Frequency dependence and cooperation: theory and a test with bacteria

Hamilton's inclusive fitness theory provides a leading explanation for the problem of cooperation. A general result from inclusive fitness theory is that, except under restrictive conditions, cooperation should not be subject to frequency-dependent selection. However, several recent studies in microbial systems have demonstrated that the relative fitness of cheaters, which do not cooperate, is greater when cheaters are rarer. Here we demonstrate theoretically that such frequency-dependent selection can occur in microbes when there is (1) sufficient population structuring or (2) an association between the level of cooperation and total population growth. We test prediction (2) and its underlying assumption, using the pathogenic bacterium Pseudomonas aeruginosa, by competing strains that produce iron-scavenging siderophore molecules (cooperators) with nonproducers (cheaters) at various ratios, under conditions that minimize population structuring. We found that both the relative fitness of cheaters and the productivity of the mixed culture were significantly negatively related to initial cheater frequency. Furthermore, when the period of population growth was experimentally shortened, the strength of frequency dependence was reduced. More generally, we argue that frequency-dependent selection on cooperative traits may be more common in microbes than in metazoans because strong selection, structuring, and cooperation-dependent growth will be more common in microbial populations.     

The public and private benefit of an impure public good determines the sensitivity of bacteria to population collapse in a snowdrift game

When cooperation is critical for survival, cheating can lead to population collapse. One mechanism of cooperation that permits the coexistence of cooperators and cheaters is an impure public good, whose public benefits are shared, but with a private benefit retained by the cooperator. It has yet to be determined how the contributions of the public and private benefit affect population survival. Using simulations and experiments with β-lactamase-expressing bacteria, we found that for a given amount of public and private benefit, the population was most sensitive to collapse when initiated from an intermediate fraction of cooperators due to the near-concurrent collapse of the cooperator and cheater populations. We found that increasing the ratio of public to private benefit increased sensitivity to collapse. A low ratio allowed cooperators to survive on their private benefit after the public benefit could not rescue the cheaters. A high ratio allowed the cheaters to survive to high concentrations of ampicillin due to the high public benefit. However, small increases in ampicillin caused a rapid decline in the entire population as the private benefit was insufficient to allow self-rescue of the cooperators. Our findings have implications in the persistence of populations that rely on cooperation for survival.     

Population dynamics of microbial cross-feeding are determined by co-localization probabilities and cooperation-independent cheater growth

As natural selection acts on individual organisms the evolution of costly cooperation between microorganisms is an intriguing phenomenon. Introduction of spatial structure to privatize exchanged molecules can explain the evolution of cooperation. However, in many natural systems cells can also grow to low cell concentrations in the absence of these exchanged molecules, thus showing “cooperation-independent background growth”. We here serially propagated a synthetic cross-feeding consortium of lactococci in the droplets of a water-in-oil emulsion, essentially mimicking group selection with varying founder population sizes. The results show that when the growth of cheaters completely depends on cooperators, cooperators outcompete cheaters. However, cheaters outcompete cooperators when they can independently grow to only ten percent of the consortium carrying capacity. This result is the consequence of a probabilistic effect, as low founder population sizes in droplets decrease the frequency of cooperator co-localization. Cooperator-enrichment can be recovered by increasing the founder population size in droplets to intermediate values. Together with mathematical modelling our results suggest that co-localization probabilities in a spatially structured environment leave a small window of opportunity for the evolution of cooperation between organisms that do not benefit from their cooperative trait when in isolation or form multispecies aggregates.Subject terms: Community ecology, Microbial ecology, Evolution, Microbial ecology     

