The costs and benefits of being a chimera

Foster, Kevin R.; Fortunato, Angelo; Strassmann, Joan E.; Queller, David C.

doi:10.1098/rspb.2002.2163

Cited by 122 publications

(138 citation statements)

References 33 publications

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“…Velicer and colleagues (Velicer et al 1998(Velicer et al , 2000Velicer & Stredwick 2002;Fiegna & Velicer 2003;Velicer & Yu 2003) and Strassmann and colleagues (Strassmann et al 2000;Foster et al 2002;Fortunato et al 2003a,b;Queller et al 2003) have shown that cheaters may be common in the bacterium Myxococcus xanthus and in the social amoeba, Dictyostelium discoideum, respectively. In these cases, when the organisms are starved they amass into a non-migrating fruiting body or a slug, respectively, and cheater clones make up a small fraction of stalk-like reproductive structures.…”

Section: Resultsmentioning

confidence: 99%

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

et al. 2004

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The evolution of group-beneficial traits potentially allows the survival of 'cheaters' that would otherwise be unfit. Here we describe experimental work on group-beneficial traits and the consequences of frequencydependent selection in the context of bacterial antibiotic resistance. We constructed a 'self-limited antibiotic resistant' (SLAR) strain of Escherichia coli in which a TEM-1 b-lactamase was anchored to the inner membrane. In pairwise competition experiments between the SLAR strain and ampicillin-sensitive strains, only the SLAR strain survived in the presence of ampicillin. We also constructed a 'shared antibiotic resistant' (SAR) strain in which TEM-1 b-lactamase protected both the SAR strain and nearby sensitive cells, thus acting as a model for a genetically defined group-beneficial trait. In pairwise competition experiments of the SAR strain against two different sensitive strains of E. coli , we found that the sensitive strains maintained themselves at frequencies of 5-12% in the presence of ampicillin. When the relative cost of the SAR strain was lowered, its equilibrial frequency rose. Sensitive strains also arose from pure cultures of the SAR strain. In these cases, too, the sensitive 'cheaters' were maintained in ampicillin at frequencies comparable to those observed in the previous competitions. These results suggest that traits which benefit other group members can permit survival of genotypes that otherwise would be eliminated by natural selection, and allow the maintenance of greater genetic variation upon which evolution can operate.

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Section: Resultsmentioning

confidence: 99%

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

et al. 2004

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“…Third, joining a chimera can give size advantages that accrue to a larger multicellular individual. These include longer migration during the motile slug stage (Foster et al 2002) and greater fruiting body height, which may increase dispersal success and outweigh the potential cost of victimization.…”

Section: Discussionmentioning

confidence: 99%

An invitation to die: initiators of sociality in a social amoeba become selfish spores

2010

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Greater size and strength are common attributes of contest winners. Even in social insects with high cooperation, the right to reproduce falls to the well-fed queens rather than to poorly fed workers. In Dictyostelium discoideum , formerly solitary amoebae aggregate when faced with starvation, and some cells die to form a stalk which others ride up to reach a better location to sporulate. The first cells to starve have lower energy reserves than those that starve later, and previous studies have shown that the better-fed cells in a mix tend to form disproportionately more reproductive spores. Therefore, one might expect that the first cells to starve and initiate the social stage should act altruistically and form disproportionately more of the sterile stalk, thereby enticing other better-fed cells into joining the aggregate. This would resemble caste determination in social insects, where altruistic workers are typically fed less than reproductive queens. However, we show that the opposite result holds: the first cells to starve become reproductive spores, presumably by gearing up for competition and outcompeting late starvers to become prespore first. These findings pose the interesting question of why others would join selfish organizers.

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“…4). Chimeric slugs move less far than clonal slugs when cell number is controlled (53). This may be the result of increased competition to stay out of the front control region that becomes the sterile stalk.…”

Section: Dictyostelium Discoideum As a Model System For Cooperationmentioning

confidence: 99%

Evolution of cooperation and control of cheating in a social microbe

Strassmann

Queller

2011

Proc. Natl. Acad. Sci. U.S.A.

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Much of what we know about the evolution of altruism comes from animals. Here, we show that studying a microbe has yielded unique insights, particularly in understanding how social cheaters are controlled. The social stage of Dictylostelium discoideum occurs when the amoebae run out of their bacterial prey and aggregate into a multicellular, motile slug. This slug forms a fruiting body in which about a fifth of cells die to form a stalk that supports the remaining cells as they form hardy dispersal-ready spores. Because this social stage forms from aggregation, it is analogous to a social group, or a chimeric multicellular organism, and is vulnerable to internal conflict. Advances in cell labeling, microscopy, single-gene knockouts, and genomics, as well as the results of decades of study of D. discoideum as a model for development, allow us to explore the genetic basis of social contests and control of cheaters in unprecedented detail. Cheaters are limited from exploiting other clones by high relatedness, kin discrimination, pleiotropy, noble resistance, and lottery-like role assignment. The active nature of these limits is reflected in the elevated rates of change in social genes compared with nonsocial genes. Despite control of cheaters, some conflict is still expressed in chimeras, with slower movement of slugs, slightly decreased investment in stalk compared with spore cells, and differential contributions to stalk and spores. D. discoideum is rapidly becoming a model system of choice for molecular studies of social evolution.kin selection | kin recognition | multicellularity | major transitions

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The costs and benefits of being a chimera

Cited by 122 publications

References 33 publications

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

An invitation to die: initiators of sociality in a social amoeba become selfish spores

Evolution of cooperation and control of cheating in a social microbe

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