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Microbial cooperation typically consists in the sharing of secreted metabolites (referred to as public goods) within the community. Although public goods generally promote population growth, they are also vulnerable to exploitation by cheating mutants, which no longer contribute, but still benefit from the public goods produced by others. Although previous studies have identified a number of key factors that prevent the spreading of cheaters, little is known about how these factors interact and jointly shape the evolution of microbial cooperation. Here, we address this issue by investigating the interaction effects of cell diffusion, cell density, public good diffusion and durability (factors known to individually influence costs and benefits of public goods production) on selection for cooperation. To be able to quantify these effects across a wide parameter space, we developed an individual-based simulation platform, consisting of digital cooperator and cheater bacteria inhabiting a finite two-dimensional continuous toroidal surface. Our simulations, which closely mimic microbial microcolony growth, revealed that: (i) either reduced cell diffusion (which keeps cooperators together) or reduced public good diffusion (which keeps the public goods closer to the producer) is not only essential but also sufficient for cooperation to be promoted; (ii) the sign of selection for or against cooperation can change as a function of cell density and in interaction with diffusion parameters; and (iii) increased public goods durability has opposing effects on the evolution of cooperation depending on the level of cell and public good diffusion. Our work highlights that interactions between key parameters of public goods cooperation give rise to complex fitness landscapes, a finding that calls for multifactorial approaches when studying microbial cooperation in natural systems.

How communication systems emerge and remain stable is an important question in both cognitive science and evolutionary biology. For communication to arise, not only must individuals cooperate by signaling reliable information, but they must also coordinate and perpetuate signals. Most studies on the emergence of communication in humans typically consider scenarios where individuals implicitly share the same interests. Likewise, most studies on human cooperation consider scenarios where shared conventions of signals and meanings cannot be developed de novo. Here, we combined both approaches with an economic experiment where participants could develop a common language, but under different conditions fostering or hindering cooperation. Participants endeavored to acquire a resource through a learning task in a computer-based environment. After this task, participants had the option to transmit a signal (a color) to a fellow group member, who would subsequently play the same learning task. We varied the way participants competed with each other (either global scale or local scale) and the cost of transmitting a signal (either costly or noncostly) and tracked the way in which signals were used as communication among players. Under global competition, players signaled more often and more consistently, scored higher individual payoffs, and established shared associations of signals and meanings. In addition, costly signals were also more likely to be used under global competition; whereas under local competition, fewer signals were sent and no effective communication system was developed. Our results demonstrate that communication involves both a coordination and a cooperative dilemma and show the importance of studying language evolution under different conditions influencing human cooperation.

Bacteria frequently exhibit cooperative behaviors but cooperative strains are vulnerable to invasion by cheater strains that reap the benefits of cooperation but do not perform the cooperative behavior themselves. Bacterial genomes often contain mobile genetic elements such as plasmids. When a gene for cooperative behavior exists on a plasmid, cheaters can be forced to cooperate by infection with this plasmid, rescuing cooperation in a population in which mutation or migration has allowed cheaters to arise. Here we introduce a second plasmid that does not code for cooperation and show that the social dilemma repeats itself at the plasmid level in both within-patch and metapopulation scenarios, and under various scenarios of plasmid incompatibility. Our results suggest that although plasmid carriage of cooperative genes can provide a transient defense against defection in structured environments, plasmid and chromosomal defection remain the only stable strategies in an unstructured environment. We discuss our results in the light of recent bioinformatic evidence that cooperative genes are overrepresented on mobile elements.

Natural selection ultimately acts on genes and other DNA sequences. Adaptations that are good for the gene can have adverse effects at higher levels of organization, including the individual or the population. Mobile genetic elements illustrate this principle well, because they can self-replicate within a genome at a cost to their host. As they are costly and can be transmitted horizontally, mobile elements can be seen as genomic parasites. It has been suggested that mobile elements may cause the extinction of their host populations. In organisms with very large populations, such as most bacteria, individual selection is highly effective in purging genomes of deleterious elements, suggesting that extinction is unlikely. Here we investigate the conditions under which mobile DNA can drive bacterial lineages to extinction. We use a range of epidemiological and ecological models to show that harmful mobile DNA can invade, and drive populations to extinction, provided their transmission rate is high and that mobile element-induced mortality is not too high. Population extinction becomes more likely when there are more elements in the population. Even if elements are costly, extinction can still occur because of the combined effect of horizontal gene transfer, a mortality induced by mobile elements. Our study highlights the potential of mobile DNA to be selected at the population level, as well as at the individual level.