Concurrent coevolution of intra‐organismal cheaters and resisters

The evolution of multicellularity is a major transition that is not yet fully understood. Specifically, we do not know whether there are any mechanisms by which multicellularity can be maintained without a single‐cell bottleneck or other relatedness‐enhancing mechanisms. Under low relatedness, cheaters can evolve that benefit from the altruistic behaviour of others without themselves sacrificing. If these are obligate cheaters, incapable of cooperating, their spread can lead to the demise of multicellularity. One possibility, however, is that cooperators can evolve resistance to cheaters. We tested this idea in a facultatively multicellular social amoeba, Dictyostelium discoideum. This amoeba usually exists as a single cell but, when stressed, thousands of cells aggregate to form a multicellular organism in which some of the cells sacrifice for the good of others. We used lineages that had undergone experimental evolution at very low relatedness, during which time obligate cheaters evolved. Unlike earlier experiments, which found resistance to cheaters that were prevented from evolving, we competed cheaters and noncheaters that evolved together, and cheaters with their ancestors. We found that noncheaters can evolve resistance to cheating before cheating sweeps through the population and multicellularity is lost. Our results provide insight into cheater–resister coevolutionary dynamics, in turn providing experimental evidence for the maintenance of at least a simple form of multicellularity by means other than high relatedness.     

The good, the bad, and the rare: memory for partners in social interactions

For cooperation to evolve via direct reciprocity, individuals must track their partners' behavior to avoid exploitation. With increasing size of the interaction group, however, memory becomes error prone. To decrease memory effort, people could categorize partners into types, distinguishing cooperators and cheaters. We explored two ways in which people might preferentially track one partner type: remember cheaters or remember the rare type in the population. We assigned participants to one of three interaction groups which differed in the proportion of computer partners' types (defectors rare, equal proportion, or cooperators rare). We extended research on both hypotheses in two ways. First, participants experienced their partners repeatedly by interacting in Prisoner's Dilemma games. Second, we tested categorization of partners as cooperators or defectors in memory tests after a short and long retention interval (10 min and 1 week). Participants remembered rare partner types better than they remembered common ones at both retention intervals. We propose that the flexibility of responding to the environment suggests an ecologically rational memory strategy in social interactions.     

Microbial Communication,Cooperation and Cheating: Quorum Sensing Drives the Evolution of Cooperation in Bacteria

An increasing body of empirical evidence suggests that cooperation among clone-mates is common in bacteria. Bacterial cooperation may take the form of the excretion of “public goods”: exoproducts such as virulence factors, exoenzymes or components of the matrix in biofilms, to yield significant benefit for individuals joining in the common effort of producing them. Supposedly in order to spare unnecessary costs when the population is too sparse to supply the sufficient exoproduct level, many bacteria have evolved a simple chemical communication system called quorum sensing (QS), to “measure” the population density of clone-mates in their close neighborhood. Cooperation genes are expressed only above a threshold rate of QS signal molecule re-capture, i.e., above the local quorum of cooperators. The cooperative population is exposed to exploitation by cheaters, i.e., mutants who contribute less or nil to the effort but fully enjoy the benefits of cooperation. The communication system is also vulnerable to a different type of cheaters (“Liars”) who may produce the QS signal but not the exoproduct, thus ruining the reliability of the signal. Since there is no reason to assume that such cheaters cannot evolve and invade the populations of honestly signaling cooperators, the empirical fact of the existence of both bacterial cooperation and the associated QS communication system seems puzzling. Using a stochastic cellular automaton approach and allowing mutations in an initially non-cooperating, non-communicating strain we show that both cooperation and the associated communication system can evolve, spread and remain persistent. The QS genes help cooperative behavior to invade the population, and vice versa; cooperation and communication might have evolved synergistically in bacteria. Moreover, in good agreement with the empirical data recently available, this synergism opens up a remarkably rich repertoire of social interactions in which cheating and exploitation are commonplace.     

