The Evolution of Cooperation, Especially in Humans Submitted for the Degree of Doctor of Philosophy Trinity Term 2011 presented by supervised by Claire El Mouden Prof. Stuart West Dr. Andy Gardner dedicated in memory of my sparkly little cousin dedicated to the memoryCelia of my sp Brennerarkly little cousin Celia Brenner Table of Contents Declaration 4 Acknowledgements 6 Abstract 8 Chapter 1. Introduction. 9 Chapter 2. Nice natives and mean migrants: the evolution of dispersal- dependent social behaviour in viscous populations. 38 Chapter 3. The enforcement of cooperation by policing. 66 Chapter 4. Group competition and the evolution of cooperation in humans. 98 Chapter 5. Reproductive levelling and the evolution of cooperation between non-kin. 118 Chapter 6. Promiscuity and the evolution of cooperative breeding. 133 Chapter 7. Spatial structure and inter-specific cooperation: Theory and an empirical test using the mycorrhizal mutualism 150 Chapter 8. Discussion. 178 Literature Cited 188 Appendix 205 Declaration The literature review in Chapter 1 is adapted from a forthcoming book chapter: El Mouden, C, West S, Gardner A, Burton-Chellew M. (2012). ‘What do humans maximise?’, in: Evolution and Rationality: Decisions, Cooperation and Strategic Behaviour, Samir Okasha and Ken Binmore (eds) OUP. This is my own work; my coauthors provided comments and advice on draft manuscripts. Chapter 2 is a published paper: El Mouden, C and Gardner, A. (2008) ‘Nice natives and mean migrants: the evolution of dispersal-dependent social behaviour in viscous populations’, Journal of Evolutionary Biology 21, 1480-1491. The original idea for the paper was AG’s, I led the theory and write-up, with significant assistance from AG at all stages; AG wrote the Appendix in response to reviewer comments. Chapter 3 is a published paper: El Mouden, C., West, S. A. and Gardner, A (2010). ‘The enforcement of cooperation by policing’, Evolution. 64, 2139-2152. The original idea for the paper was developed together with SW and AG. I led the theory and write-up, with assistance from both coauthors. AG wrote the original Mathematica code for the eigenvalue analysis, which I extended. Chapter 4 is being prepared for publication. I developed the original idea and led the theory and write up. AG and SW provided advice and ideas throughout. Chapter 5 is in review at Evolution and Human Behaviour as a research paper. I had the original idea for the paper, developed the theory and performed the analysis. AG and SW contributed to the write up. 4 Chapter 6 is a published paper: Leggett, H., El Mouden, C., Wild, G., and West, S. A. (2011) ‘Promiscuity and the evolution of cooperative breeding’, Proceedings of the Royal Society, B doi:10.1098/rspb.2011.1627. HL and GW conceived the original idea, I helped formulate the inclusive fitness equation, I led the model analysis and wrote the Appendix, GW conducted the numerical investigation, HL led the write-up, to which SW, GW and I contributed. Chapter 7 is in press: Verbruggen, E., El Mouden, C., Jansa, J. Akkermans, G., Bucking,̈ H., West, S. A. and Kiers, T. (2012) ‘Spatial structure and cooperation: Theory and an empirical test using the mycorrhizal mutualism’, American Naturalist. In collaboration with SW, I developed the theory, analyzed and wrote the theory section of the paper. The experimental work and remaining write-up was undertaken by my coauthors. The Appendix contains my three other publications. Section 1 is a published book review: El Mouden, C. (2011) Life: social to its core. Evolution and Human Behaviour 33(1): 79-80. This is entirely my own work. Section 2 is a published experimental paper: Harrison, F. H. and El Mouden, C. (2011). ‘Money for nothing, cooperation for free: exploring the effects of working for endowments on behaviour in standard economic games’, PLoS ONE 6(11): e27623. FH had the original idea and designed the experiments. I collected one-third of the data for the public goods game and all the dictator game data (together with FH). FH performed the statistical analysis and we both wrote the paper. Section 3 is a published review paper: West, S.A., El Mouden, C. and Gardner, A. (2011). ‘Sixteen common misconceptions about the evolution of cooperation in humans’, Evolution and Human Behavior 32(4): 231-262. SW, AG and I developed the paper’s ideas together. SW led the write-up; AG and I wrote some sub-sections and provided extensive comments. 