Cue-driven microbial cooperation and communication: evolving quorum sensing with honest signaling.

BACKGROUND: Quorum sensing (QS) is the ability of microorganisms to assess local clonal density by measuring the extracellular concentration of signal molecules that they produce and excrete. QS is also the only known way of bacterial communication that supports the coordination of within-clone cooperative actions requiring a certain threshold density of cooperating cells. Cooperation aided by QS communication is sensitive to cheating in two different ways: laggards may benefit from not investing in cooperation but enjoying the benefit provided by their cooperating neighbors, whereas Liars explicitly promise cooperation but fail to do so, thereby convincing potential cooperating neighbors to help them, for almost free. Given this double vulnerability to cheats, it is not trivial why QS-supported cooperation is so widespread among prokaryotes. RESULTS: We investigated the evolutionary dynamics of QS in populations of cooperators for whom the QS signal is an inevitable side effect of producing the public good itself (cue-based QS). Using spatially explicit agent-based lattice simulations of QS-aided threshold cooperation (whereby cooperation is effective only above a critical cumulative level of contributions) and three different (analytical and numerical) approximations of the lattice model, we explored the dynamics of QS-aided threshold cooperation under a feasible range of parameter values. We demonstrate three major advantages of cue-driven cooperation. First, laggards cannot wipe out cooperation under a wide range of reasonable environmental conditions, in spite of an unconstrained possibility to mutate to cheating; in fact, cooperators may even exclude laggards at high cooperation thresholds. Second, lying almost never pays off, if the signal is an inevitable byproduct (i.e., the cue) of cooperation; even very cheap fake signals are selected against. And thirdly, QS is most useful if local cooperator densities are the least predictable, i.e., if their lattice-wise mean is close to the cooperation threshold with a substantial variance. CONCLUSIONS: Comparing the results of the four different modeling approaches indicates that cue-driven threshold cooperation may be a viable evolutionary strategy for microbes that cannot keep track of past behavior of their potential cooperating partners, in spatially viscous and in well-mixed environments alike. Our model can be seen as a version of the famous greenbeard effect, where greenbeards coexist with defectors in a evolutionarily stable polymorphism. Such polymorphism is maintained by the condition-dependent trade-offs of signal production which are characteristic of cue-based QS.

Honesty in signalling games is maintained by trade-offs rather than costs.

BACKGROUND: Signal reliability poses a central problem for explaining the evolution of communication. According to Zahavi's Handicap Principle, signals are honest only if they are costly at the evolutionary equilibrium; otherwise, deception becomes common and communication breaks down. Theoretical signalling games have proved to be useful for understanding the logic of signalling interactions. Theoretical evaluations of the Handicap Principle are difficult, however, because finding the equilibrium cost function in such signalling games is notoriously complicated. Here, we provide a general solution to this problem and show how cost functions can be calculated for any arbitrary, pairwise asymmetric signalling game at the evolutionary equilibrium. RESULTS: Our model clarifies the relationship between signalling costs at equilibrium and the conditions for reliable signalling. It shows that these two terms are independent in both additive and multiplicative models, and that the cost of signalling at honest equilibrium has no effect on the stability of communication. Moreover, it demonstrates that honest signals at the equilibrium can have any cost value, even negative, being beneficial for the signaller independently of the receiver's response at equilibrium and without requiring further constraints. Our results are general and we show how they apply to seminal signalling models, including Grafen's model of sexual selection and Godfray's model of parent-offspring communication. CONCLUSIONS: Our results refute the claim that signals must be costly at the evolutionary equilibrium to be reliable, as predicted by the Handicap Principle and so-called 'costly signalling' theory. Thus, our results raise serious concerns about the handicap paradigm. We argue that the evolution of reliable signalling is better understood within a Darwinian life-history framework, and that the conditions for honest signalling are more clearly stated and understood by evaluating their trade-offs rather than their costs per se. We discuss potential shortcomings of equilibrium models and we provide testable predictions to help advance the field and establish a better explanation for honest signals. Last but not least, our results highlight why signals are expected to be efficient rather than wasteful.

Condition-dependent trade-offs maintain honest signalling.