Understanding policing as a mechanism of cheater control in cooperating bacteria

Policing occurs in insect, animal and human societies, where it evolved as a mechanism maintaining cooperation. Recently, it has been suggested that policing might even be relevant in enforcing cooperation in much simpler organisms such as bacteria. Here, we used individual‐based modelling to develop an evolutionary concept for policing in bacteria and identify the conditions under which it can be adaptive. We modelled interactions between cooperators, producing a beneficial public good, cheaters, exploiting the public good without contributing to it, and public good‐producing policers that secrete a toxin to selectively target cheaters. We found that toxin‐mediated policing is favoured when (a) toxins are potent and durable, (b) toxins are cheap to produce, (c) cell and public good diffusion is intermediate, and (d) toxins diffuse farther than the public good. Although our simulations identify the parameter space where toxin‐mediated policing can evolve, we further found that policing decays when the genetic linkage between public good and toxin production breaks. This is because policing is itself a public good, offering protection to toxin‐resistant mutants that still produce public goods, yet no longer invest in toxins. Our work thus highlights that not only specific environmental conditions are required for toxin‐mediated policing to evolve, but also strong genetic linkage between the expression of public goods, toxins and toxin resistance is essential for this mechanism to remain evolutionarily stable in the long run.     

从合作的进化探讨植物与传粉者的相互作用

合作的进化为研究植物–传粉者相互关系提供了新的视角。植物与传粉者通过"报酬换服务"建立种间合作关系。这一合作关系从建立、维持到解体面临着3个关键问题:(1)在植物和传粉者不了解对方质量信息时,双方如何选择出最适伙伴,进而建立合作关系;(2)合作方如何限制欺骗策略(比如,盗蜜和欺骗性传粉)的扩散以维持合作关系;(3)什么过程可导致传粉合作关系的解体。植物与传粉者间信号博弈或筛选博弈可促进二者合作关系的建立。面对欺骗策略,传粉者和植物分别采用伙伴选择机制和防御机制加以应对。合作者与欺骗者的稳定共存也有助于植物–传粉者合作的维持。从合作转向对抗、转向新的伙伴和合作放弃3个过程可导致植物–传粉者的合作关系的解体。植物与传粉者合作关系的理论预期已经得到了部分实验结果支持,深化了我们对植物与传粉者合作过程中关键机制的理解。在今后的研究中,需要进一步探讨以下问题:(1)传粉者对植物信号诚实性的选择作用和植物对传粉者的筛选作用;(2)植物与传粉者各自应对欺骗策略的可能机制及其相对重要性;(3)合作者与欺骗者稳定共存的机制;(4)植物与传粉者合作系统对全球变化的响应。     

Spatial Structure Facilitates Cooperation in a Social Dilemma: Empirical Evidence from a Bacterial Community

Cooperative organisms are ubiquitous in nature, despite their vulnerability to exploitation by cheaters. Although numerous theoretical studies suggest that spatial structure is critical for cooperation to persist, the spatial ecology of microbial cooperation remains largely unexplored experimentally. By tracking the community dynamics of cooperating (rpoS wild-type) and cheating (rpoS mutant) Escherichia coli in well-mixed flasks and microfabricated habitats, we demonstrate that spatial structure stabilizes coexistence between wild-type and mutant and thus facilitates cooperator maintenance. We develop a method to interpret our experimental results in the context of game theory, and show that the game wild-type and mutant bacteria play in an unstructured environment changes markedly over time, and eventually obeys a prisoner’s dilemma leading to cheater dominance. In contrast, when wild-type and mutant E. coli co-inhabit a spatially-structured habitat, cooperators and cheaters coexist at intermediate frequencies. Our findings show that even in microhabitats lacking patchiness or spatial heterogeneities in resource availability, surface growth allows cells to form multi-cellular aggregates, yielding a self-structured community in which cooperators persist.     

