Kin recognition protects cooperators against cheaters.
ABSTRACT: 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:Free-living cells of the social amoebae Dictyostelium discoideum can aggregate and develop into multicellular fruiting bodies in which many die altruistically as they become stalk cells that support the surviving spores. Dictyostelium cells exhibit kin discrimination--a potential defense against cheaters, which sporulate without contributing to the stalk. Kin discrimination depends on strain relatedness, and the polymorphic genes tgrB1 and tgrC1 are potential components of that mechanism. Here, we demonstrate a direct role for these genes in kin discrimination. We show that a matching pair of tgrB1 and tgrC1 alleles is necessary and sufficient for attractive self-recognition, which is mediated by differential cell-cell adhesion. We propose that TgrB1 and TgrC1 proteins mediate this adhesion through direct binding. This system is a genetically tractable ancient model of eukaryotic self-recognition.
Project description: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: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: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 cooperative developmental system of the social amoeba Dictyostelium discoideum is susceptible to exploitation by cheaters-strains that make more than their fair share of spores in chimerae. Laboratory screens in Dictyostelium have shown that the genetic potential for facultative cheating is high, and field surveys have shown that cheaters are abundant in nature, but the cheating mechanisms are largely unknown. Here we describe cheater C (chtC), a strong facultative cheater mutant that cheats by affecting prestalk differentiation. The chtC gene is developmentally regulated and its mRNA becomes stalk-enriched at the end of development. chtC mutants are defective in maintaining the prestalk cell fate as some of their prestalk cells transdifferentiate into prespore cells, but that defect does not affect gross developmental morphology or sporulation efficiency. In chimerae between wild-type and chtC mutant cells, the wild-type cells preferentially give rise to prestalk cells, and the chtC mutants increase their representation in the spore mass. Mixing chtC mutants with other cell-type proportioning mutants revealed that the cheating is directly related to the prestalk-differentiation propensity of the victim. These findings illustrate that a cheater can victimize cooperative strains by exploiting an established developmental pathway.
Project description:Contributing to cooperation is typically costly, while its rewards are often available to all members of a social group. So why should individuals be willing to pay these costs, especially if they could cheat by exploiting the investments of others? Kin selection theory broadly predicts that individuals should invest more into cooperation if their relatedness to group members is high (assuming they can discriminate kin from nonkin). To better understand how relatedness affects cooperation, we derived the ?Collective Investment" game, which provides quantitative predictions for patterns of strategic investment depending on the level of relatedness. We then tested these predictions by experimentally manipulating relatedness (genotype frequencies) in mixed cooperative aggregations of the social amoeba Dictyostelium discoideum, which builds a stalk to facilitate spore dispersal. Measurements of stalk investment by natural strains correspond to the predicted patterns of relatedness-dependent strategic investment, wherein investment by a strain increases with its relatedness to the group. Furthermore, if overall group relatedness is relatively low (i.e., no strain is at high frequency in a group) strains face a scenario akin to the "Prisoner's Dilemma" and suffer from insufficient collective investment. We find that strains employ relatedness-dependent segregation to avoid these pernicious conditions. These findings demonstrate that simple organisms like D. discoideum are not restricted to being ?cheaters" or ?cooperators" but instead measure their relatedness to their group and strategically modulate their investment into cooperation accordingly. Consequently, all individuals will sometimes appear to cooperate and sometimes cheat due to the dynamics of strategic investing.
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:Self and kin discrimination are observed in most kingdoms of life and are mediated by highly polymorphic plasma membrane proteins. Sequence polymorphism, which is essential for effective recognition, is maintained by balancing selection. Dictyostelium discoideum are social amoebas that propagate as unicellular organisms but aggregate upon starvation and form fruiting bodies with viable spores and dead stalk cells. Aggregative development exposes Dictyostelium to the perils of chimerism, including cheating, which raises questions about how the victims survive in nature and how social cooperation persists. Dictyostelids can minimize the cost of chimerism by preferential cooperation with kin, but the mechanisms of kin discrimination are largely unknown. Dictyostelium lag genes encode transmembrane proteins with multiple immunoglobulin (Ig) repeats that participate in cell adhesion and signaling. Here, we describe their role in kin discrimination. We show that lagB1 and lagC1 are highly polymorphic in natural populations and that their sequence dissimilarity correlates well with wild-strain segregation. Deleting lagB1 and lagC1 results in strain segregation in chimeras with wild-type cells, whereas elimination of the nearly invariant homolog lagD1 has no such consequences. These findings reveal an early evolutionary origin of kin discrimination and provide insight into the mechanism of social recognition and immunity.
Project description:In all domains of life, mechanisms exist that protect cooperating groups from exploitation by cheaters. Recent observations with the bacterium Pseudomonas aeruginosa have suggested a paradigmatic cheater control mechanism in which cooperator cells punish or "police" cheater cells by cyanide poisoning. These cheater cells are deficient in a pleiotropic quorum-sensing regulator that controls the production of cooperative secretions including cyanide, and presumably also cyanide resistance. In this study, we directly tested and refuted the cyanide policing model. Contrary to the hypothesis, cheater fitness was unaffected by the presence of cyanide. Cheater mutants grew equally well in co-cultures with either cyanide-proficient or cyanide-deficient cooperators, and they were as resistant to exogenous cyanide as wild-type cells. We show that these behaviors are the result of quorum-sensing-independent and cyanide-responsive resistance gene regulation. Our results highlight the role of genetic architecture in the evolution of cooperative behavior.
Project description:Cheaters disrupt cooperation by reaping the benefits without paying their fair share of associated costs. Cheater impact can be diminished if cooperators display a tag ('greenbeard') and recognise and preferentially direct cooperation towards other tag carriers. Despite its popular appeal, the feasibility of such greenbeards has been questioned because the complex patterns of partner-specific cooperative behaviours seen in nature require greenbeards to come in different colours. Here we show that a locus ('Tgr') of a social amoeba represents a polychromatic greenbeard. Patterns of natural Tgr locus sequence polymorphisms predict partner-specific patterns of cooperation by underlying variation in partner-specific protein-protein binding strength and recognition specificity. Finally, Tgr locus polymorphisms increase fitness because they help avoid potential costs of cooperating with incompatible partners. These results suggest that a polychromatic greenbeard can provide a key mechanism for the evolutionary maintenance of cooperation.