How and why animals and humans signal reliably is a key issue in biology and social sciences that needs to be understood to explain the evolution of communication. In situations in which the receiver needs to differentiate between low- and high-quality signallers, once a ruling paradigm, the Handicap Principle has claimed that honest signals have to be costly to produce. Subsequent game theoretical models, however, highlighted that honest signals are not necessarily costly. Honesty is maintained by the potential cost of cheating: by the difference in the marginal benefit to marginal cost for low versus high-quality signallers; i.e. by differential trade-offs. Owing to the difficulties of manipulating signal costs and benefits, there is lack of empirical tests of these predictions. We present the results of a laboratory decision-making experiment with human participants to test the role of equilibrium signal cost and signalling trade-offs for the development of honest communication. We found that the trade-off manipulation had a much higher influence on the reliability of communication than the manipulation of the equilibrium cost of signal. Contrary to the predictions of the Handicap Principle, negative production cost promoted honesty at a very high level in the differential trade-off condition.

Four Puzzles of Reputation-Based Cooperation : Content, Process, Honesty, and Structure.

Research in various disciplines has highlighted that humans are uniquely able to solve the problem of cooperation through the informal mechanisms of reputation and gossip. Reputation coordinates the evaluative judgments of individuals about one another. Direct observation of actions and communication are the essential routes that are used to establish and update reputations. In large groups, where opportunities for direct observation are limited, gossip becomes an important channel to share individual perceptions and evaluations of others that can be used to condition cooperative action. Although reputation and gossip might consequently support large-scale human cooperation, four puzzles need to be resolved to understand the operation of reputation-based mechanisms. First, we need empirical evidence of the processes and content that form reputations and how this may vary cross-culturally. Second, we lack an understanding of how reputation is determined from the muddle of imperfect, biased inputs people receive. Third, coordination between individuals is only possible if reputation sharing and signaling is to a large extent reliable and valid. Communication, however, is not necessarily honest and reliable, so theoretical and empirical work is needed to understand how gossip and reputation can effectively promote cooperation despite the circulation of dishonest gossip. Fourth, reputation is not constructed in a social vacuum; hence we need a better understanding of the way in which the structure of interactions affects the efficiency of gossip for establishing reputations and fostering cooperation.

Honesty and dishonesty in gossip strategies: a fitness interdependence analysis.

Gossip, or sharing information about absent others, has been identified as an effective solution to free rider problems in situations with conflicting interests. Yet, the information transmitted via gossip can be biased, because gossipers may send dishonest information about others for personal gains. Such dishonest gossip makes reputation-based cooperation more difficult to evolve. But when are people likely to share honest or dishonest gossip? We build formal models to provide the theoretical foundation for individuals' gossip strategies, taking into account the gossiper's fitness interdependence with the receiver and the target. Our models across four different games suggest a very simple rule: when there is a perfect match (mismatch) between fitness interdependence and the effect of honest gossip, the gossiper should always be honest (dishonest); however, in the case of a partial match, the gossiper should make a choice based on their fitness interdependence with the receiver and the target and the marginal cost/benefit in terms of pay-off differences caused by possible choices of the receiver and the target in the game. Moreover, gossipers can use this simple rule to make optimal decisions even under noise. We discuss empirical examples that support the predictions of our model and potential extensions. This article is part of the theme issue 'The language of cooperation: reputation and honest signalling'.

Cooperating to show that you care: costly helping as an honest signal of fitness interdependence.

Social organisms often need to know how much to trust others to cooperate. Organisms can expect cooperation from another organism that depends on them (i.e. stake or fitness interdependence), but how do individuals assess fitness interdependence? Here, we extend fitness interdependence into a signalling context: costly helping behaviour can honestly signal one's stake in others, such that those who help are trusted more. We present a mathematical model in which agents help others based on their stake in the recipient's welfare, and recipients use that information to assess whom to trust. At equilibrium, helping is a costly signal of stake: helping is worthwhile for those who value the recipient (and thus will repay any trust), but is not worthwhile for those who do not value the recipient (and thus will betray the trust). Recipients demand signals when they value the signallers less and when the cost of betrayed trust is higher; signal costs are higher when signallers have more incentive to defect. Signalling systems are more likely when the trust games resemble Prisoner's Dilemmas, Stag Hunts or Harmony Games, and are less likely in Snowdrift Games. Furthermore, we find that honest signals need not benefit recipients and can even occur between hostile parties. By signalling their interdependence, organisms benefit from increased trust, even when no future interactions will occur. This article is part of the theme issue 'The language of cooperation: reputation and honest signalling'.