Evolutionary Dynamics of Nitrogen Fixation in the Legume–Rhizobia Symbiosis

The stabilization of host–symbiont mutualism against the emergence of parasitic individuals is pivotal to the evolution of cooperation. One of the most famous symbioses occurs between legumes and their colonizing rhizobia, in which rhizobia extract nutrients (or benefits) from legume plants while supplying them with nitrogen resources produced by nitrogen fixation (or costs). Natural environments, however, are widely populated by ineffective rhizobia that extract benefits without paying costs and thus proliferate more efficiently than nitrogen-fixing cooperators. How and why this mutualism becomes stabilized and evolutionarily persists has been extensively discussed. To better understand the evolutionary dynamics of this symbiosis system, we construct a simple model based on the continuous snowdrift game with multiple interacting players. We investigate the model using adaptive dynamics and numerical simulations. We find that symbiotic evolution depends on the cost–benefit balance, and that cheaters widely emerge when the cost and benefit are similar in strength. In this scenario, the persistence of the symbiotic system is compatible with the presence of cheaters. This result suggests that the symbiotic relationship is robust to the emergence of cheaters, and may explain the prevalence of cheating rhizobia in nature. In addition, various stabilizing mechanisms, such as partner fidelity feedback, partner choice, and host sanction, can reinforce the symbiotic relationship by affecting the fitness of symbionts in various ways. This result suggests that the symbiotic relationship is cooperatively stabilized by various mechanisms. In addition, mixed nodule populations are thought to encourage cheater emergence, but our model predicts that, in certain situations, cheaters can disappear from such populations. These findings provide a theoretical basis of the evolutionary dynamics of legume–rhizobia symbioses, which is extendable to other single-host, multiple-colonizer systems.     

Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus

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.     

Resource abundance and the critical transition to cooperation

Cooperation is abundant in nature, occurring at all levels of biological complexity. Yet cooperation is continually threatened by subversion from noncooperating cheaters. Previous studies have shown that cooperation can nevertheless be maintained when the benefits that cooperation provides to relatives outweigh the associated costs. These fitness costs and benefits are not fixed properties, but can be affected by the environment in which populations reside. Here, we describe how one environmental factor, resource abundance, decisively affects the evolution of cooperative public goods production in two independent evolving systems. In the Avida digital evolution platform, populations evolved in environments with different levels of a required resource, whereas populations of Vibrio cholerae evolved in the presence of different nutrient concentrations. In both systems, cooperators and cheaters co‐existed stably in resource‐rich environments, whereas cheaters dominated in resource‐poor environments. These two outcomes were separated by a sharp transition that occurred at a critical level of resource. These results offer new insights into how the environment affects the evolution of cooperation and highlight the challenges that populations of cooperators face when they experience environmental change.     

Cooperation and cheating in microbial exoenzyme production – Theoretical analysis for biotechnological applications

The engineering of microorganisms to produce a variety of extracellular enzymes (exoenzymes), for example for producing renewable fuels and in biodegradation of xenobiotics, has recently attracted increasing interest. Productivity is often reduced by “cheater” mutants, which are deficient in exoenzyme production and benefit from the product provided by the “cooperating” cells. We present a game-theoretical model to analyze population structure and exoenzyme productivity in terms of biotechnologically relevant parameters. For any given population density, three distinct regimes are predicted: when the metabolic effort for exoenzyme production and secretion is low, all cells cooperate; at intermediate metabolic costs, cooperators and cheaters coexist; while at high costs, all cells use the cheating strategy. These regimes correspond to the harmony game, snowdrift game, and Prisoner's Dilemma, respectively. Thus, our results indicate that microbial strains engineered for exoenzyme production will not, under appropriate conditions, be outcompeted by cheater mutants. We also analyze the dependence of the population structure on cell density. At low costs, the fraction of cooperating cells increases with decreasing cell density and reaches unity at a critical threshold. Our model provides an estimate of the cell density maximizing exoenzyme production.     

Cooperation as a volunteer’s dilemma and the strategy of conflict in public goods games

Conflict and cooperation for the exploitation of public goods are usually modelled as an N‐person prisoner’s dilemma. Many social dilemmas, however, would be described more properly as a volunteer’s dilemma, in which a certain number of individuals are necessary to produce a public good. If volunteering is costly, but so is failure to produce the public good, cheaters can invade and form a stable mixed equilibrium with cooperators. The dilemma is that the benefit for the group decreases with group size because the larger the group is, the less likely it is that someone volunteers. This problem persists even in the presence of a high degree of relatedness between group members. This model provides precise, testable predictions for the stability of cooperation. It also suggests a counterintuitive but practical solution for this kind of social dilemmas: increasing the damage resulting from the failure to produce the public good increases the probability that the public good is actually produced. Adopting a strategy that entails a deliberate risk (brinkmanship), therefore, can lead to a benefit for the society without being detrimental for the individual.     

