Adaptation to a new environment allows cooperators to purge cheaters stochastically.
ABSTRACT: Cooperation via production of common goods is found in diverse life forms ranging from viruses to social animals. However, natural selection predicts a "tragedy of the commons": Cheaters, benefiting from without producing costly common goods, are more fit than cooperators and should destroy cooperation. In an attempt to discover novel mechanisms of cheater control, we eliminated known ones using a yeast cooperator-cheater system engineered to supply or exploit essential nutrients. Surprisingly, although less fit than cheaters, cooperators quickly dominated a fraction of cocultures. Cooperators isolated from these cocultures were superior to the cheater isolates they had been cocultured with, even though these cheaters were superior to ancestral cooperators. Resequencing and phenotypic analyses revealed that evolved cooperators and cheaters all harbored mutations adaptive to the nutrient-limited cooperative environment, allowing growth at a much lower concentration of nutrient than their ancestors. Even after the initial round of adaptation, evolved cooperators still stochastically dominated cheaters derived from them. We propose the "adaptive race" model: If during adaptation to an environment, the fitness gain of cooperators exceeds that of cheaters by at least the fitness cost of cooperation, the tragedy of the commons can be averted. Although cooperators and cheaters sample from the same pool of adaptive mutations, this symmetry is soon broken: The best cooperators purge cheaters and continue to grow, whereas the best cheaters cause rapid self-extinction. We speculate that adaptation to changing environments may contribute to the persistence of cooperative systems before the appearance of more sophisticated mechanisms of cheater control.
Project description:In a process termed quorum sensing (QS), the opportunistic bacterial pathogen Pseudomonas aeruginosa uses diffusible signaling molecules to regulate the expression of numerous secreted factors or public goods that are shared within the population. But not all cells respond to QS signals. These social cheaters typically harbor a mutation in the QS receptor gene lasR and exploit the public goods produced by cooperators. Here we show that non-social adaptation under growth conditions that require QS-dependent public goods increases tolerance to cheating and defers a tragedy of the commons. The underlying mutation is in the transcriptional repressor gene psdR. This mutation has no effect on public goods expression but instead increases individual fitness by derepressing growth-limiting intracellular metabolism. Even though psdR mutant populations remain susceptible to invasion by isogenic psdR lasR cheaters, they bear a lower cheater load than do wild-type populations, and they are completely resistant to invasion by lasR cheaters with functional psdR. Mutations in psdR also sustain growth near wild-type levels when paired with certain partial loss-of-function lasR mutations. Targeted sequencing of multiple evolved isolates revealed that mutations in psdR arise before mutations in lasR, and rapidly sweep through the population. Our results indicate that a QS-favoring environment can lead to adaptations in non-social, intracellular traits that increase the fitness of cooperating individuals and thereby contribute to population-wide maintenance of QS and associated cooperative behaviors.
Project description:The opportunistic pathogen Pseudomonas aeruginosa uses a cell-cell communication system termed "quorum sensing" to control production of public goods, extracellular products that can be used by any community member. Not all individuals respond to quorum-sensing signals and synthesize public goods. Such social cheaters enjoy the benefits of the products secreted by cooperators. There are some P. aeruginosa cellular enzymes controlled by quorum sensing, and we show that quorum sensing-controlled expression of such private goods can put a metabolic constraint on social cheating and prevent a tragedy of the commons. Metabolic constraint of social cheating provides an explanation for private-goods regulation by a cooperative system and has general implications for population biology, infection control, and stabilization of quorum-sensing circuits in synthetic biology.
Project description: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: http://dx.doi.org/10.7554/eLife.00960.001.