Pre-hunt charade as the cradle of human musicality.

Human language and human music are both unique communication systems that evolved in the human lineage. Here, I propose that they share the same root, they evolved from an ancestral communication system yet to be described in detail. I suggest that pre-hunt charade was this shared root, which helped organize and coordinate the hunt of early hominins.

Scarce and directly beneficial reputations support cooperation.

A human solution to the problem of cooperation is the maintenance of informal reputation hierarchies. Reputational information contributes to cooperation by providing guidelines about previous group-beneficial or free-rider behaviour in social dilemma interactions. How reputation information could be credible, however, remains a puzzle. We test two potential safeguards to ensure credibility: (i) reputation is a scarce resource and (ii) it is not earned for direct benefits. We test these solutions in a laboratory experiment in which participants played two-person Prisoner's Dilemma games without partner selection, could observe some other interactions, and could communicate reputational information about possible opponents to each other. Reputational information clearly influenced cooperation decisions. Although cooperation was not sustained at a high level in any of the conditions, the possibility of exchanging third-party information was able to temporarily increase the level of strategic cooperation when reputation was a scarce resource and reputational scores were directly translated into monetary benefits. We found that competition for monetary rewards or unrestricted non-monetary reputational rewards helped the reputation system to be informative. Finally, we found that high reputational scores are reinforced further as they are rewarded with positive messages, and positive gossip was leading to higher reputations.

The Handicap Principle: how an erroneous hypothesis became a scientific principle.

The most widely cited explanation for the evolution of reliable signals is Zahavi's so-called Handicap Principle, which proposes that signals are honest because they are costly to produce. Here we provide a critical review of the Handicap Principle and its theoretical development. We explain why this idea is erroneous, and how it nevertheless became widely accepted as the leading explanation for honest signalling. In 1975, Zahavi proposed that elaborate secondary sexual characters impose 'handicaps' on male survival, not due to inadvertent signalling trade-offs, but as a mechanism that functions to demonstrate males' genetic quality to potential mates. His handicap hypothesis received many criticisms, and in response, Zahavi clarified his hypothesis and explained that it assumes that signals are wasteful as well as costly, and that they evolve because wastefulness enforces honesty. He proposed that signals evolve under 'signal selection', a non-Darwinian type of selection that favours waste rather than efficiency. He maintained that the handicap hypothesis provides a general principle to explain the evolution of all types of signalling systems, i.e. the Handicap Principle. In 1977, Zahavi proposed a second hypothesis for honest signalling, which received many different labels and interpretations, although it was assumed to be another example of handicap signalling. In 1990, Grafen published models that he claimed vindicated Zahavi's Handicap Principle. His conclusions were widely accepted and the Handicap Principle subsequently became the dominant paradigm for explaining the evolution of honest signalling in the biological and social sciences. Researchers have subsequently focused on testing predications of the Handicap Principle, such as measuring the absolute costs of honest signals (and using energetic and other proximate costs as proxies for fitness), but very few have attempted to test Grafen's models. We show that Grafen's models do not support the handicap hypothesis, although they do support Zahavi's second hypothesis, which proposes that males adjust their investment into the expression of their sexual signals according to their condition and ability to bear the costs (and risks to their survival). Rather than being wasteful over-investments, honest signals evolve in this scenario because selection favours efficient and optimal investment into signal expression and minimizes signalling costs. This idea is very different from the handicap hypothesis, but it has been widely misinterpreted and equated to the Handicap Principle. Theoretical studies have since shown that signalling costs paid at the equilibrium are neither sufficient nor necessary to maintain signal honesty, and that honesty can evolve through differential benefits, as well as differential costs. There have been increasing criticisms of the Handicap Principle, but they have focused on the limitations of Grafen's model and overlooked the fact that it is not a handicap model. This model is better understood within a Darwinian framework of adaptive signalling trade-offs, without the added burden and confusing logic of the Handicap Principle. There is no theoretical or empirical support for the Handicap Principle and the time is long overdue to usher this idea into an 'honorable retirement'.

