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Optimal foraging predicts the ecology but not the evolution of host specialization in bacteriophages.

Guyader S, Burch CL - PLoS ONE (2008)

Bottom Line: Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density.Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density.These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina, Chapel Hill, North Carolina, United States of America.

ABSTRACT
We explore the ability of optimal foraging theory to explain the observation among marine bacteriophages that host range appears to be negatively correlated with host abundance in the local marine environment. We modified Charnov's classic diet composition model to describe the ecological dynamics of the related generalist and specialist bacteriophages phiX174 and G4, and confirmed that specialist phages are ecologically favored only at high host densities. Our modified model accurately predicted the ecological dynamics of phage populations in laboratory microcosms, but had only limited success predicting evolutionary dynamics. We monitored evolution of attachment rate, the phenotype that governs diet breadth, in phage populations adapting to both low and high host density microcosms. Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density. Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density. These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.

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Evolutionary response in the attachment rate to S. typhimurium during adaptation to two-host microcosms.For individual populations, responses were calculated as k10−k0, where ki was the mean attachment rate measured after i generations (passages) of adaptation to growth at high or low host density. Data are grand means±95% confidence intervals based on four replicate evolution experiments. The black dot (low density) indicates a difference significantly greater than 0 (1-tailed paired t-test, P = 0.0056).
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pone-0001946-g004: Evolutionary response in the attachment rate to S. typhimurium during adaptation to two-host microcosms.For individual populations, responses were calculated as k10−k0, where ki was the mean attachment rate measured after i generations (passages) of adaptation to growth at high or low host density. Data are grand means±95% confidence intervals based on four replicate evolution experiments. The black dot (low density) indicates a difference significantly greater than 0 (1-tailed paired t-test, P = 0.0056).

Mentions: Low host density was expected to impose selection to incorporate the less profitable host S. typhimurium into the diet, and to result in an increased rate of attachment to S. typhimurium. In contrast, high host density was expected to impose selection to specialize on the more profitable host E. coli, and to result in a reduced rate of attachment to S. typhimurium. To determine if attachment rate was, in fact, a target of selection in our experiments, we measured the attachment rates to S. typhimurium for each mutagenized population both before and after evolution (fig. 4). As expected, the mean attachment rate of populations adapted to the low host density treatment was significantly higher than the mean of the ancestral populations (t = 5.6076, P = 0.0056), whereas the mean attachment rates of populations adapted to the high density treatment did not change significantly over the course of the experiment (t = 0.9633, P = 0.2032).


Optimal foraging predicts the ecology but not the evolution of host specialization in bacteriophages.

Guyader S, Burch CL - PLoS ONE (2008)

Evolutionary response in the attachment rate to S. typhimurium during adaptation to two-host microcosms.For individual populations, responses were calculated as k10−k0, where ki was the mean attachment rate measured after i generations (passages) of adaptation to growth at high or low host density. Data are grand means±95% confidence intervals based on four replicate evolution experiments. The black dot (low density) indicates a difference significantly greater than 0 (1-tailed paired t-test, P = 0.0056).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2279161&req=5

pone-0001946-g004: Evolutionary response in the attachment rate to S. typhimurium during adaptation to two-host microcosms.For individual populations, responses were calculated as k10−k0, where ki was the mean attachment rate measured after i generations (passages) of adaptation to growth at high or low host density. Data are grand means±95% confidence intervals based on four replicate evolution experiments. The black dot (low density) indicates a difference significantly greater than 0 (1-tailed paired t-test, P = 0.0056).
Mentions: Low host density was expected to impose selection to incorporate the less profitable host S. typhimurium into the diet, and to result in an increased rate of attachment to S. typhimurium. In contrast, high host density was expected to impose selection to specialize on the more profitable host E. coli, and to result in a reduced rate of attachment to S. typhimurium. To determine if attachment rate was, in fact, a target of selection in our experiments, we measured the attachment rates to S. typhimurium for each mutagenized population both before and after evolution (fig. 4). As expected, the mean attachment rate of populations adapted to the low host density treatment was significantly higher than the mean of the ancestral populations (t = 5.6076, P = 0.0056), whereas the mean attachment rates of populations adapted to the high density treatment did not change significantly over the course of the experiment (t = 0.9633, P = 0.2032).

Bottom Line: Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density.Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density.These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina, Chapel Hill, North Carolina, United States of America.

ABSTRACT
We explore the ability of optimal foraging theory to explain the observation among marine bacteriophages that host range appears to be negatively correlated with host abundance in the local marine environment. We modified Charnov's classic diet composition model to describe the ecological dynamics of the related generalist and specialist bacteriophages phiX174 and G4, and confirmed that specialist phages are ecologically favored only at high host densities. Our modified model accurately predicted the ecological dynamics of phage populations in laboratory microcosms, but had only limited success predicting evolutionary dynamics. We monitored evolution of attachment rate, the phenotype that governs diet breadth, in phage populations adapting to both low and high host density microcosms. Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density. Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density. These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.

Show MeSH