Background Microbes engage in a remarkable array of cooperative behaviors, secreting shared proteins that are essential for foraging, shelter, microbial warfare, and virulence. These proteins are costly, rendering populations of cooperators vulnerable to exploitation by nonproducing cheaters arising by gene loss or migration. In such conditions, how can cooperation persist? Results Our model predicts that differential gene mobility drives intragenomic variation in investment in cooperative traits. More mobile loci generate stronger among-individual genetic correlations at these loci (higher relatedness) and thereby allow the maintenance of more cooperative traits via kin selection. By analyzing 21 Escherichia genomes, we confirm that genes coding for secreted proteins-the secretome-are very frequently lost and gained and are associated with mobile elements. We show that homologs of the secretome are overrepresented among human gut metagenomics samples, consistent with increased relatedness at secretome loci across multiple species. The biosynthetic cost of secreted proteins is shown to be under intense selective pressure, even more than for highly expressed proteins, consistent with a cost of cooperation driving social dilemmas. Finally, we demonstrate that mobile elements are in conflict with their chromosomal hosts over the chimeric ensemble's social strategy, with mobile elements enforcing cooperation on their otherwise selfish hosts via the cotransfer of secretome genes with "mafia strategy" addictive systems (toxin-antitoxin and restriction-modification). Conclusion Our analysis matches the predictions of our model suggesting that horizontal transfer promotes cooperation, as transmission increases local genetic relatedness at mobile loci and enforces cooperation on the resident genes. As a consequence, horizontal transfer promoted by agents such as plasmids, phages, or integrons drives microbial cooperation.

The population consequences of sexual selection remain empirically unexplored. Comparative studies, involving extinction risk, have yielded different results as to the effect of sexual selection on population densities make contrasting predictions. Here, we investigate the relationship between sexual dimorphism (SD) and population productivity in the seed beetle Callosobruchus maculatus, using 13 populations that have evolved in isolation. Geometric morphometric methods and image analysis are employed to form integrative measures of sexual dimorphism, composed of variation in weight, size, body shape, and pigmentation. We found a positive relationship between SD and adult fitness (net adult offspring production) across our study populations, but failed to find any association between SD and juvenile fitness (egg-to-adult survival). Several mechanisms may have contributed to the pattern found, and variance in sexual selection regimes across populations, either in female choice for "good genes" or in the magnitude of direct benefits provided by their mates, would tend to produce the pattern seen. However, our results suggest that evolutionary constraints in the form of intralocus sexual conflict may have been the major generator of the relationship seen between SD and population fitness.

The twofold cost of sex implies that sexual and asexual reproduction do not coexist easily. Asexual forms tend to outcompete sexuals but may eventually suffer higher extinction rates, creating tension between short- and long-term advantages of different reproductive modes. The ‘short-sightedness’ of asexual reproduction takes a particularly intriguing form in gynogenetic species complexes, in which an asexual species requires sperm from a related sexual host species to trigger embryogenesis. Asexuals are then predicted to outcompete their host, after which neither species can persist. We examine whether spatial structure can explain continued coexistence of the species complex, and assess the evidence based on data on the Amazon molly (Poecilia formosa). A modification of the Levins metapopulation model creates two regions of good prospects for coexistence, connected by a region of poorer patch occupancy levels. In the first case, mate discrimination and/or niche differentiation keep local extinction rates low, and most patches contain both species; the other possibility resembles host–parasite dynamics where parasites frequently drive the host locally extinct. Several dynamical features are counterintuitive and relate to the parasitic nature of interactions in the species complex: for example, high local extinction rates of the asexual species can be beneficial for its own persistence. This creates a link from the evolution of sexual reproduction to that of prudent predation.