One problem, too many solutions: How costly is honest signalling of need?

The "cost of begging" is a prominent prediction of costly signalling theory, suggesting that offspring begging has to be costly in order to be honest. Seminal signalling models predict that there is a unique equilibrium cost function for the offspring that results in honest signalling and this cost function must be proportional to parent's fitness loss. This prediction is only valid if signal cost and offspring condition is assumed to be independent. Here we generalize these models by allowing signal cost to depend on offspring condition. We demonstrate in the generalized model that any signal cost proportional to the fitness gain of the offspring also results in honest signalling. Moreover, we show that any linear combination of the two cost functions (one proportional to parent's fitness loss, as in previous models, the other to offspring's fitness gain) also leads to honest signalling in equilibrium, yielding infinitely many solutions. Furthermore, we demonstrate that there exist linear combinations such that the equilibrium cost of signals is negative and the signal is honest. Our results show that costly signalling theory cannot predict a unique equilibrium cost in signalling games of parent-offspring conflicts if signal cost depends on offspring condition. It follows, contrary to previous claims, that the existence of parent-offspring conflict does not imply costly equilibrium signals. As an important consequence, it is meaningless to measure the "cost of begging" as long as the dependence of signal cost on offspring condition is unknown. Any measured equilibrium cost in case of condition-dependent signal cost has to be compared both to the parent's fitness loss and to the offspring's fitness gain in order to provide meaningful interpretation.

Does the handicap principle explain the evolution of dimorphic ornaments?

•We reinvestigate a new model based on the handicap hypothesis.•We show the handicap hypothesis does not explain male dimorphisms.•The results are due to the 'playing-the-field' assumption of the model.•The generality of the 'playing-the-field' assumption is suspect.•The evolutionary stability of the proposed new equilibrium is questionable.

Juvenile honest food solicitation and parental investment as a life history strategy: A kin demographic selection model.

Parent-offspring communication remains an unresolved challenge for biologist. The difficulty of the challenge comes from the fact that it is a multifaceted problem with connections to life-history evolution, parent-offspring conflict, kin selection and signalling. Previous efforts mainly focused on modelling resource allocation at the expense of the dynamic interaction during a reproductive season. Here we present a two-stage model of begging where the first stage models the interaction between nestlings and parents within a nest and the second stage models the life-history trade-offs. We show in an asexual population that honest begging results in decreased variance of collected food between siblings, which leads to mean number of surviving offspring. Thus, honest begging can be seen as a special bet-hedging against informational uncertainty, which not just decreases the variance of fitness but also increases the arithmetic mean.

Farming the mitochondrial ancestor as a model of endosymbiotic establishment by natural selection.

The origin of mitochondria was a major evolutionary transition leading to eukaryotes, and is a hotly debated issue. It is unknown whether mitochondria were acquired early or late, and whether it was captured via phagocytosis or syntrophic integration. We present dynamical models to directly simulate the emergence of mitochondria in an ecoevolutionary context. Our results show that regulated farming of prey bacteria and delayed digestion can facilitate the establishment of stable endosymbiosis if prey-rich and prey-poor periods alternate. Stable endosymbiosis emerges without assuming any initial metabolic benefit provided by the engulfed partner, in a wide range of parameters, despite that during good periods farming is costly. Our approach lends support to the appearance of mitochondria before any metabolic coupling has emerged, but after the evolution of primitive phagocytosis by the urkaryote.

When honesty and cheating pay off: the evolution of honest and dishonest equilibria in a conventional signalling game.

