Cheating is a term used in behavioral ecology and ethology to describe behavior whereby organisms receive a benefit at the cost of other organisms. Cheating is common in many mutualistic and altruistic relationships. A cheater is an individual who does not cooperate (or cooperates less than their fair share) but can potentially gain the benefit from others cooperating. Cheaters are also those who selfishly use common resources to maximize their individual fitness at the expense of a group. Natural selection favors cheating, but there are mechanisms to regulate it. The stress gradient hypothesis states that facilitation, cooperation, or mutualism should be more common in stressful environments, while cheating, competition, or parasitism are common in benign environments (such as nutrient excess).
Theoretical models Organisms communicate and cooperate to perform a wide range of behaviors. Mutualism, or mutually beneficial interactions between species, is common in ecological systems. These interactions can be thought of "biological markets" in which species offer partners goods that are relatively inexpensive for them to produce and receive goods that are more expensive or even impossible for them to produce. However, these systems provide opportunities for exploitation by individuals that can obtain resources while providing nothing in return. Exploiters can take on several forms: individuals outside a mutualistic relationship who obtain a commodity in a way that confers no benefit to either mutualist, individuals who receive benefits from a partner but have lost the ability to give any in return, or individuals who have the option of behaving mutualistically towards their partners but chose not to do so.
Cheaters, who do not cooperate but benefit from others who do cooperate gain a competitive edge. In an evolutionary context, this competitive edge refers to a greater ability to survive or to reproduce. If individuals who cheat are able to gain survivorship and reproductive benefits while incurring no costs, natural selection should favor cheaters. However, mechanisms also exist that prevent cheaters from undermining mutualistic systems. One main factor is that the advantages of cheating are often frequency-dependent. Frequency-dependent selection occurs when the fitness of a phenotype depends on its frequency relative to other phenotypes in a population. Cheater phenotypes often display negative frequency-dependent selection, where fitness increases as a phenotype becomes less common and vice versa. In other words, cheaters do best (in terms of evolutionary benefits such as increased survival and reproduction) when there are relatively few of them, but as cheaters become more abundant they do worse.
For example, in Escherichia coli colonies, there are antibiotic-sensitive "cheaters" that persist at low numbers on antibiotic-laced mediums when in a cooperative colony. These cheaters enjoy the benefit of others producing antibiotic-resistant agents while producing none themselves. However, as numbers increase, if they persist in not producing the antibiotic agent themselves, they are more likely to be negatively impacted by the antibiotic substrate because there is less antibiotic agent to protect everyone. Thus, cheaters can persist in a population because their exploitative behavior gives them an advantage when they exist at low frequencies but these benefits are diminished when they are greater in number.
Others have proposed that cheating (exploitive behavior) can stabilize cooperation in mutualistic systems. In many mutualistic systems, there will be feedback benefits to those that cooperate. For instance, the fitness of both partners may be improved. If there is a high reward or many benefits for the individual that initiated the cooperative behavior, mutualism should be selected for. When researchers investigated the co-evolution of cooperation and choice in a choosy host and its symbiont (an organism that lives in a relationship that benefits all parties involved), their model indicated that although choice and cooperation may be initially selected for, this would often be unstable. In other words, one cooperative partner will choose another cooperative partner if given a choice. However, if this choice is made over and over, variation is removed and this selection can no longer be maintained. This situation is similar to the lek paradox in female choice. For example, in lek paradox, if females consistently choose for a particular male trait, genetic variance for that trait should eventually be eliminated, removing the benefits of choice. However, that choice somehow still persists.
One theory states that cheating maintains genetic variation in the face of selection for mutualism. One study shows that a small influx of immigrants with a tendency to cooperate less can generate enough genetic variability to stabilize selection for mutualism. This suggests that the presence of exploitive individuals, otherwise known as cheaters, contribute enough genetic variation to maintain mutualism itself. Both this theory and the negative frequency-dependent theory suggest that that cheating exists as part of a stable mixed evolutionary strategy with mutualism. In other words, cheating is a stable strategy used by individuals in a population where many other individuals cooperate. Another study supports that cheating can exist as a mixed strategy with mutualism using a mathematical game model. Thus, cheating can arise and be maintained in mutualistic populations.
