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Santorelli, L. A. et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107-1110

Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005, USA.
Nature (Impact Factor: 41.46). 03/2008; 451(7182):1107-10. DOI: 10.1038/nature06558
Source: PubMed

ABSTRACT

Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves. Several cheater mutants have been studied before, but no study has attempted a genome-scale investigation of the genetic opportunities for cheating. Here we describe such a screen in a social amoeba and show that cheating is multifaceted by revealing cheater mutations in well over 100 genes of diverse types. Many of these mutants cheat facultatively, producing more than their fair share of spores in chimaeras, but cooperating normally when clonal. These findings indicate that phenotypically stable cooperative systems may nevertheless harbour genetic conflicts. The opportunities for evolutionary moves and countermoves in such conflicts may select for the involvement of multiple pathways and numerous genes.

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    • "Unlike most multicellular organisms, a Dictyostelium FB can be composed of multiple clones, and it has emerged as a model system of conflict and cooperation (Strassmann and Queller 2011b). Cheating is clearly important in the lab (Ennis et al. 2000; Khare et al. 2009; Kuzdzal-Fick et al. 2011; Santorelli et al. 2008) and there is some evidence of apparent conflict adaptations – for example social hierarchies (Buttery et al. 2009; Fortunato et al. 2003a), costs of chimerism (Castillo et al. 2011; Foster et al. 2002), competition strategies (Kuzdzal-Fick et al. 2011), and kin discrimination (Benabentos et al. 2009; Ostrowski et al. 2008). However, our results suggest that competitive ability is a rather weak fitness component in nature. "
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    ABSTRACT: We performed a mutation accumulation (MA) experiment in the social amoeba Dictyostelium discoideum to estimate the rate and distribution of effects of spontaneous mutations affecting eight putative fitness traits. We found that the per-generation mutation rate for most fitness components is 0.0019 mutations per haploid genome per generation or larger. This rate is an order of magnitude higher than estimates for fitness components in the unicellular eukaryote Saccharomyces cerevisiae, even though the base-pair
    Full-text · Article · Jul 2013 · G3-Genes Genomes Genetics
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    • "Unlike most multicellular organisms, a Dictyostelium FB can be composed of multiple clones, and it has emerged as a model system of conflict and cooperation (Strassmann and Queller 2011b). Cheating is clearly important in the lab (Ennis et al. 2000; Khare et al. 2009; Kuzdzal-Fick et al. 2011; Santorelli et al. 2008) and there is some evidence of apparent conflict adaptations – for example social hierarchies (Buttery et al. 2009; Fortunato et al. 2003a), costs of chimerism (Castillo et al. 2011; Foster et al. 2002), competition strategies (Kuzdzal-Fick et al. 2011), and kin discrimination (Benabentos et al. 2009; Ostrowski et al. 2008). However, our results suggest that competitive ability is a rather weak fitness component in nature. "
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    ABSTRACT: We performed a mutation accumulation (MA) experiment using the social amoeba Dictyostelium discoideum to estimate the rate and distribution of effects of spontaneous mutations affecting eight putative fitness traits. We found that the per generation mutation rate for most fitness components is 0.0019 mutations per haploid genome per generation, or larger. This rate is an order of magnitude higher than estimates for fitness components in the unicellular eukaryote Saccharomyces cerevisiae, even though the base-pair substitution rate is two orders of magnitude lower. The high rate of fitness-altering mutations observed in this species may be partially explained by a large mutational target relative to Saccharomyces cerevisiae. Also, fitness-altering mutations may occur primarily at simple sequence repeats, which are common throughout the genome, including in coding regions, and may represent a target that is particularly likely to give fitness effects upon mutation. The majority of mutations had deleterious effects on fitness, but there was evidence for a substantial fraction, up to 40%, being beneficial for some of the putative fitness traits. Competitive ability within the multicellular slug appears to be under weak directional selection, perhaps reflecting the fact that slugs are sometimes, but not often, comprised of multiple clones in nature. Evidence for pleiotropy among fitness components across MA lines was absent, suggesting that mutations tend to act on single fitness components.
    Full-text · Article · May 2013 · G3-Genes Genomes Genetics
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    • "A mutant called chtB (cheater B) was recovered at the end of a selection for mutants that preferentially produce spores rather than stalks in a mixed population [21]. "
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    ABSTRACT: Background Competitive social interactions are ubiquitous in nature, but their genetic basis is difficult to determine. Much can be learned from single gene knockouts in a eukaryote microbe. The mutants can be competed with the parent to discern the social impact of that specific gene. Dictyostelium discoideum is a social amoeba that exhibits cooperative behavior in the construction of a multicellular fruiting body. It is a good model organism to study the genetic basis of cooperation since it has a sequenced genome and it is amenable to genetic manipulation. When two strains of D. discoideum are mixed, a cheater strain can exploit its social partner by differentiating more spore than its fair share relative to stalk cells. Cheater strains can be generated in the lab or found in the wild and genetic analyses have shown that cheating behavior can be achieved through many pathways. Results We have characterized the knockout mutant chtB, which was isolated from a screen for cheater mutants that were also able to form normal fruiting bodies on their own. When mixed in equal proportions with parental strain cells, chtB mutants contributed almost 60% of the total number of spores. To do so, chtB cells inhibit wild type cells from becoming spores, as indicated by counts and by the wild type cells’ reduced expression of the prespore gene, cotB. We found no obvious fitness costs (morphology, doubling time in liquid medium, spore production, and germination efficiency) associated with the cheating ability of the chtB knockout. Conclusions In this study we describe a new gene in D. discoideum, chtB, which when knocked out inhibits the parental strain from producing spores. Moreover, under lab conditions, we did not detect any fitness costs associated with this behavior.
    Full-text · Article · Jan 2013 · BMC Evolutionary Biology
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