Sociovirology: Conflict, Cooperation, and Communication Among Viruses
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Cell Host & Microbe Commentary Sociovirology: Conflict, Cooperation, and Communication among Viruses Samuel L. Dı´az-Mun˜ oz,1,* Rafael Sanjua´ n,2,3 and Stuart West4 1Department of Microbiology and Molecular Genetics, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA 2Institute for Integrative Systems Biology (I2SysBio), Universitat de Vale` ncia, C/Catedra´ tico Agustı´n Escardino 9, 46980 Paterna Valencia, Spain 3Department of Genetics, Universitat de Vale` ncia, C/Dr. Moliner 50, Burjassot, Vale` ncia 46100, Spain 4Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK *Correspondence: [email protected] https://doi.org/10.1016/j.chom.2017.09.012 Viruses are involved in various interactions both within and between infected cells. Social evolution theory offers a conceptual framework for how virus-virus interactions, ranging from conflict to cooperation, have evolved. A critical examination of these interactions could expand our understanding of viruses and be exploited for epidemiological and medical interventions. Virus-virus interactions are pervasive and Potential misgivings with this social- of another individual. As such, evolu- highly diverse (DaPalma et al., 2010; evolution approach include the idea that tionary analysis of social interactions re- Figure 1). Some viruses need another, viruses are too simple to interact socially, lies fundamentally on natural selection. ‘‘helper’’ virus to complete their infection or that to infer traits like cooperation The only major difference with non-social cycle, and other viruses are commonly would be anthropomorphic. On the flip models is that two or more interacting activated or suppressed by the presence side, social interactions have driven the individuals are involved. For example, of secondary viral infections. Viral pro- evolution of life at all levels of complexity cooperative traits, which benefit others, teins can mix and produce mosaic-like and thus could have a role in viral will only be selected for by natural selec- viral particles (pseudotypes) when a cell evolution as well: genes cooperate to tion if they provide a fitness benefit to the is coinfected with two different viruses. form genomes, cells cooperate to form individual performing them (Figure 2A). Viral coinfection of microbes is wide- multicellular organisms, and multicellular Cooperative traits cannot evolve merely spread (Dı´az-Mun˜ oz, 2017), and viruses organisms form complex cooperative so- because they provide a benefit to a have mechanisms enabling multiple cieties. Conflict is also ubiquitous: ‘‘self- population. Furthermore, the evolution of viral genomes to be cotransmitted in the ish’’ genes drive their transmission at a cooperation does not require the ability same infectious unit (reviewed in Sanjua´ n, cost to the genome, cells exploit collec- of individuals to foresee the conse- 2017). Coinfecting viral genomes can be tively produced goods like nutrient- quences of their actions. In other words, distinct, variants of the same virus, or scavenging molecules, and organisms cooperation and social evolution can be even genetically identical, suggesting compete with each other for resources. explained by, and are not at odds with, different types of functional interplay. Since no complex phenotypes are neces- individual-based natural selection. Furthermore, bacteriophages use a form sary for the evolution of social traits, the One way cooperation can be evolution- of communication to regulate lysis of the appearance of anthropomorphism or the arily favored is when it is directed toward infected cell (Erez et al., 2017). Finally, ‘‘simple’’ organization of viruses may not genetically identical individuals or rela- virus-virus interactions in the absence of pose problems for the application of tives. From an evolutionary perspective, cellular coinfection can also be mediated sociobiology models in virology. helping a genetically identical individual by changes at the host level, such as We argue for a social evolution reproduce is the same as reproducing immune responses. approach to understand and predict yourself. By extension, helping relatives Despite this growing body of empirical virus-virus interactions. This framework reproduce provides a fitness benefit to evidence suggesting virus-virus interac- can clarify unexplained phenomena in the actor, as relatives share a fraction of tions, we lack a well-founded conceptual virus-virus interactions by identifying the actor’s genes. This process by which framework that provides an understand- evolved viral social traits, their genetic individuals increase their fitness by ing of how these interactions have and mechanistic basis, and