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Evolution of Cooperation and Control of Cheating in a Social Microbe

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Evolution of Cooperation and Control of Cheating in a Social Microbe Evolution of cooperation and control of cheating in a social microbe Joan E. Strassmann1 and David C. Queller Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 Edited by John C. Avise, University of California, Irvine, CA, and approved March 30, 2011 (received for review February 11, 2011) Much of what we know about the evolution of altruism comes or food digestion are vulnerable to exploitation by neighboring from animals. Here, we show that studying a microbe has yielded individuals (7, 21, 22). Microorganisms evaluate their numbers unique insights, particularly in understanding how social cheaters with quorum sensing, kill nonclonemates with bacteriocins, hunt are controlled. The social stage of Dictylostelium discoideum occurs in groups, and cooperatively swarm through their environment, to when the amoebae run out of their bacterial prey and aggregate name just a few examples of their social attributes (21, 23–25). into a multicellular, motile slug. This slug forms a fruiting body in Sociality in nontraditional study organisms is only beginning to be which about a fifth of cells die to form a stalk that supports the understood, however. remaining cells as they form hardy dispersal-ready spores. Because this social stage forms from aggregation, it is analogous to a social Cooperation, Organismality, and Major Transitions in group, or a chimeric multicellular organism, and is vulnerable to Evolution internal conflict. Advances in cell labeling, microscopy, single-gene The second reason for expanded interest in cooperation is a knockouts, and genomics, as well as the results of decades of study growing appreciation that it is important for how organisms of D. discoideum as a model for development, allow us to explore came to be. Cooperative major transitions in life alter the raw the genetic basis of social contests and control of cheaters in un- material for natural selection in fundamental ways (26, 27). One precedented detail. Cheaters are limited from exploiting other of the earliest transitions brought molecules together into cells in clones by high relatedness, kin discrimination, pleiotropy, noble which the fates of all were intertwined in a cooperative network. resistance, and lottery-like role assignment. The active nature of Eukaryotes themselves represent a major transition resulting these limits is reflected in the elevated rates of change in social from the capture of a bacterium that becomes the mitochondrion genes compared with nonsocial genes. Despite control of cheaters, (28). The level of cooperation between these partners is pro- some conflict is still expressed in chimeras, with slower movement found but not complete. Mitochondria are maternally inherited of slugs, slightly decreased investment in stalk compared with and do not go through meiosis, and thus will favor daughter spore cells, and differential contributions to stalk and spores. D. production and have no interest in son production. discoideum is rapidly becoming a model system of choice for mo- Another major transition resulted in multicellularity (29–32). lecular studies of social evolution. Multicellularity has evolved multiple times in both bacterial and eukaryote lineages. Animals and plants have elaborated multi- kin selection | kin recognition | multicellularity | major transitions cellularity into a plethora of diverse types. There are also a number of comparatively simple multicellular forms, like some atural selection favors cooperation when genes underlying single-species biofilms, the algal group Volvocales, or Dictyoste- Nit increase in frequency compared with their noncooperative lium (29, 33). The transition to multicellularity is different from counterparts (1–3). Evolutionary studies of cooperative interac- the transition to eukaryotes because the former involves an ag- tions have focused on the selective advantages of cooperating, how gregate of like entities, whereas the latter binds different ele- cooperation is organized, whether cheating a cooperative system ments. The major transitions can thus be categorized as fraternal, can occur, and how cheaters are controlled (4–11). These studies with like cooperating with like, or egalitarian, where the coop- generally, but not always, focus on within-species interactions and erating units bring different things to the collaboration (30). Ei- have been behaviorally oriented. Social insects have been a major ther kind of collaborative organism will usually retain conflicts, focus (12–14), with cooperative birds and mammals also getting but these conflicts must be controlled if the partnership is to considerable attention (15–17). The past few decades have seen survive. How these controls operate is a major research topic phenomenal progress in understanding cooperation in these under this view of life. organisms by applying the powerful logic of kin selection (1, 3, 18). The selective factors that favored a past transition are not easy Our advances in understanding the evolution of social behavior to study because they have already completed their work. There through kin selection have been very satisfying, but they have are living systems that could be considered to be more repre- been isolated in some respects. This is because most organisms sentative of transitional stages, however. These, we believe, may have not been seen to be particularly cooperative. They may be the most productive for investigation into the advantages of fl come together briefly for mating but, otherwise, go about the cooperation and how con ict is controlled. We have argued fi business of securing nutrients, avoiding disease and predation, elsewhere that organisms themselves can be de ned as adapted fl and producing progeny largely on their own. bundles of cooperative elements, wherein actual con ict is at a Cooperation Is Widespread Behavioral ecologists have begun to study a wider selection of This paper results from the Arthur M. Sackler Colloquium of the National Academy of fi Sciences, “In the Light of Evolution V: Cooperation and Conflict,” held January 7–8, 2011, organisms and are nding cooperative interactions to be much at the Arnold and Mabel Beckman Center of the National Academies of Sciences and more pervasive than previously appreciated. This is particularly Engineering in Irvine, CA. The complete program and audio files of most presentations true for microbes, wherein the structured environments neces- are available on the NAS Web site at www.nasonline.org/SACKLER_cooperation. sary for cooperation have been discovered to be pervasive (10, Author contributions: J.E.S. and D.C.Q. designed research; performed research; and wrote 19, 20). Microbes are particularly affected by the actions of their the paper. neighbors, because many functions that are internal in multi- The authors declare no conflict of interest. cellular organisms are external in single-celled organisms. Se- This article is a PNAS Direct Submission. creted compounds involved in processes like iron sequestration 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1102451108 PNAS Early Edition | 1of8 Downloaded by guest on September 23, 2021 minimum (33, 34). In a 2D space, with one axis being cooperation and the other being conflict, organisms are those collaborative living units at the high end of cooperation and the low end of conflict. There is variation in the level of organismality, however, and those lacking complete cooperation and retaining conflict represent the best choices for studying the origins of cooperation. Laboratory-Friendly, Social Model Organism Kin selection has been very successful for generating predictions on the impact of queen number, mate number, and caste on sociality in social insects (12, 35). Nevertheless, one would have to say that social insects fall short as an ideal model for studies of social evolution. They are long-lived, often do poorly in the lab- oratory (except ants), are not amenable to genetic experimenta- tion, and have mostly already crossed the threshold to obligate Fig. 1. D. discoideum fruiting bodies on an agar plate. sociality. Thus, social evolution research has not found its Drosophila here. Another problem with the organisms currently favored for enough other amoebae in the area, they begin to release cAMP studies of cooperation is that the actual genes underlying co- and to make receptors to it, products of the CAR genes (42, 43). operative behavior are elusive. This is particularly true for long- A signal relay system causes the amoebae to move up the cAMP lived social insects and vertebrates, although the advances of gradient and form a mound of hundreds of thousands of cells. genomics are slowly mitigating this (14, 36). Still, the twin powers Differentiation begins in the mound stage, wherein some cells of experimental evolution and single-gene knockouts are beyond sort out toward the tip and express prestalk genes. The tip the reach of most currently studied social organisms. becomes the anterior of the slug and organizes forward move- A social evolution Drosophila would need to address these ment. During movement, cells are lost from the slug posterior. At issues; thus, it would probably be single-celled. In addition to being amenable for experimental evolution and single-gene least some of these are capable of dedifferentiating and con- knockouts, it should have full altruism, with some individuals suming any bacteria encountered (44). The slug itself will not fall dying to help others. This makes it easier
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