Examples
Studies of cheating and dishonest communication in populations presupposes an organismal system that cooperates. Without a collective population that has signaling and interactions among individuals, behaviors such as cheating do not manifest. In other words, in order to study cheating behavior, a model system that engages in cooperation is needed. Models that provide insight on cheating include the social amoeba Dictyostelium discoideum; eusocial insects, such as ants, bees, and wasps; and inter-specific interactions found in cleaning mutualisms. Common examples of cleaning mutualisms include cleaner fish such as wrasses and gobies, and some cleaner shrimp.
In Dictyostelium discoideum Dictyostelium discoideum is a widely used model for cooperation and the development of multicellularity. This species of amoeba is most commonly found in a haploid, single-celled state that feeds independently and undergoes asexual reproduction. However, when the scarcity of food sources causes individual cells to starve, roughly 10⁴ to 10⁵ cells aggregate to form a mobile, multicellular structure dubbed a "slug". In the wild, aggregates generally contain multiple genotypes, resulting in chimeric mixtures. Unlike clonal (genetically identical) aggregates typically found in multicellular organisms, the potential for competition exists in chimeric aggregates. For example, because individuals in the aggregate contain different genomes, differences in fitness can result in conflict of interest among cells in the aggregate, where different genotypes could potentially compete against each other for resources and reproduction. In Dictyostelium discoideum, roughly 20% of the cells in the aggregate become dead to make the stalk of a fruiting body. The remaining 80% of cells become spores in the sorus of the fruiting body, which can germinate again once conditions are more favorable. In this case, 20% of the cells must give up reproduction so that the fruiting body forms successfully. This makes chimeric aggregates of Dictyostelium discoideum susceptible to cheating individuals that take advantage of the reproductive behavior without paying the fair price. In other words, if certain individuals tend to become a part of the sorus more frequently, they can gain increased benefit from the fruiting body system without sacrificing their own opportunities to reproduce. Cheating behavior in D. discoideum is well established, and many studies have attempted to elucidate the evolutionary and genetic mechanisms underlying the behavior. Having a 34Mb genome that is completely sequenced and well annotated makes D. discoideum a useful model in studying the genetic bases and molecular mechanisms of cheating, and in a broader sense, social evolution.
In eusocial insects Eusocial insects also serve as valuable tools in studying cheating. Eusocial insects behave cooperatively, where members of the community forgo reproduction to assist a few individuals to reproduce. Such model systems have potential for conflict of interest to arise among individuals, and thus also have potential for cheating to occur. Eusocial insects in the order Hymenoptera, which includes bees and wasps, exhibit good examples of conflicts of interest present in insect societies. In these systems, queen bees and wasps can mate and lay fertilized eggs that hatch into females. On the other hand, workers of most species in Hymenoptera can produce eggs, but cannot produce fertilized eggs due to loss of mating ability. Workers that lay eggs represent a cost for the colony because workers that lay eggs often do significantly less work, and thus negatively impact the health of the colony (for example: decreased amount of collected food, or less attention given to tending the queen's eggs). In this case, a conflict of interest arises between the workers and the colony. The workers should lay eggs in order to pass on their genes; however, as a colony, having only the queen reproduce leads to better productivity. If workers sought to pass their own genes by laying eggs, foraging activities would diminish, leading to decreased resources for the entire colony. This, in turn, can cause a tragedy of the commons, where selfish behavior lead to the depletion of resources, with long-term negative consequences for the group. However, in natural bee and wasp societies, only 0.01–0.1% and 1%, respectively, of the workers lay eggs, suggesting that strategies exist to combat cheating to prevent tragedy of the commons. These insect systems have given scientists opportunities to study strategies that keep cheating in check. Such strategies are commonly referred to as "policing" strategies, generally where additional costs are imposed on cheaters to discourage or eliminate cheating behaviors. For example, honeybees and wasps may eat eggs produced by workers. In some ant species and yellowjackets, policing may occur via aggression towards or killing egg-laying individuals to minimize cheating.
In cleaning symbiosis