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THE PHYSIOLOGY AND ECOLOGY OF DIAPAUSE UNDER PRESENT AND FUTURE CLIMATE CONDITIONS IN THE BLOW FLY, CALLIPHORA VICINA By Paul C Coleman A thesis submitted to The University of Birmingham For the degree of DOCTOR OF PHILOSOPHY School of Biosciences College of Life and Environmental Sciences University of Birmingham June 2014 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Abstract __________________________________________________ Virtually all temperate insects overwinter in diapause, a pre-emptive response to adverse environmental conditions and for many species a pre-requisite of winter survival. Increased global temperatures have the potential to disrupt the induction and maintenance of diapause. In the first part of this thesis, a four year phenological study of the blow fly, Calliphora vicina, identifies that diapause is already being delayed due to high temperatures experienced by larvae within the soil layer. Laboratory studies identified that non-diapause life stages are capable of heightening cold tolerance through a rapid cold hardening ability, and winter acclimated adults maintain locomotion at lower temperatures than summer acclimated adults. A previously unrecognised threat, however, is that higher adult temperatures have the transgenerational effect of reducing the cold tolerance of diapausing progeny. In the second part of this thesis, the relationship between diapause and cold hardiness was investigated. The amino acid, alanine, was up-regulated as part of the diapause programme. Non-diapause larvae developed on an alanine augmented-diet expressed cold tolerance phenotypes similar to those of their diapausing counterparts. This adds to a growing body of evidence to suggest that amino acids have a direct role in insect cold tolerance. i Acknowledgements __________________________________________________ First, I would like to thank my supervisors Professor Jeff Bale and Dr Scott Hayward for providing me with an opportunity to undertake a PhD at the University of Birmingham. I am particularly grateful to Scott, for his continued advice and for providing me with the flexibility to focus on areas which I have found most interesting, while always pointing me in the right direction. Secondly, I am extremely grateful to all members of the Arthropod Ecophysiology Research Group for such an amazing four years. I would like to thank Gwen and Lucy for their willingness to answer naïve questions and provide helpful tips at the start of the PhD. Megan, I am extremely glad that we started the PhD at the same time and have thoroughly enjoyed making it to the end together. Thank you to Ji for all the delicious Thai food and for her good company while in South Korea. Matt (I have no idea how you finished your PhD first!) I will never forget our epic bike ride up the snow covered mountain to Finse station (1,222m), well done us! Thank you to Emily, the hours spent pestering you helped ease the stress of the PhD and it was a delight explaining rapid cold hardening to you, on numerous occasions. Nicky, you were a late entrant to the lab group but you made the whole experience more enjoyable. Particular thanks to Bobbie, who provided excellent company while in the lab, some assistance and help in experiments and lots of immortal wisdom, such as “you only know once you know”. Thank you also to Emma. Meeting you was an unexpected bonus of the PhD, you have provided help and support in every imaginable way, most importantly in the form of several hot meals in the final weeks of writing up. Finally, I would like to thank my parents who have encouraged me in the decisions that I have made, provided me with both financial and emotional support during my many years in higher education and have spent countless hours lugging my belongings between universities. I can’t thank you both enough. ii List of publications __________________________________________________ Chapter 2 Coleman, P.C., Bale, J.S., Hayward S.A.L. (2014) Cross generation plasticity in cold hardiness is associated with diapause, but not the non-diapause developmental pathway, in the blow fly, Calliphora vicina. Journal of Experimental Biology 217, 1454 – 1461. iii Declaration of Author’s contribution __________________________________________________ Contributions made by: Paul Coleman (PCC), Scott Hayward (SH) and Jeff Bale (JB) Chapter 1: Entirely my own work Chapter 2: PC designed the experiment, with input from SH. PC collected the data, analysed the data and wrote the chapter. SH assisted with the discussion and analysis of data and SH and JB assisted with the writing of the manuscript. Chapter 3: PC designed the experiment, with input from SH. PC collected the data, analysed the data and wrote the chapter. SH assisted with the discussion and analysis of data and SH has assisted with writing of the manuscript. Chapter 4: PC designed the experiment, with input from SH. PC collected the data, analysed the data and wrote the chapter with assistance from SH. Chapter 5: PC designed the experiment, with input from SH. PC collected the data, analysed the data and wrote the chapter with assistance from SH. Chapter 6: PC designed the experiment, with input from SH. PC collected the data, analysed the data and wrote the chapter with assistance from SH. Chapter 7: PC designed the experiment, with input from SH and Professor Mark Viant. PC collected the data with assistance from the University of Birmingham NERC funded metabolomics facility and Dr Ulf Sommer. PC analysed the data with assistance from Jaspreet Sihra. PC wrote the chapter with assistance from SH. Chapter 8: Entirely my own work iv Abbreviations __________________________________________________ AFPs – Antifreeze proteins CDL – Critical day length CTmin – Critical thermal minima CTmax – Critical thermal maxima d – day D15 – Diapause larvae produced from adults acclimated to 15°C D20 – Diapause larvae produced from adults acclimated to 20°C DT – Discriminating treatment DS – Diapause selected strain DS15 – Diapause selected strain from adults at 15°C DS20 – Diapause selected strain from adults at 20°C h – hour HSPs – Heat shock proteins INAs – Ice nucleating agents LD – Light:Day length LT – Lethal time ND15 – Non-diapause larvae produced from adults acclimated to 15°C ND20 – Non-diapause larvae produced from adults acclimated to 20°C NDS – Non-diapause selected strain NDS20 – Non-diapause selected strain from adults at 15°C NDS15 – Non-diapause selected strain from adults at 20°C NMR – Nuclear magnetic resonance PE – Protein excluded PF – Protein fed RCH – Rapid cold hardening SCP – Supercooling point v Contents __________________________________________________ Chapter 1 General introduction....................................................................................... 1 1.1 Insect diversity ......................................................................................................... 2 1.2 Thermal limits of survival ......................................................................................... 3 1.3 Responses to climate change .................................................................................. 5 1.4 The biology of overwintering insects ........................................................................ 7 1.5 The phases of diapause ......................................................................................... 10 1.6 Diapause and cold hardiness ................................................................................. 17 1.7 Classes of cold hardiness ...................................................................................... 18 1.8 Activity at low temperatures ................................................................................... 25 1.9 Phenotypic plasticity .............................................................................................. 25 1.10 Climate change ....................................................................................................... 28 1.11 Calliphora vicina (Robineau-Desvoidy) ................................................................... 30 1.12 Summary and objectives ......................................................................................... 33 Chapter 2 Cross generation plasticity in cold hardiness is associated with diapause, but not the non-diapause, developmental pathway......................................................... 37 2.1 Abstract ................................................................................................................. 38 2.2 Introduction ............................................................................................................ 38 2.3 Materials and methods ........................................................................................... 42 2.4 Results .................................................................................................................. 47 2.5 Discussion ............................................................................................................
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