Evolution of cooperation and control of cheating in a social microbe

Strassmann, Joan E.; Queller, David C.

doi:10.1073/pnas.1102451108

Cited by 194 publications

(208 citation statements)

References 88 publications

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“…Thus, selection should favour 'cheaters' that benefit from the social contributions of others while offering little or nothing in return. But nature tells a different story: cooperative behaviour is taxonomically widespread, and it has persisted and even flourished over long periods of evolutionary time [1][2][3][4]. This apparent contradiction has led the evolution of cooperation to be regarded as one of evolutionary biology's greatest puzzles [5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

Cheating and punishment in cooperative animal societies

Riehl

Frederickson

2016

Phil. Trans. R. Soc. B

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Cheaters—genotypes that gain a selective advantage by taking the benefits of the social contributions of others while avoiding the costs of cooperating—are thought to pose a major threat to the evolutionary stability of cooperative societies. In order for cheaters to undermine cooperation, cheating must be an adaptive strategy: cheaters must have higher fitness than cooperators, and their behaviour must reduce the fitness of their cooperative partners. It is frequently suggested that cheating is not adaptive because cooperators have evolved mechanisms to punish these behaviours, thereby reducing the fitness of selfish individuals. However, a simpler hypothesis is that such societies arise precisely because cooperative strategies have been favoured over selfish ones—hence, behaviours that have been interpreted as ‘cheating’ may not actually result in increased fitness, even when they go unpunished. Here, we review the empirical evidence for cheating behaviours in animal societies, including cooperatively breeding vertebrates and social insects, and we ask whether such behaviours are primarily limited by punishment. Our review suggests that both cheating and punishment are probably rarer than often supposed. Uncooperative individuals typically have lower, not higher, fitness than cooperators; and when evidence suggests that cheating may be adaptive, it is often limited by frequency-dependent selection rather than by punishment. When apparently punitive behaviours do occur, it remains an open question whether they evolved in order to limit cheating, or whether they arose before the evolution of cooperation.

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Section: Introductionmentioning

confidence: 99%

Cheating and punishment in cooperative animal societies

Riehl

Frederickson

2016

Phil. Trans. R. Soc. B

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“…Microbes may exhibit rapid ecological and evolutionary responses and are amenable to controlled laboratory experimentation (36,38). Bacteria, in particular, show a variety of behaviors consistent with basic social interactions.…”

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Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Vasse

Noble

Akhmetzhanov

et al. 2017

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

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Cheats are a pervasive threat to public goods production in natural and human communities, as they benefit from the commons without contributing to it. Although ecological antagonisms such as predation, parasitism, competition, and abiotic environmental stress play key roles in shaping population biology, it is unknown how such stresses generally affect the ability of cheats to undermine cooperation. We used theory and experiments to address this question in the pathogenic bacterium, Pseudomonas aeruginosa. Although public goods producers were selected against in all populations, our competition experiments showed that antibiotics significantly increased the advantage of nonproducers. Moreover, the dominance of nonproducers in mixed cultures was associated with higher resistance to antibiotics than in either monoculture. Mathematical modeling indicates that accentuated costs to producer phenotypes underlie the observed patterns. Mathematical analysis further shows how these patterns should generalize to other taxa with public goods behaviors. Our findings suggest that explaining the maintenance of cooperative public goods behaviors in certain natural systems will be more challenging than previously thought. Our results also have specific implications for the control of pathogenic bacteria using antibiotics and for understanding natural bacterial ecosystems, where subinhibitory concentrations of antimicrobials frequently occur.evolution | cooperation | antibiotics | social behavior | resistance P ublic goods production is a characteristic of a diverse range of taxa, from microbes to humans (1-3). Explaining the persistence of this costly behavior is challenging, because cheats can exploit the commons without contributing. Kin selection theory has proven to be a successful framework for addressing this question, with the central prediction that cooperation is favored by sufficient benefits to, and positive assortment between, cooperators (4-8). For example, recent study in experimental bacterial populations has elucidated mechanisms such as assortment emerging from limited or budding dispersal (9, 10) and kin discrimination (11, 12) that are consistent with kin selection fostering cooperative behaviors (e.g., refs. 8 and 13). However, despite this accumulating consensus, little is known about how social populations respond to differences and variation in abiotic and biotic components of their environment. In particular, it is unclear how ecological antagonisms affect the ability of cheats to invade cooperator communities.Cooperation can be affected by stress directly through differential selection on cooperative phenotypes (14, 15), or by inducing specific plastic behaviors (16-22), especially when cooperation leads to increased stress resistance. However, in the absence of a direct benefit of the cooperative behavior against stress, the ecological and evolutionary outcomes of the interactions between nondefensive public goods and stress responses are less clear and are potentially complex. Cooperation may be infl...

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“…Upon exhausting their local supply of food, amoebae initiate a developmental program, joining with neighbors to form an aggregate. The culmination of development is a fruiting body made of stalk and spores (1)(2)(3)(4). In nature, there is significant diversity and coexistence of multiple species and genotypes of cellular slime molds (5,6).…”

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Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds

Tarnita¹,

Washburne²,

Martínez-García³

et al. 2015

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

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Cellular slime molds, including the well-studied Dictyostelium discoideum, are amoebae whose life cycle includes both a single-cellular and a multicellular stage. To achieve the multicellular stage, individual amoebae aggregate upon starvation to form a fruiting body made of dead stalk cells and reproductive spores, a process that has been described in terms of cooperation and altruism. When amoebae aggregate they do not perfectly discriminate against nonkin, leading to chimeric fruiting bodies. Within chimeras, complex interactions among genotypes have been documented, which should theoretically reduce genetic diversity. This is however inconsistent with the great diversity of genotypes found in nature. Recent work has shown that a little-studied component of D. discoideum fitness-the loner cells that do not participate in the aggregation-can be selected for depending on environmental conditions and that, together with the spores, they could represent a bet-hedging strategy. We suggest that in all cellular slime molds the existence of loners could resolve the apparent diversity paradox in two ways. First, if loners are accounted for, then apparent genotypic skew in the spores of chimeras could simply be the result of different investments into spores versus loners. Second, in an ecosystem with multiple local environments differing in their food recovery characteristics and connected globally via weak-to-moderate dispersal, coexistence of multiple genotypes can occur. Finally, we argue that the loners make it impossible to define altruistic behavior, winners or losers, without a clear description of the ecology.

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Evolution of cooperation and control of cheating in a social microbe

Cited by 194 publications

References 88 publications

Cheating and punishment in cooperative animal societies

Cheating and punishment in cooperative animal societies

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds

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