Article

Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae

Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005, USA.
Nature (Impact Factor: 42.35). 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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    • "Some strains have been shown to be cheats in that, when there are mixed genotype fruiting bodies, they contribute less than their proportional share to the dead stalk, and more to the reproductive spore head (Strassmann et al. 2000). It has also been shown that a number of strains are facultative cheats, which cheat when in mixed genotype fruiting bodies, but are able to produce a normal fruiting body when in single genotype (clonal) fruiting bodies (Fortunato et al. 2003; Santorelli et al. 2008; Buttery et al. 2009; Khare and Shaulsky 2010). Another important exception is the analogous fruiting body formation in the bacteria M. xanthus, where facultative cheating has also been observed (Velicer et al. 2000; Fiegna and Velicer 2005; Fiegna et al. 2006). "
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    ABSTRACT: The term "cheating" is used in the evolutionary and ecological literature to describe a wide range of exploitative or deceitful traits. Although many find this a useful short hand, others have suggested that it implies cognitive intent in a misleading way, and is used inconsistently. We provide a formal justification of the use of the term "cheat" from the perspective of an individual as a maximizing agent. We provide a definition for cheating that can be applied widely, and show that cheats can be broadly classified on the basis of four distinctions: (i) whether cooperation is an option; (ii) whether deception is involved; (iii) whether members of the same or different species are cheated; and (iv) whether the cheat is facultative or obligate. Our formal definition and classification provide a framework that allow us to resolve and clarify a number of issues, regarding the detection and evolutionary consequences of cheating, as well as illuminating common principles and similarities in the underlying selection pressures.
    Evolution 09/2013; 68(2). DOI:10.1111/evo.12266 · 4.66 Impact Factor
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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
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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. "
    [Show abstract] [Hide abstract]
    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.
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