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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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Related in: MedlinePlus

G4 growth curve illustrates how lysis time (L) and burst size (B) were determined.Data are means and standard errors for the number of plaque-forming units (PFU = number of infected cells+free phage particles) at various times during the course of infection. The curve was drawn by hand through the data for illustrative purposes. Two bursts occur during this time window. The first burst started around 15 minutes, the second burst started around 30 minutes.
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pone-0001946-g001: G4 growth curve illustrates how lysis time (L) and burst size (B) were determined.Data are means and standard errors for the number of plaque-forming units (PFU = number of infected cells+free phage particles) at various times during the course of infection. The curve was drawn by hand through the data for illustrative purposes. Two bursts occur during this time window. The first burst started around 15 minutes, the second burst started around 30 minutes.

Mentions: Lysis times were estimated from one step growth curves (Figure 1). Approximately 103 phages were mixed with 3 mL of an exponentially growing culture at a density of 108 bacteria/mL, and incubated shaking at 37°C. Aliquots of this mixture were plated at different time intervals to monitor the increase in phage concentration. Preliminary experiments indicated that lysis time occurred at about 15 minutes, so we plated to estimate phage concentration every 5 minutes for the first 10 minutes (well before lysis), and every 2 minutes between 14 and 22 minutes, and between 26 and 32 minutes (the time intervals in which lysis events were expected to occur). An initial latent period in which the concentration of plaque forming units (PFU) remains constant was followed by a lysis period in which the PFU concentration increases sharply (note that before lysis, the number of progeny phages increases, but as they remain inside the same bacterial cell, the apparent count in PFU is unchanged). The first time point at which the phage concentration increased to more than twice the initial concentration was identified, and lysis time (L) was calculated as the mean between this time point (immediately post lysis) and the previous time point (immediately pre lysis). Burst sizes were also estimated from one step growth curves (Figure 1). Once all infected cells have been lysed, the concentration of PFU levels off and achieves a maximum value before the next lysis period begins. Burst size was then determined by dividing this maximum value (obtained at time t = 2L) by the initial PFU concentration. Lysis times and burst sizes were measured in triplicate.


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

Guyader S, Burch CL - PLoS ONE (2008)

G4 growth curve illustrates how lysis time (L) and burst size (B) were determined.Data are means and standard errors for the number of plaque-forming units (PFU = number of infected cells+free phage particles) at various times during the course of infection. The curve was drawn by hand through the data for illustrative purposes. Two bursts occur during this time window. The first burst started around 15 minutes, the second burst started around 30 minutes.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001946-g001: G4 growth curve illustrates how lysis time (L) and burst size (B) were determined.Data are means and standard errors for the number of plaque-forming units (PFU = number of infected cells+free phage particles) at various times during the course of infection. The curve was drawn by hand through the data for illustrative purposes. Two bursts occur during this time window. The first burst started around 15 minutes, the second burst started around 30 minutes.
Mentions: Lysis times were estimated from one step growth curves (Figure 1). Approximately 103 phages were mixed with 3 mL of an exponentially growing culture at a density of 108 bacteria/mL, and incubated shaking at 37°C. Aliquots of this mixture were plated at different time intervals to monitor the increase in phage concentration. Preliminary experiments indicated that lysis time occurred at about 15 minutes, so we plated to estimate phage concentration every 5 minutes for the first 10 minutes (well before lysis), and every 2 minutes between 14 and 22 minutes, and between 26 and 32 minutes (the time intervals in which lysis events were expected to occur). An initial latent period in which the concentration of plaque forming units (PFU) remains constant was followed by a lysis period in which the PFU concentration increases sharply (note that before lysis, the number of progeny phages increases, but as they remain inside the same bacterial cell, the apparent count in PFU is unchanged). The first time point at which the phage concentration increased to more than twice the initial concentration was identified, and lysis time (L) was calculated as the mean between this time point (immediately post lysis) and the previous time point (immediately pre lysis). Burst sizes were also estimated from one step growth curves (Figure 1). Once all infected cells have been lysed, the concentration of PFU levels off and achieves a maximum value before the next lysis period begins. Burst size was then determined by dividing this maximum value (obtained at time t = 2L) by the initial PFU concentration. Lysis times and burst sizes were measured in triplicate.

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
Related in: MedlinePlus