Sociobiology of biodegradation and the role of predatory protozoa in biodegrading communities

Predatory protozoa are known to enhance biodegradation by bacteria in a variety of systems including rumen. This is apparently counterintuitive since many protozoa do not themselves produce extracellular degradative enzymes and prey upon bacterial degraders. We propose a mechanism of protozoal enhancement of bacterial biodegradation based on the sociobiology of biodegradation. Since extracellular enzyme production by degraders involves a cost to the bacterial cell, cheaters that do not make the enzyme will have a selective advantage. In the presence of cheaters, degraders that physically attach to water-insoluble substrate will have a selective advantage over free-floating degraders. On the other hand, cheaters will benefit by being free floaters since they consume the solubilized products of extracellular enzymes. Predatory ciliated protozoa are more likely to consume free-floating cheaters. Thus, due to protozoan predation a control is exerted on the cheater population. We illustrate the dynamics of such a system with the help of a computer simulation model. Available data on rumen and other biodegradation systems involving protozoa are compatible with the assumptions and predictions of the model.     

细菌群体感应“合作-欺骗”研究进展

细菌利用信号分子进行细胞间的交流即为群体感应.群体感应调控着生物膜形成、公共物质合成、基因水平转移等一系列社会性行为.在群体感应过程中,公共物质分泌后可以被群体中任何个体所使用即合作;亦可以被一些不分泌公共物质的个体所使用形成欺骗.群体感应合作-欺骗既可能在种群中稳定维持,也可能由于欺骗子的快速增长造成种群崩溃.欺骗子致种群崩溃为病原菌控制新策略研发带来了希望,是目前群体感应研究方面的前沿和热点.本文在介绍细菌群体感应合作及欺骗的基础上,分析了群体感应合作-欺骗生态关系形成和发展的影响因素,重点从亲缘选择、谨慎代谢、代谢限制(基因多效型)、群体感应监管等方面探讨了细菌群体感应合作-欺骗的稳定维持机制,并对细菌群体感应合作-欺骗的相关研究进行了问题总结和展望,以期为深入理解群体感应、微生物种群生态提供参考.     

Testing the out-of-Florida hypothesis on the origin of cheating in the yucca-yucca moth mutualism

Mutualistic interactions can be exploited by cheaters that take the rewards offered by mutualists without providing services in return. The evolution of cheater species from mutualist ancestors is thought to be possible under particular ecological conditions. Here we provide a test of the first explicit model of the transition from mutualism to antagonism. We used the obligate pollination mutualism between yuccas and yucca moths to examine the origins of a nonpollinating cheater moth, Tegeticula intermedia, and its pollinating sister species, T. cassandra. Based on geographic distribution and ecological factors affecting the pollinators, previous research had indicated that the cheaters evolved in Florida as a result of sympatry of T. cassandra and another pollinator species. We used mitochondrial DNA (mtDNA) sequences and amplified fragment length polymorphism (AFLP) data to investigate the phylogeographic history of the pollinator-cheater sister pair and to test whether the cheaters arose in Florida. Contrary to predictions, phylogenetic and population genetic analyses suggested that the cheaters evolved in the western United States and subsequently spread eastward. Western populations of cheaters had the most ancestral haplotypes and the highest genetic diversity, and there was also significant genetic structure associated with a geographic split between eastern and western populations. In comparison, there was evidence for weak genetic structure between northern and southern pollinator populations, suggesting a long history in Florida. The western origin of the cheaters indicated that the pollinators have more recently become restricted to the southeastern United States. This was supported by AFLP analyses that indicated that the pollinators were more closely related to the western cheaters than they were to geographically proximate cheaters in the east. Shared mtDNA between pollinators and eastern cheaters suggested hybridization, possibly in a secondary contact zone. The results negate the out-of-Florida hypothesis and reveal instead a long, complex, and disparate history for the pollinator-cheater sister pair.     

Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

Reproduction is one of the requirements for evolution and a defining feature of life. Yet, across the tree of life, organisms reproduce in many different ways. Groups of cells (e.g., multicellular organisms, colonial microbes, or multispecies biofilms) divide by releasing propagules that can be single-celled or multicellular. What conditions determine the number and size of reproductive propagules? In multicellular organisms, existing theory suggests that single-cell propagules prevent the accumulation of deleterious mutations (e.g., cheaters). However, groups of cells, such as biofilms, sometimes contain multiple metabolically interdependent species. This creates a reproductive dilemma: small daughter groups, which prevent the accumulation of cheaters, are also unlikely to contain the species diversity that is required for ecological success. Here, we developed an individual-based, multilevel selection model to investigate how such multi-species groups can resolve this dilemma. By tracking the dynamics of groups of cells that reproduce by fragmenting into smaller groups, we identified fragmentation modes that can maintain cooperative interactions. We systematically varied the fragmentation mode and calculated the maximum mutation rate that communities can withstand before being driven to extinction by the accumulation of cheaters. We find that for groups consisting of a single species, the optimal fragmentation mode consists of releasing single-cell propagules. For multi-species groups we find various optimal strategies. With migration between groups, single-cell propagules are favored. Without migration, larger propagules sizes are optimal; in this case, group-size dependent fissioning rates can prevent the accumulation of cheaters. Our work shows that multi-species groups can evolve reproductive strategies that allow them to maintain cooperative interactions.     

Cost of cooperation rules selection for cheats in bacterial metapopulations

Bacteria secrete a large variety of beneficial metabolites into the environment, which can be shared as public goods among producing bacteria, but also be exploited by nonproducing cheats. Here, we focus on cooperative production of iron-chelating molecules (siderophores) in the bacterium Pseudomonas aeruginosa to study how relevant ecological factors influence selection for cheating. We designed patch-structured metapopulations that allowed us introducing among-patch ecological variation. We found that cheating readily evolved in uniform iron-limited environments. This finding is explained by severe iron limitation demanding high siderophore-production efforts, which results in high metabolic costs accruing to cooperators, and thereby facilitates the spread of cheats. In contrast, we observed a significant reduction or even negation of selection for cheating in metapopulations where we introduced patches with increased iron availability and/or opportunities to recycle siderophores. These findings are compatible with the view that cheats are less likely to invade in environments that allow bacteria to reduce siderophore-production efforts, as this lowers the overall metabolic costs accruing to cooperators. Because we increased iron availability and siderophore recycling opportunities moderately, and only in some patches, our findings demonstrate that already-small local variations in ecological conditions as occurring in nature can significantly affect selection for public-goods secretion in microbes. In addition, we found that most (84.6%) of the evolved cheats were partially deficient for siderophore production and not loss-of-function mutants. Genetic considerations indicate that mutations leading to partial deficiency occur more frequent than mutations leading to loss of function, but also suggest that partially deficient mutants might often be the more competitive cheats.     

On the limits of interpreting some plastic responses through a cooperator/cheater prism. A comment on Harrison

Micro‐organisms are known to exhibit phenotypic plasticity in response to changes in their environment. Recent studies have shown that a parasite strain can adjust its host exploitation strategies to the presence of unrelated strains, e.g. for Plasmodium chabaudi by adjusting its sex‐ratio. J. Evol. Biol. 2013; 26 : 1370–1378 claims to report a similar plastic response to the presence of unrelated strains in the case of siderophore‐producing bacteria. I argue that she does not provide sufficient evidence to support the interpretation of the plastic response she observes (increasing siderophore production in the presence of cheaters) through a cooperator/cheater framework. I show that known plastic responses to physicochemical factors, such as siderophore or iron concentration, seem to offer a clearer and more parsimonious explanation. Finally, I also challenge the parallel she makes between the process she observes in siderophore‐producing bacteria and compensation in bi‐parental care models.