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Final Copy 2019 01 23 Kenn This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: Kennedy, Patrick Title: Uncertainty and the evolution of altruism theory and fieldwork in the paper wasps of Central and South America 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. Uncertainty and the evolution of altruism Theory and fieldwork in the paper wasps of Central and South America Patrick Kennedy Supervised by Dr Seirian Sumner and Professor Andrew Radford 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 Life Sciences. “Many problems of insect social life are at best seen darkly. The study of living wasps in the tropics will undoubtedly throw a great deal of light onto these problems.” – Émile Roubaud, 1916 (translated: Starr, 1996) Main text: 70,578 | Appendices: 7,445 University of Bristol Author’s 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. 2 3 GENERAL ABSTRACT The evolution of altruism (costly self-sacrifice in the service of others) has fascinated biologists since the origins of evolutionary biology. Why should selection favour altruism over self-interest? Nowhere is the problem more striking than in the social insects, where large numbers of non-reproductive workers raise the offspring of reproductive queens. For over fifty years, the dominant explanation for altruism has been ‘inclusive fitness’ theory and an associated principle known as ‘Hamilton’s rule’, which emphasises the role of relatedness: altruists help carriers of shared genes. In this thesis, I explore two outstanding problems in the evolution of altruism and inclusive fitness theory. First, does altruism evolve differently in unpredictable environments? Second, what explains the evolution of altruism by Neotropical Polistes wasps to foreign queens, a situation in which ‘drifting’ workers paradoxically divert help to distant relatives? To answer the first question, I show that altruism in unpredictable environments can be favoured without any effects on the expected reproductive success of recipients – and, in principle, can evolve even if both altruist and recipient suffer a reduction in expected reproductive success. Instead, altruists can confer volatility-suppressing benefits on recipients, stabilising their otherwise uncertain reproduction. This extends ‘bet-hedging’ theory to social behaviour, and implies a stochastic version of Hamilton’s rule that differs from the interpretation of Hamilton’s rule commonly used empirically. To answer the second question, I use field experiments in the paper wasp Polistes canadensis in French Guiana and Panama, and Polistes satan in Brazil. Using a combination of radio-tagging, queen removals, recognition tests, and a longitudinal study of brood development, I explore various hypotheses for ‘drifting’. I argue that two recently published hypotheses for cooperative ‘drifting’ in Polistes may be unlikely to provide a general explanation for paradoxical altruism. Using longitudinal data, I show strong diminishing returns to cooperation in free-living colonies, which may represent an adaptive context in which altruism to more distantly-related recipients can evolve. Finally, I discuss the tension between adaptive and neutral explanations of subtle social traits. 4 5 ACKNOWLEDGEMENTS A huge thank you to both my supervisors, Dr Seirian Sumner (University College London) and Professor Andy Radford (University of Bristol) for their guidance, brilliant support, and advice: I’ve been very lucky to have had such great supervisors. Thank you to everyone in the Sumner Lab for a fantastic four years, especially Dr Emily Bell, Robin Southon (a slightly supernatural ‘wasp whisperer’), Sam Duckerin, Adam Devenish, Sandra Moreno, Dr Daisy Udall, Ben Taylor, and Dr Michael Bentley (who read much of the modelling). Also in LSB, thanks to Barney Wharam and Andy Saxon for many in-depth conversations about wasps. The members of the Radford Lab generously tolerated wasps amongst the mongooses and fish; thank you especially to Dr Ines Goncalves and Dr Benjamin Ashton. In French Guiana, I am grateful for the support of Professor Alain Dejean (University of Toulouse) and Dr Bruno Corbara (Global Canopy Programme), who hosted Dr Thibault Lengronne and myself and provided a tip-off about the wasp mecca of Sinnamary; thank you to Thibault for sharing his fieldwork wisdom. Thank you also to the Centre d’Étude de la Biodiversité de l’Amazonie (CEBA) for funding and EcoFOG in Kourou for providing accommodation and laboratory space. Sinnamary town council generously granted us permission to work in the town. Thanks are also due to the anonymous figure who rescued us after a bad puncture on the road between Kourou and Sinnamary. In Brazil, I am very grateful to Professor Fabio Nascimento and Dr André de Souza (both of the University of São Paulo), Sam Morris, and Dr Alice Chadwick for collaboration in radio-tagging the spectacular wasp Polistes satan. In Panama, many thanks to Dr William Wcislo (Smithsonian Tropical Research Institute, STRI) for hosting me at STRI. I am grateful to STRI for funding via a Short-Term Fellowship, the STRI field station at Punta Galeta for providing accommodation, and the Behaviour Discussion Group at Tupper for helpful discussions about bet-hedging. Thank you to the soldiers of the Servicio Nacional Aeronaval for so thoughtfully offering us a surprised Polybia rejecta colony in a plastic bag, and to Dr Egbert Leigh for a memorable stay on BCI. Collecting Polistes with the whirlwind of enthusiasm that is Dr Barrett Klein was just what was needed after one sting too many. In Panama, the biggest thanks of all must go to Pieter Botha: it was a real pleasure to spend several months in the company of Pieter and Polistes, absorbing a country that can be breathtakingly beautiful. I am very grateful for the support of the National Geographic Society, who funded my fieldwork through a Young Explorer Grant (GEF-NE 145-15). The adventure into modelling (Chapters 3 and 4) has opened my eyes to the amazing power of sociobiology. I am especially grateful to Professor Andy Gardner (University of St Andrews), who hosted me at St Andrews during the most productive week of my PhD – scribbling his many insights on whiteboards exactly as I have always hoped theory work was done. I am also very grateful to Dr Andy Higginson (University of Exeter) for his excellent guidance and collaboration. Thanks are also due to Professor Samir Okasha, Professor John McNamara, Dr Suzanne Schindler and Dr Bengt Autzen (all at the University of Bristol), for conversations about modelling risk and Professor Mark Beaumount for conversations about statistics. Finally, I am grateful to Professor Barbara Koenig for generously inviting me to give a talk at the University of Zurich on the topics in Chapters 3 and 4 – and for introducing me to her incredible barn of RFID-tagged mice. 6 Closer to home, thank you for the brilliant support from: Alice Chadwick, who followed me to Brazil to risk a Polistes satan sting or two, Caris and Paddy Kennedy, Stefanie Hugh-Donovan, Geraint (and Maisie) Norris, and Ted and Henri Kennedy, who wisely didn’t ask too many questions about why there were dead wasps in their freezer and who have supported me throughout. I was inspired to launch into the PhD after the fantastic experience of learning from Professor Owen Lewis and Dr Heikki Helanterä at undergrad, and I’m ever grateful to Vivian Oi Hui, whose mission to inject The Selfish Gene into the A-level curriculum first set me on the path of biology. Lastly, a tip of the hat to the inimitable Ian Bentley – I hope he would have enjoyed reading this thesis. This PhD has taken me to some unlikely places. Hiding in a tarpaulin tent behind a fried chicken stall during a Panamanian gang shooting is not entirely what I had pictured evolutionary biologists doing. Similarly, watching the French Guiana gendarmerie swabbing my kitchen for fingerprints after child burglars made off with several items of expensive equipment, a passport, and a toothbrush was a new experience. Ultimately, wasping into strange parts of South America has left me with a love of the tropics. Any job that means there’s a good chance of sharing the shower with a small tree frog is a job worth doing.
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