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Cheating Viruses and Game Theory

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Cheating Viruses and Game Theory Cheating Viruses and Game Theory The theory of games can explain how viruses evolve when they compete against one another in a test of evolutionary fitness Paul E. Turner he 19th-century circus showman reptitious copulations. This strategy them easy subjects for manipulation TP. T. Barnum is reputed to have is very successful for maintaining a and study. Although the experiments coined the phrase “There’s a sucker subpopulation of sneakers, but it’s un- are conducted in the laboratory, evo- born every minute”—although Bar- likely that the population will evolve lution proceeds by natural selection num denied the saying was his, and to contain only cheaters because ter- because the laboratory habitat dictates it has been variously attributed by ritorial males are most attractive to fe- which genetic variants are favored to biographers. In any event, whoever male mates. contribute their genes to the next gen- did voice this cynical view of human In general, cheaters are highly suc- eration. This is very different from ar- gullibility could not have predicted cessful when they are rare because tificial selection, such as dog breeding, that the terms “cheaters” and “suck- they frequently encounter suckers. The where the experimenter determines ers” would describe individuals in benefits of cheating wane as more indi- the variants that will reproduce. Per- the world of microorganisms as well. viduals in the population opt to cheat. haps most important, microorganisms However, my colleagues and I have In the parlance of evolutionary biology, can be stored in a freezer indefinitely, been studying interactions between vi- the success of cheaters should be gov- creating a “fossil record” that permits ruses, and it seems that strategies for erned by frequency-dependent selection. direct comparisons between the genet- taking advantage of the other fellow That is, some cost should be associated ic makeup of an ancestral population are just another way for the viruses, with a cheating strategy so that selfish and that of its evolved descendants. too, to make a “living.” individuals are at an advantage when Our experiments suggest that yes, The temptation to cheat appears they are rare, but disadvantaged when perhaps at this moment, there may be to be a universal fact of life. In the they are common. cheaters among the viruses vying for struggle to survive and reproduce that Game theory is a useful approach survival within and near your own drives evolution, selfish individuals for mathematically predicting which cells. But in the long run, such crimes may be favored over cooperators be- strategy, if any, will dominate such don’t always pay. cause they are more energy efficient. a contest. Social scientists use game By definition, cheaters expend rela- theory to predict which behaviors will Viruses in Conflict tively little energy in a task because spread through a population, especial- We experience viruses mainly through they specialize in taking advantage of ly in contests involving classic strat- the symptoms, such as fever and fa- others—“suckers”—whose efforts they egies such as “hawk” versus “dove,” tigue, that signal that our body is de- co-opt to their own advantage. In cer- and “cooperator” versus “cheater.” One fending against an invader’s attempt tain animal species some males exert of the most intriguing results of this to commandeer the normal activities tremendous energy maintaining and approach is a mathematical proof dem- of the body’s cells. Viruses are para- defending territories to attract females. onstrating that cheating can take over sites that rely on the genetic machinery Meanwhile, the population may con- a population, even though deceit can of a host organism to make copies of tain subordinate “sneaker” males that be considered an irrational behavior themselves. At any particular moment are uninterested in territory but linger because it is punishable. an infected individual can harbor sev- at the boundaries and specialize in sur- My colleagues and I have applied eral species of viruses or even genetic game theory to the experimental evo- variants (genotypes) of the same spe- lution of viruses in the laboratory. This cies. So the host serves as an ecosystem Paul E. Turner is an assistant professor of ecology is a field that is relatively new, but is for potential interactions between the and evolutionary biology at Yale University. He re- proving to be powerful for testing fun- viruses. These interactions may be in- ceived his Ph.D. from Michigan State University in damental questions in evolutionary direct—for example, when the host’s 1995. He is interested in the ecology and evolution of infectious diseases and the use of laboratory popu- biology. It’s an approach with many immune system takes action against lations of microbes as models to address these topics. advantages: Viruses are easy to cul- one species of virus, while