au/theses1 University of Wollongong Copyright Warning You may print or download ONE copy of this document for the purpose of your own research or study. The University does not authorise you to copy, communicate or otherwise make available electronically to any other person any copyright material contained on this site. You are reminded of the following: This work is copyright. Apart from any use permitted under the Copyright Act 1968, no part of this work may be reproduced by any process, nor may any other exclusive right be exercised, without the permission of the author. Copyright owners are entitled to take legal action against persons who infringe their copyright. A reproduction of material that is protected by copyright may be a copyright infringement. A court may impose penalties and award damages in relation to offences and infringements relating to copyright material. Higher penalties may apply, and higher damages may be awarded, for offences and infringements involving the conversion of material into digital or electronic form. Unless otherwise indicated, the views expressed in this thesis are those of the author and do not necessarily represent the views of the University of Wollongong. Recommended Citation Butterworth, Nathan, Love at first flight: an investigation of the chemical and visual cues that mediate mate recognition in blowflies (Diptera: Calliphoridae), Doctor of Philosophy thesis, School of Earth, Atmospheric and Life Sciences, University of Wollongong, 2020. https://ro.uow.edu.au/theses1/850 Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] Love at first flight: an investigation of the chemical and visual cues that mediate mate recognition in blowflies (Diptera: Calliphoridae) Nathan Butterworth Supervisors: Professor James F. Wallman Associate Professor Phillip G. Byrne Professor Paul A. Keller This thesis is presented as part of the requirement for the conferral of the degree: Doctor of Philosophy This research has been conducted with the support of the Australian Government Research Training Program Scholarship. University of Wollongong School of Earth, Atmospheric and Life Sciences 21st February 2020 Abstract Sex is widespread throughout the animal kingdom and has undoubtedly played a crucial role in shaping the exceptional diversity of life on Earth. This must be particularly true in the insects, which are the most diverse group of animals and exhibit an astounding array of sexual adaptations. Despite this, sexual behaviour has been studied in less than 1% of species, and our understanding of the role that sexual selection has played in insect speciation is limited. The blowflies (Diptera: Calliphoridae) are some of the most commonly encountered insects, and like many insect taxa, almost nothing is known of their mating behavior. Several species show sexual dimorphisms in eye morphology, so it has been assumed that visual cues such as movement are the primary means by which blowflies recognise mates. However, there is limited evidence to support this. In addition, although chemical cues are almost universally important in insect communication, their role in blowflies has been overlooked. As such, our current understanding of blowfly sexual signaling is superficial, and the extent to which sexual selection has contributed to the evolution of blowflies is entirely unclear. To deepen our understanding of how sexual selection has shaped blowfly diversity, this thesis aims to identify some of the sexual signals that may facilitate mate recognition in blowflies. Using the ecologically diverse blowfly genus Chrysomya, I focus on two traits that are widespread in insects and commonly involved in sexual communication: cuticular hydrocarbons (CHCs) and wing interference patterns (WIPs). I aim to highlight how these traits vary between species, sexes, and life stages, with the broader goal of elucidating their potential to act as signals of mate-compatibility in blowflies. First, I use the widespread Australian species Chrysomya varipes to assess whether CHCs are sex-specific signals and facilitate sexual attraction (Chapter 2). Using the same species, I also explore whether CHCs change over the life span of blowflies and function as signals of sexual maturity (Chapter 3). I then use Australian representatives of the genus Chrysomya to examine the evolutionary patterns of CHC and WIP diversification in the context of sexual selection (Chapters 4 and 5). Finally, I provide a detailed documentation of the mating behaviour of Chrysomya flavifrons in order to highlight how these traits may function in a multimodal context (Chapter 6). i Overall, I demonstrate that both CHCs and WIPs are sexually dimorphic in several species, and have diverged rapidly between species, suggesting that they have likely played key roles as signals of mate-compatibility in many blowfly species. I then highlight that CHCs are sex- specific and may act as key signals of sexual maturity in Ch. varipes. Lastly, in documenting the complex male courtship display of Chrysomya flavifrons, I demonstrate that blowfly mating behaviour is highly variable, and that blowflies produce and receive a complex suite of multimodal signals during mating. Taken together, these findings 1) highlight the diversity of sexual signaling in Chrysomya blowflies, 2) highlight the key role sexual selection has likely played in blowfly diversification, and 3) advance the notion that multimodal signalling is widespread among insects. ii iii Acknowledgments I would like to extend a huge thank you to my supervisors James, Phil, and Paul. James, five years ago you took me on as an undergraduate student, at which point in time I had no idea what career path I wanted to take. From that point onwards, you have been endlessly supportive in both an academic and personal sense and have given me the opportunity to develop as a scientist, and to start building my own career. Most importantly, you have sparked my interest in insects, which will be a life-long passion. I am in constant admiration of the beauty and majesty of these tiny animals, and they have been a source of great inspiration and enlightenment. I must thank you for this, and for being such a fantastic teacher and mentor. I truly cannot express the extent of my gratitude. Phil, thanks to you I have developed a crippling addiction to evolutionary biology. I was once a young man who enjoyed a simple life, filled with hopes and dreams. Now, I spend my days huddled in a dusty office, obsessively ruminating on the sexual exploits of insects. At least I can say that while guiding me down this dark path, you have been a fantastic teacher and mentor. Your guidance has consistently inspired me and has improved the way I communicate science and how I contemplate evolution. I would often visit your office to query experiments or to discuss ideas – and you always found the time to give advice and encouragement, which never failed to lift my spirits and gave me the confidence to keep going. Paul, without your help this project would have been impossible. You helped secure access to a world-class GC-MS instrument which cut the time needed for sample analysis in half. You have always been swift to provide guidance and feedback and have an uncanny ability to pick out tautologies in my writing, and to notice repetitive sentences that manage to slip by. I am hugely grateful for all the time and help you have provided. To Roslyn and Martin, I couldn’t ask for better or more supportive parents. You have always encouraged me to do what I love and have supported me along the way. I’m not sure where you went wrong to raise a son who watches flies have sex for a career - but thank you for everything you have done to help me get here. A huge thank you to all my lab colleagues. Firstly, to Tracey who has been a huge help with experiments, consumables, and cataloguing. Having you as part of the lab has been a massive iv help to all of us and we will miss having you around! Huge thankyou to everyone in the EARL lab for all your support, especially Emma and Shannon – the intense guilt I felt for never presenting anything at our writing workshops forced me to finish and publish my 6th chapter early last year! Finally, Blake. You have been a constant source of inspiration. Watching you develop from a young, naïve, undergraduate student into a young, naïve, PhD student has been a sight to behold. Thank you for the many discussions we have had, and for always reminding me of my shortcomings. Nikolas. They say that only the dead have seen the end of war. Having endured you for the last five years, and upon the realisation that I will be stuck with you again in 2020, I feel the weight of this truth. From the horrific Jatz debacle of 2016, to the great ‘Canberra road trip’ betrayal, the chilling battle of the house plant, and the harrowing ‘Attack of the Almonds’ in 2019 – you have been a constant source of torment. Nevertheless, I must thank you – the unbearable pain you have brought into my life has consistently motivated me to work harder and become a better scientist. Despite it all, we have remained great friends, and I genuinely hope we can continue to annoy each other for the rest of our careers. I’d also like to thank Megan - you have supported me throughout my entire PhD for which I am endlessly grateful.
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