Quarantine is one possible solution to limit the propagation of an emerging infectious disease. Typically, infected individuals are removed from the population by avoiding physical contact with healthy individuals. A key factor for the success of a quarantine strategy is the carrying capacity of the facility. This is often a known parameter, while other parameters such as those defining the population structure are more difficult to assess. Here we develop a model where we explicitly introduce the carrying capacity of the quarantine facility into a susceptible–infected–recovered (SIR) framework. We show how the model can address the propagation and control of contact and sexually transmitted infections. We illustrate this by a case study of the city of Zurich during the 16th century, when it had to face an epidemic of syphilis. After Swiss mercenaries came back from a war in Naples in 1495, the authorities of the city addressed subsequent epidemics by, among others, placing infected members of the population in quarantine. Our results suggest that a modestly sized quarantine facility can successfully prevent or reduce an epidemic. However, false detection can present a real impediment for this solution. Indiscriminate quarantine of individuals can lead to the overfilling of the facility, and prevent the intake of infected individuals. This results in the failure of the quarantine policy. Hence, improving the rate of true over false detection becomes the key factor for quarantine strategies. Moreover, in the case of sexually transmitted infections, asymmetries in the male to female ratio, and the force of infection pertaining to each sex and class of sexual encounter can alter the effectiveness of quarantine measures. For example, a heterosexually transmitted disease that mainly affects one sex is harder to control in a population with more individuals of the opposite sex. Hence an imbalance in the sex ratios as seen in situations such as mining colonies, or populations at war, can present impediments for the success of quarantine policies.

Bacterial genomes commonly contain ‘addiction’ gene complexes that code for both a toxin and a corresponding antitoxin. As long as both genes are expressed, cells carrying the complex can remain healthy. However, loss of the complex (including segregational loss in daughter cells) can entail death of the cell. We develop a theoretical model to explore a number of evolutionary puzzles posed by toxin–antitoxin (TA) population biology. We first extend earlier results demonstrating that TA complexes can spread on plasmids, as an adaptation to plasmid competition in spatially structured environments, and highlight the role of kin selection. We then considered the emergence of TA complexes on plasmids from previously unlinked toxin and antitoxin genes. We find that one of these traits must offer at least initially a direct advantage in some but not all environments encountered by the evolving plasmid population. Finally, our study predicts non-transitive ‘rock-paper-scissors’ dynamics to be a feature of intragenomic conflict mediated by TA complexes. Intragenomic conflict could be sufficient to select deleterious genes on chromosomes and helps to explain the previously perplexing observation that many TA genes are found on bacterial chromosomes.

It has recently been proposed that mobile elements may be a significant driver of cooperation in microorganisms. This may drive a potential conflict, where cooperative genes are transmitted independently of the rest of the genome, resulting in scenarios where horizontally spread cooperative genes are favored, whereas a chromosomal equivalent would not be. This can lead to the whole genome being exploited by surrounding noncooperative individuals. Given that there are costs associated with mobile elements themselves, infection with a plasmid carrying a cooperative trait may lead to a significant conflict within the host genome. Here, we model the mechanisms that allow the host to resolve this conflict, either by exhibiting complete resistance to the mobile element or by controlling its gene expression via a chromosomally based suppressor. We find that the gene suppression mechanism will be more stable than full resistance, implying that suppressing the expression of costly genes within a cell is preferable to preventing the acquisition of the mobile element, for the resolution of conflict within a genome.

