Spatial self-organization favors heterotypic cooperation over cheating

RESEARCH ARTICLE elife.elifesciences.org Spatial self-organization favors heterotypic cooperation over cheating Babak Momeni*, Adam James Waite, Wenying Shou* Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States Abstract Heterotypic cooperation—two populations exchanging distinct benefits that are costly to produce—is widespread. Cheaters, exploiting benefits while evading contribution, can undermine cooperation. Two mechanisms can stabilize heterotypic cooperation. In ‘partner choice’, cooperators recognize and choose cooperating over cheating partners; in ‘partner fidelity feedback’, fitness-feedback from repeated interactions ensures that aiding your partner helps yourself. How might a spatial environment, which facilitates repeated interactions, promote fitness-feedback? We examined this process through mathematical models and engineered Saccharomyces cerevisiae strains incapable of recognition. Here, cooperators and their heterotypic cooperative partners (partners) exchanged distinct essential metabolites. Cheaters exploited partner-produced metabolites without reciprocating, and were competitively superior to cooperators. Despite initially random spatial distributions, cooperators gained more partner neighbors than cheaters did. The less a cheater contributed, the more it was excluded and disfavored. This self-organization, driven by asymmetric fitness effects of cooperators and cheaters on partners during cell growth into open space, achieves assortment. DOI: 10.7554/eLife.00960.001 *For correspondence: (BM); (WS) Competing interests: The authors declare that no competing interests exist. Funding: See page 16 Received: 17 May 2013 Accepted: 04 October 2013 Published: 12 November 2013 Reviewing editor: Diethard Tautz, Max Planck Institute for Evolutionary Biology, Germany Copyright Momeni et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Introduction Cooperation, providing a benefit available to others at a cost to self, has been postulated to drive major transitions in evolution (Maynard Smith and Szathmary, 1998). Cooperation may take place between similar individuals contributing and sharing identical benefits (homotypic cooperation) or between two populations exchanging distinct benefits such as in some forms of mutualism (heterotypic cooperation). Both homotypic and heterotypic cooperation are vulnerable to cheaters (Turner and Chao, 1999; Strassmann et al., 2000; Bronstein, 2001; Rainey and Rainey, 2003; Travisano and Velicer, 2004). Cheaters exploit cooperative benefits without contributing their fair share and are therefore competitively superior to their cooperating counterparts. How might cooperation avoid being taken over by cheaters? The answer lies in ‘positive assortment’ (Fletcher and Doebeli, 2009), in which benefit-supplying individuals interact more with other benefit-supplying individuals than with cheaters. In homotypic cooperation that involves genetic relatives, positive assortment can be realized through ‘kin discrimination’, which is based on the active recognition and preferential treatment of more closely related individuals over distantly related ones (Sachs et al., 2004). Positive assortment can also be realized through ‘kin fidelity’ (Sachs et al., 2004). For example, restricted migration in a spatial environment causes homotypic cooperators and cheaters to cluster with their respective progeny. This clustering allows cooperators to preferentially interact with each other (Figure 1A, top). Both mechanisms of positive assortment can favor cooperation (Hamilton, 1964a; Hamilton, 1964b; Maynard Smith, 1964; Chao and Levin, 1981; Nowak and May, 1992; Fletcher and Doebeli, 2006; Kerr et al., 2006; MacLean and Gudelj, 2006; West et al., 2006; Lion and Baalen, 2008; Wild et al., 2009; West and Gardner, 2010). A spatial environment may also impede homotypic cooperation by intensifying competition among cooperators (Taylor, 1992; Wilson et al., 1992; Momeni et al. eLife 2013;2:e00960. DOI: 10.7554/eLife.00960 1 of 18 Research article Ecology | Genomics and evolutionary biology eLife digest Cooperation between individuals of the same species, and also between different species, is known to be important in evolution. Large fish, for example, rely on small cleaner fish to remove parasites, while the small fish benefit from the nutrients in these parasites. However, cooperation can be undermined by other individuals or species who “cheat” by taking advantage of those who cooperate, without providing any benefits in return. For example, some cleaner fish cheat by biting off healthy tissue from their host, in addition to parasites. Genetically-related individuals who cooperate by sharing identical benefits can combat cheaters by giving preferential treatment to their relatives (a process known as kin discrimination) or by staying close to the relatives to form clusters (kin fidelity). However, two genetically-unrelated populations that mutually cooperate by sharing different benefits cannot employ these methods to overcome cheaters. Instead they rely on either partner choice or partner fidelity feedback. Partner choice – the approach adopted by cleaner fish and their hosts – relies on one population recognizing a signal from the other population and responding accordingly: for example, large fish observe cleaner fish and approach those that cooperate with their current host and avoid those that cheat. Partner fidelity feedback, on the other hand, relies on repeated interactions between the two populations providing an advantage in terms of evolutionary fitness to both: for example, organelles called mitochondria and chloroplasts live inside cells, helping the cells to harvest energy and providing energy for themselves and the host cells in the process. In some cases – such as the cooperation between figs and fig wasps, or between certain plants and the bacteria that fix nitrogen in their roots – researchers cannot agree if the populations are relying on partner choice or partner fidelity feedback. Now Momeni et al. have used a combination of experiments on yeast and mathematical modeling to explore partner fidelity feedback in greater detail. They started by using genetic engineering techniques to produce two species of yeast that mutually cooperate, each providing a metabolite that is essential to the other, but are not able to recognize each other: this means that these populations cannot rely on partner choice to combat cheaters. Momeni et al. then observed how these two species interacted with each other and a third species of yeast that cheated by consuming one of the metabolites without releasing any metabolite of its own. Momeni et al. found that as long as there was space for the yeast cells to grow into, the two species that cooperated se (...truncated)