simultane- Address: Department of Ecology and Evolutionary ture. They have rapid generation times ously affecting other viruses. A host’s Biology, Yale University, P. O. Box 208106, New and large population sizes. In addi- fever may be a generalized response to Haven, CT 06520. Internet: [email protected] tion, an array of modern tools makes a specific infection, but the high tem- © 2005 Sigma Xi, The Scientific Research Society. Reproduction 428 American Scientist, Volume 93 with permission only. Contact [email protected]. The Bridgeman Art Library Figure 1. Cheaters often win in the simulations used in game theory, a branch of mathematics that analyzes competitive interactions between individuals. Regrettably too common among human beings, cheating has also been found among many other animal species and, perhaps surprisingly, among viruses. The cheating viruses were discovered in laboratory experiments by the author. In Le Tricheur (“The Cheat”), the 17th-century French painter Georges de La Tour depicts a card game with at least one deceitful player. perature can impair the growth of all extremely difficult to detect. More of- plants, but they are unable to hook up viruses within the body. ten, viruses seem to experience a con- with the aphid vector. This situation When viruses interact directly, their flict of interest over the resource pool. changes if luteoviruses and umbra- effects on each other are more difficult When this happens one virus can self- viruses happen to co-infect the same to detect because they take place within ishly usurp resources to the detriment plant. The umbraviruses steal some of an individual cell. When a virus enters a of other virus species or genotypes. the capsid proteins from the luteovi- cell, it hijacks the host’s metabolism, in- In a form of complementation known rus resource pool, attach themselves structing it to make the bits and pieces as phenotypic mixing, a virus acquires to the aphids and so move on to new needed to assemble other viral particles. certain observable (phenotypic) traits host plants. Meanwhile, the hapless lu- When more than one virus infects a cell, from another virus. This phenomenon teoviruses experience a net loss in the the metabolic products are freely acces- frequently involves a conflict over pro- capsid proteins they need to assemble sible to any of the co-infecting viruses. teins used to create the viral capsid, a their progeny. In a process called complementation, one shell that protects the genetic material Complementation can also be a fac- virus provides a useful product that of the virus. Phenotypic mixing allows a tor in conflicts when one virus usurps cannot be made by another virus. If the virus to acquire capsid proteins from the an enzyme needed for replication from viruses provide each other with useful resource pool of a different virus. This another virus. The best known exam- resources, the interaction is of mutual is critical because some proteins on the ples involve an ordinary virus and a benefit. Consider the co-infection of a capsid dictate whether a virus can at- defective form, typically a virus with cell by two mutant viruses, which differ tach to a particular host cell and thrive. a “shortened” genome, one that lacks by having inactivated genes at different An interaction between two plant one or more essential genes. This phe- locations in the genome. The common viruses illustrates how this strategy nomenon was first described in labo- resource pool allows the viruses to use can be important in the transmission ratory experiments involving poliovi- each other’s protein products. The co- of a virus. Luteoviruses infect nearly ruses. When these viruses are grown infection rescues the mutants, allowing all the crops that people grow for food at high densities there is strong selec- them to reproduce when they couldn’t or fiber. These viruses can easily travel tion pressure for them to lose genes otherwise do so. between plants by hitching a ride with (become defective) because shortened Such mutually beneficial interac- the tiny plant-sucking insects called viruses replicate much faster than vi- tions between viruses are either rare or aphids. Umbraviruses also infect crop ruses with genomes of normal length. © 2005 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2005 September–October 429 with permission only. Contact [email protected]. If the replication advantage of the defec- tive-interfering viruses drives the help- ers to extinction, both strains will die. Most virologists view defective- interfering viruses as an unfortunate nui- sance, one that may compromise their research goals—as when, for example, such a virus contaminates the purity of a commercial vaccine. To a microbial ecol- ogist, however, the defective-interfering viruses are especially intriguing be- cause they are parasites on parasites, or hyper-parasites, something rarely seen elsewhere in biology. This naturally raises the question of whether defective-interfering viruses are merely laboratory artifacts.
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