Multicellular differentiated organisms are composed of cells that begin by developing from a single pluripotent germ cell. In many organisms, a proportion of cells differentiate into specialized somatic cells. Whether these cells lose their pluripotency or are able to reverse their differentiated state has important consequences. Reversibly differentiated cells can potentially regenerate parts of an organism and allow reproduction through fragmentation. In many organisms, however, somatic differentiation is terminal, thereby restricting the developmental paths to reproduction. The reason why terminal differentiation is a common developmental strategy remains unexplored. To understand the conditions that affect the evolution of terminal versus reversible differentiation, we developed a computational model inspired by differentiating cyanobacteria. We simulated the evolution of a population of two cell types –nitrogen fixing or photosynthetic– that exchange resources. The traits that control differentiation rates between cell types are allowed to evolve in the model. Although the topology of cell interactions and differentiation costs play a role in the evolution of terminal and reversible differentiation, the most important factor is the difference in division rates between cell types. Faster dividing cells always evolve to become the germ line. Our results explain why most multicellular differentiated cyanobacteria have terminally differentiated cells, while some have reversibly differentiated cells. We further observed that symbioses involving two cooperating lineages can evolve under conditions where aggregate size, connectivity, and differentiation costs are high. This may explain why plants engage in symbiotic interactions with diazotrophic bacteria., Author Summary The evolution of multicellularity is one of the most fascinating topics of evolutionary biology. Without multicellularity the incredible diversity of extant life would not be possible. In many multicellular organisms with specialized cells, some cell types become terminally differentiated (somatic cells) and lose the ability to reproduce new organisms while other cells maintain this ability (germline). Little is known about the conditions that favor the evolution of terminal differentiation in multicellular organisms. To understand this problem we have developed a computational model, inspired by multicellular cyanobacteria, in which the cells in an organism composed of two cell types (photosynthetic and nitrogen fixing) are allowed to evolve from germline to soma cells. We find three striking results. First, faster dividing cell types always evolve to become the germline. Second, the conditions under which we find different outcomes from the model are in good agreement with the different forms of development observed in multicellular cyanobacteria. Third, some conditions lead to a symbiotic state in which the two cell types separate into different lineages evolving independently of one another. Remarkably, cyanobacteria are also known to engage in symbiotic relationships with plants, producing fixed nitrogen for the plant in exchange for carbohydrates.

It is widely understood that the costs and benefits of mating can affect the fecundity and survival of individuals. Sexual conflict may have profound consequences for populations as a result of the negative effects it causes males and females to have on one another's fitness. Here we present a model describing the evolution of sexual conflict, in which males inflict a direct cost on female fitness. We show that these costs can drive the entire population to extinction. To males, females are an essential but finite resource over which they have to compete. Population extinction owing to sexual conflict can therefore be seen as an evolutionary tragedy of the commons. Our model shows that a positive feedback between harassment and the operational sex ratio is responsible for the demise of females and, thus, for population extinction. We further show that the evolution of female resistance to counter harassment can prevent a tragedy of the commons. Our findings not only demonstrate that sexual conflict can drive a population to extinction but also highlight how simple mechanisms, such as harassment costs to males and females and the coevolution between harassment and resistance, can help avert a tragedy of the commons caused by sexual conflict.

International audience; Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Punishment of non-cooperators has been observed to promote cooperation. Such punishment is an evolutionary puzzle because it is costly to the punisher while beneficial to others, for example, through increased social cohesion. Recent studies have concluded that punishing strategies usually pay less than some non-punishing strategies. These findings suggest that punishment could not have directly evolved to promote cooperation. However, while it is well established that reputation plays a key role in human cooperation, the simple threat from a reputation of being a punisher may not have been sufficiently explored yet in order to explain the evolution of costly punishment. Here, we first show analytically that punishment can lead to long-term benefits if it influences one's reputation and thereby makes the punisher more likely to receive help in future interactions. Then, in computer simulations, we incorporate up to 40 more complex strategies that use different kinds of reputations (e.g. from generous actions), or strategies that not only include punitive behaviours directed towards defectors but also towards cooperators for example. Our findings demonstrate that punishment can directly evolve through a simple reputation system. We conclude that reputation is crucial for the evolution of punishment by making a punisher more likely to receive help in future interactions, and that experiments investigating the beneficial effects of punishment in humans should include reputation as an explicit feature.