Project description:Public goods are the key features of all human societies and are also important in many animal societies. Collaborative hunting and collective defence are but two examples of public goods that have played a crucial role in the development of human societies and still play an important role in many animal societies. Public goods allow societies composed largely of cooperators to outperform societies composed mainly of non-cooperators. However, public goods also provide an incentive for individuals to be selfish by benefiting from the public good without contributing to it. This is the essential paradox of cooperation-known variously as the Tragedy of the Commons, Multi-person Prisoner's Dilemma or Social Dilemma. Here, we show that a new model for evolution in group-structured populations provides a simple and effective mechanism for the emergence and maintenance of cooperation in such a social dilemma. This model does not depend on kin selection, direct or indirect reciprocity, punishment, optional participation or trait-group selection. Since this mechanism depends only on population dynamics and requires no cognitive abilities on the part of the agents concerned, it potentially applies to organisms at all levels of complexity.
Project description:We present a proof of principle for the phenomenon of the tragedy of the commons that is at the center of many theories on the evolution of cooperation. Whereas the tragedy is commonly set in a game theoretical context, and attributed to an underlying Prisoner's Dilemma, we take an alternative approach based on basic mechanistic principles of species growth that does not rely on the specification of payoffs which may be difficult to determine in practice. We establish the tragedy in the context of a general chemostat model with two species, the cooperator and the cheater. Both species have the same growth rate function and yield constant, but the cooperator allocates a portion of the nutrient uptake towards the production of a public good -the "Commons" in the Tragedy- which is needed to digest the externally supplied nutrient. The cheater on the other hand does not produce this enzyme, and allocates all nutrient uptake towards its own growth. We prove that when the cheater is present initially, both the cooperator and the cheater will eventually go extinct, hereby confirming the occurrence of the tragedy. We also show that without the cheater, the cooperator can survive indefinitely, provided that at least a low level of public good or processed nutrient is available initially. Our results provide a predictive framework for the analysis of cooperator-cheater dynamics in a powerful model system of experimental evolution.
Project description:Cooperation is subject to cheating strategies that exploit the benefits of cooperation without paying the fair costs, and it has been a major goal of evolutionary biology to explain the origin and maintenance of cooperation against such cheaters. Here, we report that cheater genotypes indeed coexist in field colonies of a social insect, the parthenogenetic ant Pristomyrmex punctatus. The life history of this species is exceptional, in that there is no reproductive division of labour: all females fulfil both reproduction and cooperative tasks. Previous studies reported sporadic occurrence of larger individuals when compared with their nest-mates. These larger ants lay more eggs and hardly take part in cooperative tasks, resulting in lower fitness of the whole colony. Population genetic analysis showed that at least some of these large-bodied individuals form a genetically distinct lineage, isolated from cooperators by parthenogenesis. A phylogenetic study confirmed that this cheater lineage originated intraspecifically. Coexistence of cheaters and cooperators in this species provides a good model system to investigate the evolution of cooperation in nature.
Project description:Cooperative organisms evolve within socially diverse populations. In populations harboring both cooperators and cheaters, cooperators might adapt by evolving novel interactions with either social type or both. Diverse animal traits suppress selfish behaviors when cooperation is important for fitness, but the potential for prokaryotes to evolve such traits is unclear. We allowed a strain of the bacterium Myxococcus xanthus that is proficient at cooperative fruiting body development to evolve while repeatedly encountering a non-evolving developmental cheater. Evolving populations greatly increased their fitness in the presence of the cheater, both relative to their ancestor and in terms of absolute spore productivity. However, the same evolved lineages exhibited a net disadvantage to the ancestor in the cheater's absence. Evolving populations reversed a large ancestral disadvantage to the cheater into competitive superiority and also evolved to strongly suppress cheater productivity. Moreover, in three-party mixes with the cheater, evolved populations enhanced their ancestor's productivity relative to mixes of only the ancestor and cheater. Thus, our evolved populations function as selfish police that inhibit cheaters, both to their own advantage and to the benefit of others as well. Cheater suppression was general across multiple unfamiliar cheaters but was more pronounced against the evolutionarily familiar cheater. Also, evolution generated three new mutually beneficial relationships, including complementary defect rescue between evolved cells and the selection-regime cheater. The rapid evolution of cheater suppression documented here suggests that coevolving social strategies within natural populations of prokaryotes are more diverse and complex than previously appreciated.