BACKGROUND: The reliability of signals is a key issue in the study of animal communication. Both empirical work and theoretical models show that communication need not be entirely honest, and thus signals can be deceitful. Aggressive communication appears to be a prime candidate for such deceitful communication, because bluffing has been described in several species. Bluffing in these situations are supposed to be maintained by frequency dependent selection where the fitness of a given type depends on the frequencies of the other types in the population. Previous efforts to model such a scenario through individual based simulations have yielded conflicting results. Studies have either found a rich set of polymorphic strategies including the traditional cheating scenario or found none. Thus, the modelling assumptions responsible for these diverging conclusions remain unclear. RESULTS: In this study, I investigate the effects of four modelling assumptions: the role of an extended strategy set, the initial population composition (seeding), the differences in pay-offs and finally different parameter spaces. I investigate the effects of these factors on the evolvability of both honest and mixed cheating strategies. I show that both honest and cheating equilibria readily evolve and that the investigated parameter range and the seeding of the starting populations have the greatest influence on the outcome. CONCLUSIONS: Both honest signalling and polymorphic cheating equilibria are more likely to evolve from a narrow strategy set than from a random mixture of strategies. A large potential strategy set is not a setback for the evolution of communication -honest or cheating- as long as the initial population is seeded with only a few strategies. In addition, different sections of the parameter space show consistently different behaviour. Thus, frequency dependent selection has the potential to explain various empirical observations that show consistent differences in aggressive behaviour.

Deception Undermines the Stability of Cooperation in Games of Indirect Reciprocity.

Indirect reciprocity is often claimed as one of the key mechanisms of human cooperation. It works only if there is a reputational score keeping and each individual can inform with high probability which other individuals were good or bad in the previous round. Gossip is often proposed as a mechanism that can maintain such coherence of reputations in the face of errors of transmission. Random errors, however, are not the only source of uncertainty in such situations. The possibility of deceptive communication, where the signallers aim to misinform the receiver cannot be excluded. While there is plenty of evidence for deceptive communication in humans the possibility of deception is not yet incorporated into models of indirect reciprocity. Here we show that when deceptive strategies are allowed in the population it will cause the collapse of the coherence of reputations and thus in turn it results the collapse of cooperation. This collapse is independent of the norms and the cost and benefit values. It is due to the fact that there is no selection for honest communication in the framework of indirect reciprocity. It follows that indirect reciprocity can be only proposed plausibly as a mechanism of human cooperation if additional mechanisms are specified in the model that maintains honesty.

Attention-Seeking Displays.

Animal communication abounds with extravagant displays. These signals are usually interpreted as costly signals of quality. However, there is another important function for these signals: to call the attention of the receiver to the signaller. While there is abundant empirical evidence to show the importance of this stage, it is not yet incorporated into standard signalling theory. Here I investigate a general model of signalling - based on a basic action-response game - that incorporates this searching stage. I show that giving attention-seeking displays and searching for them can be an ESS. This is a very general result and holds regardless whether only the high quality signallers or both high and low types give them. These signals need not be costly at the equilibrium and they need not be honest signals of any quality, as their function is not to signal quality but simply to call the attention of the potential receivers. These kind of displays are probably more common than their current weight in the literature would suggest.

Beneficial laggards: multilevel selection, cooperative polymorphism and division of labour in threshold public good games.

BACKGROUND: The origin and stability of cooperation is a hot topic in social and behavioural sciences. A complicated conundrum exists as defectors have an advantage over cooperators, whenever cooperation is costly so consequently, not cooperating pays off. In addition, the discovery that humans and some animal populations, such as lions, are polymorphic, where cooperators and defectors stably live together--while defectors are not being punished--, is even more puzzling. Here we offer a novel explanation based on a Threshold Public Good Game (PGG) that includes the interaction of individual and group level selection, where individuals can contribute to multiple collective actions, in our model group hunting and group defense. RESULTS: Our results show that there are polymorphic equilibria in Threshold PGGs; that multi-level selection does not select for the most cooperators per group but selects those close to the optimum number of cooperators (in terms of the Threshold PGG). In particular for medium cost values division of labour evolves within the group with regard to the two types of cooperative actions (hunting vs. defense). Moreover we show evidence that spatial population structure promotes cooperation in multiple PGGs. We also demonstrate that these results apply for a wide range of non-linear benefit function types. CONCLUSIONS: We demonstrate that cooperation can be stable in Threshold PGG, even when the proportion of so called free riders is high in the population. A fundamentally new mechanism is proposed how laggards, individuals that have a high tendency to defect during one specific group action can actually contribute to the fitness of the group, by playing part in an optimal resource allocation in Threshold Public Good Games. In general, our results show that acknowledging a multilevel selection process will open up novel explanations for collective actions.