Costly punishment represents an evolutionary puzzle because it involves an individual paying a cost to harm another individual (1, 2). A recent study by Wu et al. (3) confirmed earlier conclusions (4) that costly punishment is mostly maladaptive and may have evolved for other reasons. We welcome their emphasis on cultural differences in experimental games (5), but we argue that these first tests (3, 4) are not yet conclusive with regard to the functional significance of costly punishment. There are three problems: (i) the definition of “defection” in their Prisoner's Dilemma is problematic for studies on punishment, (ii) a closer examination of their payoff matrices reveals them to be nonconducive to punishment, and (iii) their specific game structure imposes an additional opportunity cost that further reduces the effectiveness of punishment.

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.

Adaptation does not necessarily lead to traits which are optimal for the population. This is because selection is often the strongest at the individual or gene level. The evolution of selfishness can lead to a ‘tragedy of the commons’, where traits such as aggression or social cheating reduce population size and may lead to extinction. This suggests that species-level selection will result whenever species differ in the incentive to be selfish. We explore this idea in a simple model that combines individual-level selection with ecology in two interacting species. Our model is not influenced by kin or trait-group selection. We find that individual selection in combination with competitive exclusion greatly increases the likelihood that selfish species go extinct. A simple example of this would be a vertebrate species that invests heavily into squabbles over breeding sites, which is then excluded by a species that invests more into direct reproduction. A multispecies simulation shows that these extinctions result in communities containing species that are much less selfish. Our results suggest that species-level selection and community dynamics play an important role in regulating the intensity of conflicts in natural populations.

Competition and conflict among individuals can favour exploitative strategies that undermine the common good. Theory suggests that this can lead to a tragedy of the commons and ultimately population extinction, a phenomenon known as evolutionary suicide. Here, I present a model of the evolutionary tragedy of the commons that explicitly considers the population dynamics where individuals invest in individually costly competitive traits. In the simplest form, this supports the notion that selection for high levels of conflict can cause evolutionary suicide. However, as competition comes with survival and fecundity costs, a feedback between the investment in competition and population density can act to reduce the level of conflict and prevent the population from going extinct. This suggests that the interaction between population ecology and the evolution of competition and conflict among individuals may be an important mechanism in resolving the level of competition and conflict among individuals.

Models of population dynamics generally neglect the presence of males. While this assumption holds under many circumstances, behavioural ecology increasingly tells that the presence (or absence) of males may have an impact on female fitness, and hence population sizes. Here we ask the question of whether males matter to population dynamics, operationally defined as a dependency of population growth on the relative density of males. We provide simple models, and evaluate the current 8 empirical evidence for them, that illustrate various mechanisms of such male influence: mate searching behavior, male resource use (including effects of sexual dimorphism), sexual harassment and sexual segregation. In each case, theory predicts that males can have an effect on population densities, and in some extreme cases a positive feedback between an increasingly male-biased sex ratio and the effects on female harassment may theoretically even bring about population extinction. The results of this study, and the literature reviewed, show that the males can have a substantial effect on population dynamics, particularly so when human influences result in biased sex ratios.

The population consequences of sexual conflict are relatively unexplored. In a recent paper, Le Galliard et al. now show that males of the common lizard Lacerta vivipara cause such damage to females that male-biased populations decrease in size, posing a real risk to the persistence of local lizard populations. Their study reveals surprising parallels between sexual conflict and the tragedy of the commons, where selfish competition over females destroys the very resource (i.e. the females) over which the males are fighting.

Background Antibiotic resistance represents a significant public health problem. When resistance genes are mobile, being carried on plasmids or phages, their spread can be greatly accelerated. Plasmids in particular have been implicated in the spread of antibiotic resistance genes. However, the selective pressures which favour plasmid-carried resistance genes have not been fully established. Here we address this issue with mathematical models of plasmid dynamics in response to different antibiotic treatment regimes. Results We show that transmission of plasmids is a key factor influencing plasmid-borne antibiotic resistance, but the dosage and interval between treatments is also important. Our results also hold when plasmids carrying the resistance gene are in competition with other plasmids that do not carry the resistance gene. By altering the interval between antibiotic treatments, and the dosage of antibiotic, we show that different treatment regimes can select for either plasmid-carried, or chromosome-carried, resistance. Conclusions Our research addresses the effect of environmental variation on the evolution of plasmid-carried antibiotic resistance.