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Causes and Consequences of Genetic Caste-Bias in the Eusocial Hymenoptera

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Causes and consequences of genetic caste-bias in the eusocial Hymenoptera Rowena Elisabeth Mitchell Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology September 2013 ii The candidate confirms that the work submitted is her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Chapter 6 contains work from a jointly authored publication: Mitchell, R. E., Frost, C. L., Hughes, W. O. H. (2012). Size and asymmetry: are there costs to winning the royalty race? Journal of Evolutionary Biology 25: 522– 531. Author contributions are as follows: REM designed the experiments, carried out the experimental work, analysed the data and wrote the manuscript. CLF assisted with the genotyping of ants. WOHH supervised the work, assisted with the design of the experiments, the data analysis and drafting of the manuscript. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. © 2013 The University of Leeds and Rowena Mitchell The right of Rowena Mitchell to be identified as Author of this work has been asserted by her in accordance with the Copyright, Designs and Patents Act 1988. iii Acknowledgements Firstly, I would like to thank Bill Hughes for giving me the opportunity to undertake this work and for all your help, encouragement and advice; I have learnt a lot. Thank you to Terry Crawford for nudging me down this road and for telling me I’d have what it takes. Thank you to Bill Cadmore for looking after our bees and then letting me use yours, and thank you to Koos Boomsma for letting me raid the Copenhagen Acro. colonies right at the start. Thank you to Paula Chappell for help in the lab, it would have been so much harder without you. Thank you to all the friends I have made throughout this journey. Thank you to Chris Tranter, Jasmine Parkinson and Victoria Norman for making me so welcome in Brighton and making sure I had everything I needed. Thanks to Crystal Frost, and Katherine Roberts help, advice, fun and good food, you made the lab such a great place to work. Thank you to Peter Graystock for making me chuckle, for being an adequate tea-maid and a great scientist, it rubs off on us all. Thanks to Kirsten Foley and Claire Asher for travelling this road with me, we all made it in the end. Thanks to Liz Elliot for supporting me through the good and the not-so-good, for preventing otherwise inevitable obesity, and for being such a wonderful friend. A really special thank you goes to Sophie Evison; I could not have done this without your help, you have been an absolute inspiration to me as well as a great friend. Thank you to my whole family for their love and support. Thanks to Lucy and Alex for being the best sibs ever, I hope you are as proud of me as I am of you. Thank you to Mum and Dad for giving us every opportunity we could have wished for and more, it is through a lifetime of encouragement that I have been able to get to where I am today and do so many great things along the way. Finally, thank you to Alan for your unerring belief that I can achieve anything I set my mind to, for making me laugh and for being a constant reminder that life outside the lab is so much better than a life spent in it. iv Abstract The eusocial Hymenoptera is one of the most successful groups to ever colonise the planet. They are defined by reproductive division of labour, whereby reproduction in a colony is dominated by one or a few queens, whilst all other individuals are more- or-less sterile. There has been much interest in understanding the mechanistic basis of caste determination, and particular interest in the evidence for genotypic variation in the propensity of individuals to become queens. However, the mechanisms underlying such genotypic variation in caste fate are as yet unknown. In this thesis, I examine potential causes and consequences of genetic caste-bias using the honey bee, Apis mellifera, and Acromyrmex leaf-cutting ants. In A. mellifera, individuals with queen-biased genotypes were shown to have a higher growth rate than those from genotypes with no caste-bias or a worker-bias. The variable response, in terms of growth rate, of genotypes to treatment with a juvenile hormone analogue suggested that variation in caste propensity could potentially arise from differential responses to environmentally induced physiological cues. In addition, an immune challenge by the fungal parasite Ascosphaera apis was found to affect the growth rate of A. mellifera larvae and caste determination at the colony level, suggesting that resistance to parasites may also be important in determining caste fate. In many species, workers have some control over caste determination, and I show that Ac. octospinosus workers were able to discriminate between nestmate and non-nestmate brood, even after larvae had been in contact with the fungus garden. That workers were able to discriminate between larvae within the nest suggests that they may be able to differentiate closely related kin during caste determination, despite homogenisation of fine scale cues. Finally, a positive relationship between patriline queen-worker skew and fluctuating asymmetry, an indicator of developmental stress, was found in Ac. echinatior, suggesting that subtle costs to caste-biasing strategies could explain the rarity of queen-biased genotypes. Overall this work shows that genotypic differences in the physiological response to environmental cues may underlie genetic caste-bias in the social insects. However, understanding the interaction between physiology, environment and genotype is essential if we are to understand the ultimate determinants of individual caste fate. v Contents Acknowledgements ................................................................................................... iii Abstract ...................................................................................................................... iv List of Figures ............................................................................................................ ix List of Tables ............................................................................................................. xi 1. General introduction ........................................................................................ 1 1.1 The eusocial Hymenoptera .......................................................................... 1 1.2 Conditions for the evolution of eusociality in the Hymenoptera ................. 2 1.3 Polyandry in the eusocial Hymenoptera ...................................................... 4 1.4 Altruism under conditions of low relatedness ............................................. 5 1.5 Caste determination mechanisms ................................................................ 7 1.5.1 Environmental caste determination .................................................. 7 1.5.2 Genetic caste determination ............................................................. 8 1.5.3 Gene by environment interactions.................................................. 10 1.5.4 Worker caste ................................................................................... 11 1.5.5 Social species without a queen caste .............................................. 13 1.5.6 The molecular basis of caste determination ................................... 14 1.6 Conflict over caste determination .............................................................. 15 1.7 Caste determination in the honey bee, Apis mellifera ............................... 18 1.8 ‘Royal cheats’ in leaf-cutting ants ............................................................. 19 1.9 Nepotism in the eusocial Hymenoptera ...................................................... 21 1.10 Causes and consequences of genetic caste-bias in the eusocial Hymenoptera..................................................................................................... 23 2. Raising royalty: genotypic variation in larval growth rate affects royal destiny in honey bees ...................................................................................... 25 Abstract ............................................................................................................. 25 2.1 Introduction................................................................................................ 26 vi 2.2 Methods ..................................................................................................... 28 2.2.1 Growth rate quantification ............................................................. 28 2.2.2 Royal propensity ............................................................................ 29 2.2.3 Genotyping ..................................................................................... 29 2.2.4 Statistical analysis .......................................................................... 31 2.3 Results ....................................................................................................... 32 2.3.1 Genetic variation in growth rate ..................................................... 32 2.3 2 Growth rate and royal propensity ..................................................
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