Unrestricted migration favours virulent pathogens in experimental metapopulations: evolutionary genetics of a rapacious life history

Eshelman, Christal M.; Vouk, Roxanne; Stewart, Jodi L.; Halsne, Elizabeth G.; Lindsey, Haley A.; Schneider, Stacy; Gualu, Miliyard; Dean, Anthony M.; Kerr, Benjamin

doi:10.1098/rstb.2010.0066

Cited by 39 publications

(46 citation statements)

References 58 publications

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“…Two phage strategies lead to a "tragedy of the commons" by either being fast in infecting host bacteria but with low productivity when alone or vice versa. The selection of either phage strategy is determined by spatial restrictions in migration patterns (29,30). The presented approach permits the variation of cells/phages per droplet in the emulsion, which will allow the investigation of interactions in microbial communities, which hitherto could not be addressed because of the limited number of compartments available in standard culturing techniques.…”

Section: Discussionmentioning

confidence: 99%

Availability of public goods shapes the evolution of competing metabolic strategies

Bachmann¹,

Fischlechner

Rabbers³

et al. 2013

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

178

220

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Tradeoffs provide a rationale for the outcome of natural selection. A prominent example is the negative correlation between the growth rate and the biomass yield in unicellular organisms. This tradeoff leads to a dilemma, where the optimization of growth rate is advantageous for an individual, whereas the optimization of the biomass yield would be advantageous for a population. High-rate strategies are observed in a broad variety of organisms such as Escherichia coli, yeast, and cancer cells. Growth in suspension cultures favors fast-growing organisms, whereas spatial structure is of importance for the evolution of high-yield strategies. Despite this realization, experimental methods to directly select for increased yield are lacking. We here show that the serial propagation of a microbial population in a water-in-oil emulsion allows selection of strains with increased biomass yield. The propagation in emulsion creates a spatially structured environment where the growth-limiting substrate is privatized for populations founded by individual cells. Experimental evolution of several isogenic Lactococcus lactis strains demonstrated the existence of a tradeoff between growth rate and biomass yield as an apparent Pareto front. The underlying mutations altered glucose transport and led to major shifts between homofermentative and heterofermentative metabolism, accounting for the changes in metabolic efficiency. The results demonstrated the impact of privatizing a public good on the evolutionary outcome between competing metabolic strategies. The presented approach allows the investigation of fundamental questions in biology such as the evolution of cooperation, cell-cell interactions, and the relationships between environmental and metabolic constraints.A lthough the existence of tradeoffs in evolution seems to be undisputable, experimental evidence obtained under controlled conditions is scarce. Several examples failed to show tradeoffs (1-4), whereas others could find them (5, 6) or found general but not universal tradeoffs (7,8). A tradeoff between growth rate and growth yield in microbes (9-11) has direct implications for experiments carried out in liquid cultures. This is especially of importance during prolonged cultivations such as laboratory evolution experiments. In suspension, fast-growing variants outcompete slower growing ones at the cost of biomass yield (5). The yield versus rate optimization is governed by a dilemma where fast growth is advantageous from the perspective of an individual cell, whereas slow growth, and therefore high yield, is advantageous from the perspective of a population. This dilemma is consistent with a concept termed the tragedy of the commons (12). It is well described that spatial structure is essential for the selection of high-yield strategies (13-15). The yield/rate tradeoff of microbial growth has been linked to metabolic strategies (11) such as the switch between respiration and fermentation in yeast (9). It is suggested that the underlying cause of this tradeoff is based on...

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Section: Discussionmentioning

confidence: 99%

Availability of public goods shapes the evolution of competing metabolic strategies

Bachmann¹,

Fischlechner

Rabbers³

et al. 2013

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

178

220

View full text Add to dashboard Cite

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“…Several theoretical studies have explored the role of spatial structure in promoting restraint in victimexploiter interactions (64,65). There have also been experimental demonstrations that limited dispersal favors restraint in hostparasite communities in the form of reduced parasite virulence and/or infectivity (60,61,66).…”

