Limits...
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.

Show MeSH

Related in: MedlinePlus

Optimal diet breadth given observed life history strategies in phages.Lines depict the attachment rate and lysis time combinations at which generalist and specialist phages should achieve equal growth rates for particular host combinations and densities, as predicted by equation 7 (k1 = x/[(1−x)L1N]). Here, we assume that the second best host is a proportion x as profitable as the best host, and specify a particular host density N. k1 and L1 represent the attachment rate and lysis time, respectively, of the most profitable host. Combinations above each line favor specialists; combinations below each line favor generalists. The shaded portion of the graph indicates the region over which phage life history traits have been observed. (A) Observed attachment rate and lysis times overlap the region that favors specialists only when host density is high. Here we fixed x = 0.75, and examined the cases where N = 5×105 (solid line), 1×106 (dashed line), and 5×106 hosts/ml (dotted line). (B) Observed attachment rate and lysis times overlap the region that favors specialists only when differences in host profitability are large. Here we fixed N = 1×106, and examined the cases where the second best host is 75% (solid line), 50% (dashed line), and 25% (dotted line) as profitable as the best host.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2279161&req=5

pone-0001946-g005: Optimal diet breadth given observed life history strategies in phages.Lines depict the attachment rate and lysis time combinations at which generalist and specialist phages should achieve equal growth rates for particular host combinations and densities, as predicted by equation 7 (k1 = x/[(1−x)L1N]). Here, we assume that the second best host is a proportion x as profitable as the best host, and specify a particular host density N. k1 and L1 represent the attachment rate and lysis time, respectively, of the most profitable host. Combinations above each line favor specialists; combinations below each line favor generalists. The shaded portion of the graph indicates the region over which phage life history traits have been observed. (A) Observed attachment rate and lysis times overlap the region that favors specialists only when host density is high. Here we fixed x = 0.75, and examined the cases where N = 5×105 (solid line), 1×106 (dashed line), and 5×106 hosts/ml (dotted line). (B) Observed attachment rate and lysis times overlap the region that favors specialists only when differences in host profitability are large. Here we fixed N = 1×106, and examined the cases where the second best host is 75% (solid line), 50% (dashed line), and 25% (dotted line) as profitable as the best host.

Mentions: We asked the following question. Given that a phage already consumes the most profitable host (host 1) with profitability Pr1 = lnB1/L1, and inhabits an environment with host density N, should the phage consume host 2 that is a fraction x as profitable (i.e. Pr2 = x Pr1)? By substituting xPr1 for Pr2 in equation 5, and rearranging the resulting inequality, we find that phage should consume host 2 only if the following inequality is met:(7)We used equation (7) to identify the attachment rate and lysis time combinations that favor specialists when host densities are close to the maximum (5×106 hosts/ml), mean (1×106), and median (5×105) observations from natural marine environments [14], [26] (Figure 5A), and when the second most profitable host in the environment is 75%, 50%, or 25% as profitable as the most profitable host (Figure 5B).


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

Guyader S, Burch CL - PLoS ONE (2008)

Optimal diet breadth given observed life history strategies in phages.Lines depict the attachment rate and lysis time combinations at which generalist and specialist phages should achieve equal growth rates for particular host combinations and densities, as predicted by equation 7 (k1 = x/[(1−x)L1N]). Here, we assume that the second best host is a proportion x as profitable as the best host, and specify a particular host density N. k1 and L1 represent the attachment rate and lysis time, respectively, of the most profitable host. Combinations above each line favor specialists; combinations below each line favor generalists. The shaded portion of the graph indicates the region over which phage life history traits have been observed. (A) Observed attachment rate and lysis times overlap the region that favors specialists only when host density is high. Here we fixed x = 0.75, and examined the cases where N = 5×105 (solid line), 1×106 (dashed line), and 5×106 hosts/ml (dotted line). (B) Observed attachment rate and lysis times overlap the region that favors specialists only when differences in host profitability are large. Here we fixed N = 1×106, and examined the cases where the second best host is 75% (solid line), 50% (dashed line), and 25% (dotted line) as profitable as the best host.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001946-g005: Optimal diet breadth given observed life history strategies in phages.Lines depict the attachment rate and lysis time combinations at which generalist and specialist phages should achieve equal growth rates for particular host combinations and densities, as predicted by equation 7 (k1 = x/[(1−x)L1N]). Here, we assume that the second best host is a proportion x as profitable as the best host, and specify a particular host density N. k1 and L1 represent the attachment rate and lysis time, respectively, of the most profitable host. Combinations above each line favor specialists; combinations below each line favor generalists. The shaded portion of the graph indicates the region over which phage life history traits have been observed. (A) Observed attachment rate and lysis times overlap the region that favors specialists only when host density is high. Here we fixed x = 0.75, and examined the cases where N = 5×105 (solid line), 1×106 (dashed line), and 5×106 hosts/ml (dotted line). (B) Observed attachment rate and lysis times overlap the region that favors specialists only when differences in host profitability are large. Here we fixed N = 1×106, and examined the cases where the second best host is 75% (solid line), 50% (dashed line), and 25% (dotted line) as profitable as the best host.
Mentions: We asked the following question. Given that a phage already consumes the most profitable host (host 1) with profitability Pr1 = lnB1/L1, and inhabits an environment with host density N, should the phage consume host 2 that is a fraction x as profitable (i.e. Pr2 = x Pr1)? By substituting xPr1 for Pr2 in equation 5, and rearranging the resulting inequality, we find that phage should consume host 2 only if the following inequality is met:(7)We used equation (7) to identify the attachment rate and lysis time combinations that favor specialists when host densities are close to the maximum (5×106 hosts/ml), mean (1×106), and median (5×105) observations from natural marine environments [14], [26] (Figure 5A), and when the second most profitable host in the environment is 75%, 50%, or 25% as profitable as the most profitable host (Figure 5B).

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