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Final Copy 2018 09 25 South This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: Southon, Robin Title: The adaptive value of males in simple eusocial insect societies General rights Access to the thesis is subject to the Creative Commons Attribution - NonCommercial-No Derivatives 4.0 International Public License. A copy of this may be found at https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode This license sets out your rights and the restrictions that apply to your access to the thesis so it is important you read this before proceeding. Take down policy Some pages of this thesis may have been removed for copyright restrictions prior to having it been deposited in Explore Bristol Research. However, if you have discovered material within the thesis that you consider to be unlawful e.g. breaches of copyright (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please contact [email protected] and include the following information in your message: •Your contact details •Bibliographic details for the item, including a URL •An outline nature of the complaint Your claim will be investigated and, where appropriate, the item in question will be removed from public view as soon as possible. The Adaptive Value of Males in Simple Eusocial Insect Societies Robin Jan Southon A dissertation submitted to the University of Bristol in accordance with the requirements for award of the degree of Doctor of Philosophy in the Faculty of Science (July 2018) Word Count: 69,733 The adaptive value of males in simple eusocial insect societies Abstract In the Hymenoptera (ants, bees, and wasps), female inclusive fitness is maximised directly by reproducing or indirectly through helping kin. By contrast, males have mainly evolved to disperse and mate, limiting fitness opportunities to direct reproduction. However, there are reports across the social Hymenoptera of natal males helping, by distributing food to brood, as well as defending and thermoregulating nests. It is not fully understood under what circumstances male help, how it is regulated, or whether helping carries indirect fitness benefits. Here, the hypothesis is tested that males are more than just ‘flying sperm’, and may have diversified pathways to maximising inclusive fitness. In achieving this aim, two tropical simple eusocial Polistinae paper wasps are studied, Polistes canadensis and Polistes lanio. First, through discovery and validation of new single-nucleotide polymorphism (SNP) markers, it is shown that siblings on the nest are fully related; suggesting indirect fitness opportunities for brothers. Second, using captive studies of P. canadensis, it is found that females are long-lived; suggesting short-term male investments have the potential to be assured by sisters after males depart. Third, males of P. lanio are delayed dispersers: in field studies males remained on the natal nest whilst sexually maturing; eventual dispersal was regulated by juvenile hormone. Delayed dispersal with immaturity suggests a life history phase in which direct fitness gains are not achievable for adult males. Finally, by experimentally offering food to natal P. lanio males in field trials, males were shown to help by distributing food to brood; but this effort diminished with age, suggesting male helping is temporary. In conclusion, it is proposed that males have the potential to exploit two different fitness strategies in their life, of a young helper that may benefit from indirect fitness gains and old reproductive that invests in mating and direct fitness. I II Acknowledgements First and foremost, I would like to thank the wasps. I have lost count of how many times I have been stung now, but I am sure I deserved each sting. I’d also like to thank my supervisors Seirian Sumner and Andy Radford, without their help (and patience) this study would have not been possible. The University of Bristol has provided support and encouragement throughout, and I would like to thank the School of Biological Sciences and its occupants. In addition, University College London took me in after my supervisor moved, and treated me as one of their own. Whilst in Trinidad, the University of the West Indies opened their doors to me and provide immense help without question when I showed up lost and confused on the hunt for wasps, and have been instrumental in this study (thanks for the last minute dry ice). Part of this project used samples collected from Panama, and for that I am grateful to the Smithsonian Tropical Research Institute. This study was primarily funded by the Natural Environment Research Council (NERC), with additional funding from the Genetics Society (fieldwork grant), and Bristol University’s Alumni Foundation (conference