Spatial dilemmas of diffusible public goods

Allen, Benjamin; Gore, Jeff; Nowak, Martin A.

doi:10.7554/elife.01169

Cited by 133 publications

(160 citation statements)

References 43 publications

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“…Spatial pattern formation affects not only cooperation, but also a wide range of ecological interactions Kerr et al, 2002Kerr et al, , 2006MacLean and Gudelj, 2006;Rickard et al, 2006;Hansen et al, 2007;Kim et al, 2008;Mitri et al, 2011;Elias and Banin, 2012;Momeni et al, 2013a;Momeni et al, 2013b;Allen et al, 2013). A recent study of Momeni et al, 2013a examined the opposite process: how do ecological interactions affect pattern formation?…”

Section: Discussionmentioning

confidence: 99%

Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms

et al. 2014

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In nature, most bacteria live in surface-attached sedentary communities known as biofilms. Biofilms are often studied with respect to bacterial interactions. Many cells inhabiting biofilms are assumed to express 'cooperative traits', like the secretion of extracellular polysaccharides (EPS). These traits can enhance biofilm-related properties, such as stress resilience or colony expansion, while being costly to the cells that express them. In well-mixed populations cooperation is difficult to achieve, because non-cooperative individuals can reap the benefits of cooperation without having to pay the costs. The physical process of biofilm growth can, however, result in the spatial segregation of cooperative from non-cooperative individuals. This segregation can prevent non-cooperative cells from exploiting cooperative neighbors. Here we examine the interaction between spatial pattern formation and cooperation in Bacillus subtilis biofilms. We show, experimentally and by mathematical modeling, that the density of cells at the onset of biofilm growth affects pattern formation during biofilm growth. At low initial cell densities, co-cultured strains strongly segregate in space, whereas spatial segregation does not occur at high initial cell densities. As a consequence, EPS-producing cells have a competitive advantage over non-cooperative mutants when biofilms are initiated at a low density of founder cells, whereas EPS-deficient cells have an advantage at high cell densities. These results underline the importance of spatial pattern formation for competition among bacterial strains and the evolution of microbial cooperation.

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Section: Discussionmentioning

confidence: 99%

Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms

et al. 2014

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“…13). In many cases, a likely important factor enabling coexistence is spatial structure (62)(63)(64), whereby spatial segregation of nonproducers and producers limits the exploitative potential of the former. In one of the few studies investigating interactions between antibiotics and social behaviors in bacteria, Diard et al (14) assessed the in vivo impact of ciprofloxacin on competition between virulent cooperative Salmonella enterica serovar Typhimurium and avirulent defectors.…”

Section: Discussionmentioning

confidence: 99%

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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“…Because public goods games have typically assumed a one-step diffusion range, there has been little scope for analysing diffusion gradients so far. Four recent studies [Allen et al 2013, Borenstein et al 2013, Scheuring 2013, Archetti 2013b have analysed diffusion gradients in the context of public goods, and have reached rather discordant conclusions because they used different assumptions, particularly on the shape of the benefit function. If the benefit function is non-linear, the shape of the diffusion gradient seems to be largely irrelevant for the dynamics, and can be approximated by a step function [Archetti 2014a].…”

Section: Diffusion Gradientsmentioning

confidence: 99%

Cooperation among cancer cells as public goods games on Voronoi networks

Archetti

2016

Journal of Theoretical Biology

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Cancer cells produce growth factors that diffuse and sustain tumor proliferation, a form of cooperation among cancer cells that can be studied using mathematical models of public goods in the framework of evolutionary game theory. Cell populations, however, form heterogeneous networks that cannot be described by regular lattices or scale-free networks, the types of graphs generally used in the study of cooperation. To describe the dynamics of growth factor production in populations of cancer cells, I study public goods games on Voronoi networks, using a range of non-linear benefits that account for the known properties of growth factors, and different types of diffusion gradients. The results are surprisingly similar to those obtained on regular graphs and different from results on scale-free networks, revealing that network heterogeneity per se does not promote cooperation when public goods diffuse beyond one-step neighbours. The exact shape of the diffusion gradient is not crucial, however, whereas the type of non-linear benefit is an essential determinant of the dynamics. Public goods games on Voronoi networks can shed light on intra-tumor heterogeneity, the evolution of resistance to therapies that target growth factors, and new types of cell therapy.

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Spatial dilemmas of diffusible public goods

Cited by 133 publications

References 43 publications

Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms

Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Cooperation among cancer cells as public goods games on Voronoi networks

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