the selective helping relatives reproduce is termed kin evolved and how they could shape viral pressures underlying these traits. We selection. pathogenesis. Social evolution theory outline how this approach could lead to An important potential difficulty in was originally developed to explain animal new breakthroughs in both fundamental applying social evolution to virology re- behavior, but has since been extended to and applied virology. sides in the definition of an individual. microorganisms, including bacteria and One may consider the virion as an individ- unicellular eukaryotes. Yet this social Cooperation and the Individual ual. Yet in some cases, including para- perspective has not been embraced in Social interactions take place when the myxoviruses, birnaviruses, filoviruses, the study of viruses. traits of one individual influence the fitness retroviruses, and inoviruses, a virion can Cell Host & Microbe 22, October 11, 2017 ª 2017 The Authors. Published by Elsevier Inc. 437 This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Cell Host & Microbe Commentary Figure 1. Virus-Virus Interactions Are Diverse and Provide Multiple Opportunities for Social Evolution (A–F) Indicated by gray shadows and depicting social interactions, where the action of a viral genome changes the fitness of other viral genomes. Cells are ovals with black borders. (A) A viral genome (thick curved segment) enters the cell and performs transcription (mRNAs, thin curved segments +) and translation, leading to generation of shared intracellular viral proteins (open hexagons). Transcription-translation is a social and potentially cooperative trait because it benefits the other viral genomes in the cell. (B–F) Viral genomes can prevent or promote reproduction of other genomes by changing the probability that they can infect a cell or host by: (B) blocking the entry of other viral genomes into the cell; (C) producing host-level immune changes (dark red outline) that favor the transmission of all infecting viral genomes; (D) inducing the cell to produce molecules essential for transmission to neighboring cells, benefiting all viral genomes in the cell; (E) producing viral proteins that communicate cell infection status, signaling to other viral genomes the abundance of cells available for reproduction; and (F) manipulating host immune signals to induce distant cells to differentially expose receptors favoring entry of some viral genomes over others. carry multiple genome copies (n-ploidy). If we think of a genome as an individ- Conflict and Cheating Viruses Functionally, these n-ploid virions should ual, then the natural history of viruses is Evidence in favor of viruses acting as be similar to multiple virions entering the filled with opportunities for social inter- cooperative social agents is, paradoxi- same cell, because they would both lead actions (Figure 1), even though experi- cally, provided by the occasional spread to infections with multiple viral genomes. mental demonstration is still lacking in of uncooperative ‘‘cheats.’’ If individuals As such, we suggest that the definition of many cases. A single viral genome are not genetically identical, they will not an individual should be set at the level of entering a cell needs to accomplish both necessarily have the same evolutionary the single infectious viral genome. replication and gene expression (tran- interests, creating the potential for con- Another potential complication stems scription and translation). The mRNAs flict. Social evolution theory predicts from the fact that some viruses, notably and proteins resulting from viral gene that if multiple genomes infect a cell, one RNA viruses, show extremely high muta- expression can provide a collective that invests less in cooperative traits tion rates, leading to the suggestion that benefit to genomes in the cell, such as such as transcription and invests more in the minimal level at which an individual generating capsids and proteins that its own replication will be favored, RNA virus can be defined is a sequence block host immunity. The fact that these because it will benefit from cooperation cloud, or quasispecies (Andino and Dom- factors act as public goods permits, but without paying as much of the cost ingo, 2015). In this case, the individual does not guarantee, cooperation (Chao (Chao and Elena, 2017). This is analogous could be redefined as the consensus (or and Elena, 2017). Cooperation is more to the tragedy of the commons in humans, predominant) sequence of the quasispe- likely to evolve if most interacting ge- where cooperation breaks down due to cies. If, however, functional social interac- nomes are identical, since such high selfish interests, even though everyone tions are established among genetic relatedness allows kin selection