travel grant). Thank you to Innes Cuthill and Elli Leadbeater for examining my viva. The ‘Sumner lab group’ has been my colleges and friends for the past four years, and I would like to thank Alessandro Cini, Ben Taylor, Chris Wyatt, Sam Duckerin, and Sandra Moreno. A few people in the group need a descriptive shout-out: Patrick Kennedy, you beat my ‘being stung’ count by far, for that you have my respect; Peter Graystock, thanks for teaching me how to use a pipette; Adam Devenish, our coffee/pub breaks are a cornerstone of this study; Daisy Taylor, thanks for taking me to hospital for apparent vampire bat induced rabies. Last and certainly not least, Emily Bell this all started when I turned up one day in Panama as your field assistant and escalated into this study (time will tell if I am thankful for that), you’ve been a best friend and your support has been unparalleled. I would also like to thank everyone else at both Bristol University and UCL, especially Calum McIntosh, Charlotte Bickler, Chris Langridge, Dan Jue Lan, Henry Ferguson-Gow, Jon Bridle, Paul Parsons, Brett Marshbanks, Barney Wharam (always smiling), and no other than Jeroen “J” Martins (thanks for lessons in solution dilution at 12 o’clock at night). Paramount in the field has been the help of Daniel Fabbro, Joshua Valverde (funded by the Genetics Society), Liam Crowley (NERC), and Sam Morris (NERC), thanks for dealing with the rain and machete wielding men. At STRI, thank you to William Wcislo and Donald Windsor for their help. At UWI, I would like to thank Chris Starr and Mike Rutherford for their knowledge and insight into the local wasps. In Arima Valley, Ricki, Baldeo, Mashesh, and their families, thanks for letting us into your homes. In addition, thank you to Andrew and Calum Stephenson for their knowledge of the island and help. Also, the ‘gupsters’ of Arima Valley, for showing me another side of Trinidad that wasn’t chicken sheds and abandoned buildings (also the ‘other gupsters’ hiding up in Simla, Kevin Horng, Ronnie Hernandez, and Sean Ehlman). A descriptive shout-out to Toby Hector, no one else appreciates puncheon as much as you; and Ashley Hedrick, you’ve had to deal with me the most, and have supported me the most, your funnelling of beer, nachos, and that food you make which I cannot pronounce has been valued more than anything. Lastly, the occupants of ‘home on the hill’, thanks for all the stag. Special thanks to my parents, Fran Solich & Steve Southon. Permits Panama, 2013: ANAM research permit SE/A-55-13 (Emily Bell & Seirian Sumner) Trinidad & Tobago, 2013: Wild Life Section, Special Game License (Seirian Sumner) Trinidad & Tobago, 2014: Wild Life Section, Special Game License (Robin Southon) Trinidad & Tobago, 2015: Wild Life Section, Special Game License (Robin Southon & Daisy Taylor) III IV Declaration I declare that the work in this dissertation was carried out in accordance with the requirements of the University's Regulations and Code of Practice for Research Degree Programmes and that it has not been submitted for any other academic award. Except where indicated by specific reference in the text, the work is the candidate's own work. Work done in collaboration with, or with the assistance of, others, is indicated as such. Any views expressed in the dissertation are those of the author. V VI Table of Contents Chapter 1: General Introduction 1.1. The evolution of sociality and altruism 1–2 1.2. Altruism in female Hymenoptera 3–5 1.3. The lack of helping behaviour in Hymenoptera males 6–12 1.3.1. Absence of male hymenopteran helpers: lack of ancestral paternal care 6–8 1.3.2. Absence of male hymenopteran helpers: morphological restrictions 8–9 1.3.3. Absence of male hymenopteran helpers: relatedness asymmetries 9–10 1.3.4. Absence of male hymenopteran helpers: protected invasion hypothesis 11 1.3.5. Absence of male hymenopteran helpers: other Explanations 11–12 1.4. Paradoxical acts of helping in natal male Hymenoptera 13–21 1.4.1. Helping in natal hymenopteran males: food distribution behaviour 13–15 1.4.2. Helping in natal hymenopteran males: nest defence behaviour 15–17 1.4.3. Helping in natal hymenopteran males: nest thermoregulation behaviour 18 1.4.4. A note on the unusual case of male helping in the wasp Trypoxylon politum 19–20 1.4.5. The adaptive value of hymenopteran male helping 20–21 1.5. Are helping males delayed dispersers? 21–24 1.6. Can males gain indirect fitness from helping? 24–25 1.7. The evolution of male helping behaviour – social contracts and assured fitness 25–26 1.8. The Polistinae paper wasps as a model system 26–28 1.9. Aims of the thesis 29–31 1.9.1. Chapter 2 and 3: What is the genetic structure of tropical Polistes nests? 29 1.9.2.
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