5 Acknowledgements The work herein benefited enormously from the comments, discussion, collaboration and encouragement of many people, including: Alan Grafen, Alex Kacelnik, Anthony Edwards, Ashleigh Griffin, Ben Roberts, Charlie Cornwallis, Dan Cornforth, Dan Nettle, Daniel Rankin, Dave Queller, Denis Roze, Helen Leggett, Freya Harrison, Geoff Wild, Heikki Helanterä, Joan Strassmann, Joao Alpedrinha, Ken Binmore, Kevin Foster, Laurent Lehmann, Max Burton-Chellew, Paul Seabright, Peter Taylor, Peyton Young, Rolf Kümmerli, Samir Okasha, Shakti Lamba and Tobi Kiers. Ashleigh and Joan, thank you so much for the pro-femina motivational pep talks in Denmark! You convinced me that I have a future in Science and I would not have applied to Nuffield had I not your voices in my head. I would not have survived the interview committee without Ashleigh, Alan, Kevin and Alex’s invaluable advice. In particular, from the bottom of my heart, thank you to my supervisors Stu and Andy. I cannot hope to convey how much your expertise, teaching, patience, understanding and unwavering encouragement these past four years has meant to me. You are, in your own very unique ways, outstanding role models and it’s an honour to consider you both friends. Respect. I thank the Biotechnology and Biological Sciences Research Council and the University of Edinburgh for providing me with my Doctoral Training Grant. Finally, Anass, Mum and Dad thank you for all your love and constant support. I could not have done this without you. 6 7 Abstract I develop social evolution theory to study the evolution of cooperation as follows: (1) Many organisms undergo a dispersal phase prior to breeding; I demonstrate that knowing ones dispersal status aids the evolution of helping (by non-dispersers) and harming (by dispersers). (2) Policing driven by group-benefits may be selected to enforce cooperation in human and animal societies. I extend existing theory to show that policing may be harder to evolve that previously thought, but that it is maintained more readily than it evolves. (3) Archeological and anthropological evidence suggests that warfare was prevalent during our evolution. I show that, contrary to previous suggestions, between-group competition can favour any social behaviour (pro-social or anti-social) so long as it helps the group compete, and that such traits can be altruistic or mutually beneficial. (4) Reproductive leveling is analogous to policing; in the human literature there is doubt as to whether it can evolve. I extend my previous work to consider the coevolution of culturally and genetically inherited traits for reproductive leveling and selfishness. I find that cooperation can evolve between non-kin if they share the same culture. (5) Monogamy is thought to favour the evolution of cooperative breeding. I show that in the simplest case, because of the cost of competition between non-dispersing siblings, the level of promiscuity has little or no effect on the evolution of cooperation. (6) Spatial structure (limited dispersal) is thought to favour the evolution of inter- specific mutualisms as it aligns the partners’ interests. I consider the case of plant- fungi mutualisms and show that spatial structure can disfavour cooperation if it limits the potential fungal partners available to the plant. Word Count (excluding references and appendices): 46,525 words 8 Chapter 1. Introduction. This Chapter provides a background to the field of social evolution and how it is applied to study human behaviour (section 1.1) and an outline of the thesis’s structure (section 1.2). 1.1 Background Research on human evolution and cooperative behaviour is undertaken in biology, psychology, economics, anthropology, sociology and archaeology. Whilst all these disciplines have important and relevant insights for my research, a comprehensive review would be far beyond the scope of this chapter. Therefore, the background section focuses on the question ‘what do humans maximise?’ as the answer introduces the key concepts of evolutionary theory, gives a flavour of the work being undertaken in other disciplines and neatly illustrates the breath and complexity of this field. Section 1.1.1 explains the process of natural selection, discusses the purpose of adaptation and explains why cooperation is favoured in nature. Section 1.1.2 considers why organisms are not expected to be perfect or optimal inclusive fitness maximisers. Section 1.1.3 discusses what evolutionary theory predicts humans will maximize and, having established that humans may behave as inclusive fitness maximisers, section 1.1.4 discusses the reasons why people’s actions sometimes appear not to maximize inclusive fitness (or anything else). Finally, section 1.1.5 draws on the ideas developed in the earlier sections to discuss whether or when humans are expected to match the predictions of economic rational choice models. 9 1.1.1 What is the purpose of adaptation? In crossing a heath, suppose I pitched my foot against a stone, and were asked how the stone came to be there, I might possibly answer that, for anything I knew to the contrary, it had laid there for ever...But suppose I had found a watch upon the ground, and it should be enquired how the watch happened to be in that place, I should hardly think of the answer which I had before given, that, for any thing I knew, the watch might have always been there.