Section: Discussionmentioning

confidence: 99%

Evolution of restraint in a structured rock–paper–scissors community

Nahum

Harding

Kerr

2011

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

Self Cite

107

117

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It is not immediately clear how costly behavior that benefits others evolves by natural selection. By saving on inherent costs, individuals that do not contribute socially have a selective advantage over altruists if both types receive equal benefits. Restrained consumption of a common resource is a form of altruism. The cost of this kind of prudent behavior is that restrained individuals give up resources to less-restrained individuals. The benefit of restraint is that better resource management may prolong the persistence of the group. One way to dodge the problem of defection is for altruists to interact disproportionately with other altruists. With limited dispersal, restrained individuals persist because of interaction with like types, whereas it is the unrestrained individuals that must face the negative long-term consequences of their rapacity. Here, we study the evolution of restraint in a community of three competitors exhibiting a nontransitive (rock-paper-scissors) relationship. The nontransitivity ensures a form of negative feedback, whereby improvement in growth of one competitor has the counterintuitive consequence of lowering the density of that improved player. This negative feedback generates detrimental long-term consequences for unrestrained growth. Using both computer simulations and evolution experiments with a nontransitive community of Escherichia coli, we find that restrained growth can evolve under conditions of limited dispersal in which negative feedback is present. This research, thus, highlights a set of ecological conditions sufficient for the evolution of one form of altruism.survival of the weakest | experimental evolution | positive assortment | ecological feedback | bacteriocin Wisely and slow; they stumble that run fast. William ShakespeareT he conflict between individual and group interests is a common element in many social dilemmas. Consider the rate at which an organism consumes shared resources. Prudent use of common resources promotes the longevity or fecundity of the group; however, any individual that exhibits restraint suffers in competition with those using resources rapidly. Rapacity is selectively favored and the displacement of prudent types by their unrestrained contemporaries occurs despite harmful consequences for the group (1, 2). Restraint in the use of common resources is a form of altruism: behavior that is self-sacrificial and prosocial. Like other types of altruistic behavior, restraint faces a fundamental problem of subversion (3, 4). How can restrained types persist in the midst of would-be cheaters-individuals that have a competitive edge because they are unrestrained? In this article, we address this question directly by outlining ecological conditions sufficient to favor the evolution of restraint.One ingredient found in most explanations for the evolution of altruism, and thus relevant to the evolution of restraint, is positive assortment. Altruism stands a better chance when altruistic individuals disproportionately help those possessing the genes f...

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“…Third, time to host death (that is, lysis time) can be measured accurately. Although any lytic action eventually kills a cell, lysis time is an important determinant for the speed at which a phage devours a bacterial population and may be interpreted as a component of virulence (Eshelman et al, 2010). Fourth, reproductive success of coinfecting phages can be quantified separately, which overcomes a major obstacle of many experimental studies.…”

Section: Introductionmentioning

confidence: 99%

Within-host competition determines reproductive success of temperate bacteriophages

Refardt

2011

The ISME Journal

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Within-host competition between parasites is frequently invoked as a major force for parasite evolution, yet quantitative studies on its extent in an organismal group are lacking. Temperate bacteriophages are diverse and abundant parasites of bacteria, distinguished by their ability to enter a facultative dormant state in their host. Bacteria can accumulate multiple phages that may eventually abandon dormancy in response to host stress. Host resources are then converted into phage particles, whose release requires cell death. To study within-host competition between phages, I used the bacterium Escherichia coli and 11 lambdoid phages to construct single and double lysogens. Lysogenic bacterial cultures were then induced and time to host cell lysis and productivity of phages was measured. In double lysogens, this revealed strong competitive interactions as in all cases productivity of at least one phage declined. The outcome of within-host competition was often asymmetrical, and phages were found to vary hierarchically in within-host competitive ability. In double infections, the phage with the shorter lysis time determined the timing of cell lysis, which was associated with a competitive advantage when time differences were large. The results emphasize that within-host competition greatly affects phage fitness and that multiple infections should be considered an integral part of bacteriophage ecology.

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Unrestricted migration favours virulent pathogens in experimental metapopulations: evolutionary genetics of a rapacious life history

Cited by 39 publications

References 58 publications

Availability of public goods shapes the evolution of competing metabolic strategies

Availability of public goods shapes the evolution of competing metabolic strategies

Evolution of restraint in a structured rock–paper–scissors community

Within-host competition determines reproductive success of temperate bacteriophages

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