Ecological drivers of the evolution of public‐goods cooperation in bacteria

Brockhurst, Michael A.; Habets, Michelle G. J. L.; Libberton, Ben; Buckling, Angus; Gardner, Andy

doi:10.1890/09-0293.1

Cited by 46 publications

(48 citation statements)

References 26 publications

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“…Previous research has propounded the importance of ecology in social evolution and called for a deeper integration of ecological factors in social theory (69)(70)(71)(72)(73). Further to this claim, we suggest that ecological stressors could impact social evolution in microbes and in multicellular taxa more generally.…”

Section: Discussionsupporting

confidence: 53%

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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Section: Discussionsupporting

confidence: 53%

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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“…The scenario we implement is one in which bacteria can achieve a basal growth rate by consuming a readily accessible carbon source, the basic nutrient N, which diffuses into the biofilm from the bulk liquid. Bacterial growth may be augmented by the activity of the secreted enzyme, which liberates a different growth substrate [89]. The two nutrient sources are implemented separately to allow us to independently vary the effects of two distinct phenomena on the evolution of cooperation.…”

Section: (C) Simulations With An Agent-based Modelmentioning

confidence: 99%

“…rspb.royalsocietypublishing.org Proc R Soc B 280: 20122770 public good compounds [94], the shapes of their benefit and cost functions [95], and disturbance-dispersal dynamics [89] also play an important role in the evolution of cooperation, but for the sake of illustration and brevity we have omitted these molecular and ecological details from our study.…”

Section: (C) Simulations With An Agent-based Modelmentioning

confidence: 99%

Cutting through the complexity of cell collectives

et al. 2013

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Via strength in numbers, groups of cells can influence their environments in ways that individual cells cannot. Large-scale structural patterns and collective functions underpinning virulence, tumour growth and bacterial biofilm formation are emergent properties of coupled physical and biological processes within cell groups. Owing to the abundance of factors influencing cell group behaviour, deriving general principles about them is a daunting challenge. We argue that combining mechanistic theory with theoretical ecology and evolution provides a key strategy for clarifying how cell groups form, how they change in composition over time, and how they interact with their environments. Here, we review concepts that are critical for dissecting the complexity of cell collectives, including dimensionless parameter groups, individual-based modelling and evolutionary theory. We then use this hybrid modelling approach to provide an example analysis of the evolution of cooperative enzyme secretion in bacterial biofilms.

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“…This framework models the ecological systems as a whole, including environmental features, such as the existence of limiting resources, but usually makes specific assumptions about the interactions among individuals. Experimental studies (Craig MacLean & Gudelj 2006, Brockhurst et al 2010) as well as analyses using the ecological framework, have shown that the limitation of resources might be important to explain cooperative behaviours in bacteria, plants, insects and even animals that do not posses enough information as to decide not to act as parasites. Some of these results are: the tradeoff between rate and yield of metabolic pathways, as that of aerobic and anaerobic bacteria, may foster cooperation in a two dimensional world (Pfeiffer et al 2001, Pfeiffer & Bonhoeffer 2003, Craig MacLean & Gudelj 2006; if trade of resources is possible, long term relationships allow cooperative plants to evolve (Mazancourt & Schwartz 2010); if the resource for which insects compete is the empty space left to lay eggs and they are not able to recognize their own eggs, cooperation, defection and coexistence are allowed (Mesterton-Gibbons 1991); if the individuals have the choice to parasite food items from their partners (kleptoparasitism, Broom & Ruxton 1998) all individuals will end up either always parasitizing or never doing it, and if the information about the amounts of food they will obtain is restricted, populations of cooperative individuals may evolve depending on the past history of the system (Broom & Rychtar 2009).…”

Section: Introductionmentioning

confidence: 99%

Evolution of cooperation mediated by limiting resources: Connecting resource based models and evolutionary game theory

Requejo

Camacho

2011

Journal of Theoretical Biology

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To cite this version:Rubén J. Requejo, Juan Camacho. Evolution of cooperation mediated by limiting resources: Connecting resource based models and evolutionary game theory. Journal of Theoretical Biology, Elsevier, 2011, 272 (1) This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Ecological drivers of the evolution of public‐goods cooperation in bacteria

Cited by 46 publications

References 26 publications

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Cutting through the complexity of cell collectives

Evolution of cooperation mediated by limiting resources: Connecting resource based models and evolutionary game theory

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