Project description:The evolution of sociality and altruism is enigmatic because cooperators are constantly threatened by cheaters who benefit from cooperation without incurring its full cost [1, 2]. Kin recognition is the ability to recognize and cooperate with genetically close relatives. It has also been proposed as a potential mechanism that limits cheating [3, 4], but there has been no direct experimental support for that possibility. Here we show that kin recognition protects cooperators against cheaters. The social amoebae Dictyostelium discoideum cooperate by forming multicellular aggregates that develop into fruiting bodies of viable spores and dead stalk cells. Cheaters preferentially differentiate into spores while their victims die as stalk cells in chimeric aggregates. We engineered syngeneic cheaters and victims that differed only in their kin-recognition genes, tgrB1 and tgrC1, and in a single cheater allele and found that the victims escaped exploitation by different types of nonkin cheaters. This protection depends on kin-recognition-mediated segregation because it is compromised when we disrupt strain segregation. These findings provide direct evidence for the role of kin recognition in cheater control and suggest a mechanism for the maintenance of stable cooperative systems.
Project description:BACKGROUND:Recent work on the complexity of life highlights the roles played by evolutionary forces at different levels of individuality. One of the central puzzles in explaining transitions in individuality for entities ranging from complex cells, to multicellular organisms and societies, is how different autonomous units relinquish control over their functions to others in the group. In addition to the necessity of reducing conflict over effecting specialized tasks, differentiating groups must control the exploitation of the commons, or else be out-competed by more fit groups. RESULTS:We propose that two forms of conflict - access to resources within groups and representation in germ line - may be resolved in tandem through individual and group-level selective effects. Specifically, we employ an optimization model to show the conditions under which different within-group social behaviors (cooperators producing a public good or cheaters exploiting the public good) may be selected to disperse, thereby not affecting the commons and functioning as germ line. We find that partial or complete dispersal specialization of cheaters is a general outcome. The propensity for cheaters to disperse is highest with intermediate benefit:cost ratios of cooperative acts and with high relatedness. An examination of a range of real biological systems tends to support our theory, although additional study is required to provide robust tests. CONCLUSION:We suggest that trait linkage between dispersal and cheating should be operative regardless of whether groups ever achieve higher levels of individuality, because individual selection will always tend to increase exploitation, and stronger group structure will tend to increase overall cooperation through kin selected benefits. Cheater specialization as dispersers offers simultaneous solutions to the evolution of cooperation in social groups and the origin of specialization of germ and soma in multicellular organisms.
Project description:Many Proteobacteria use quorum sensing to regulate production of public goods, such as antimicrobials and proteases, that are shared among members of a community. Public goods are vulnerable to exploitation by cheaters, such as quorum sensing-defective mutants. Quorum sensing- regulated private goods, goods that benefit only producing cells, can prevent the emergence of cheaters under certain growth conditions. Previously, we developed a laboratory co-culture model to investigate the importance of quorum-regulated antimicrobials during interspecies competition. In our model, Burkholderia thailandensis and Chromobacterium violaceum each use quorum sensing-controlled antimicrobials to inhibit the other species' growth. Here, we show that C. violaceum uses quorum sensing to increase resistance to bactobolin, a B. thailandensis antibiotic, by increasing transcription of a putative antibiotic efflux pump. We demonstrate conditions where C. violaceum quorum-defective cheaters emerge and show that in these conditions, bactobolin restrains cheaters. We also demonstrate that bactobolin restrains quorum-defective mutants in our co-culture model, and the increase in antimicrobial-producing cooperators drives the C. violaceum population to become more competitive. Our results describe a mechanism of cheater restraint involving quorum control of efflux pumps and demonstrate that interspecies competition can reinforce cooperative behaviors by placing constraints on quorum sensing-defective mutants.