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Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa.

Inglis RF, Brown SP, Buckling A - Evolution (2012)

Bottom Line: Social interactions have been shown to play an important role in bacterial evolution and virulence.These results confirm the ecological and evolutionary importance of considering multiple social traits simultaneously.Moreover, our results are consistent with recent theory regarding the invasion conditions for strong reciprocity (helping cooperators and harming noncooperators).

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oxford, Oxford, OX1 3PS, United Kingdom. fredrik.inglis@env.ethz.ch

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Bacterial density and virulence in a caterpillar host. (A) Bacterial density affected by starting frequency of spiteful and nonspiteful cooperators. Lowest densities were observed in low and intermediate spiteful cooperator treatments. High starting frequencies of spiteful cooperators reached similar densities to that of low and intermediate nonspiteful cooperators. The highest density was observed in the high nonspiteful cooperator frequency. Error bars represent ± 1 SE of the mean. (B) Average time to death of caterpillars infected with different starting frequencies of spiteful and nonspiteful cooperators. Lowest virulence (as measured by time to death) was observed in the low and intermediate spiteful cooperator treatments. The highest virulence is found in the high starting frequency of nonspiteful cooperator, with similar virulence occurring in the intermediate and low nonspiteful cooperator treatments and high starting frequencies of spiteful cooperators.
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fig06: Bacterial density and virulence in a caterpillar host. (A) Bacterial density affected by starting frequency of spiteful and nonspiteful cooperators. Lowest densities were observed in low and intermediate spiteful cooperator treatments. High starting frequencies of spiteful cooperators reached similar densities to that of low and intermediate nonspiteful cooperators. The highest density was observed in the high nonspiteful cooperator frequency. Error bars represent ± 1 SE of the mean. (B) Average time to death of caterpillars infected with different starting frequencies of spiteful and nonspiteful cooperators. Lowest virulence (as measured by time to death) was observed in the low and intermediate spiteful cooperator treatments. The highest virulence is found in the high starting frequency of nonspiteful cooperator, with similar virulence occurring in the intermediate and low nonspiteful cooperator treatments and high starting frequencies of spiteful cooperators.

Mentions: We next determined the importance of spiteful interactions in driving the relationship between starting frequency of competing genotypes and virulence, when cooperating genotypes compete with cheats. We manipulated starting populations to give high (99%), intermediate (50%), and low (1%) frequencies of the spiteful cooperator (PAO1) relative to the susceptible cheats (O:9 siderophore mutants), and compared these results with those obtained for coinfections with the nonspiteful cooperator (PAO1150–2) and susceptible cheats (O:9 siderophore mutants). Our model suggests the reduction in virulence associated with intermediate frequencies of a spiteful genotype (as seen in both theoretical and empirical studies; Inglis et al. 2009) should be attenuated or removed when spiteful cooperators compete against cheats. Virulence models (including those cited above) typically assume that virulence is simply a positive function of within-host growth rate, and when we measured density of bacteria within caterpillars, our results were entirely consistent with our model prediction. Both cooperative strains (spiteful/nonspiteful) displayed a positive curvilinear relationship between starting frequency and bacterial density after 8 h growth when in competition with susceptible cheats (linear term F1, 95= 43.15, P < 0.0001; quadratic term F1, 93= 4.65, P < 0.034), with nonspiteful cooperators reaching overall higher densities (F1, 94= 75.56, P < 0.0001) (Fig. 6A). This positive monotonic relationship between in vivo growth rate and cooperator frequency is consistent with theory (including our model) (Brown et al. 2002; West and Buckling 2003) and experimental results (Harrison et al. 2006). Crucially, there was no evidence of reduced density at intermediate frequencies of spiteful cooperators, as has been observed under almost identical experimental conditions when the spiteful cooperator competed against the susceptible cooperator used in this study (Inglis et al. 2009).


Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa.

Inglis RF, Brown SP, Buckling A - Evolution (2012)

Bacterial density and virulence in a caterpillar host. (A) Bacterial density affected by starting frequency of spiteful and nonspiteful cooperators. Lowest densities were observed in low and intermediate spiteful cooperator treatments. High starting frequencies of spiteful cooperators reached similar densities to that of low and intermediate nonspiteful cooperators. The highest density was observed in the high nonspiteful cooperator frequency. Error bars represent ± 1 SE of the mean. (B) Average time to death of caterpillars infected with different starting frequencies of spiteful and nonspiteful cooperators. Lowest virulence (as measured by time to death) was observed in the low and intermediate spiteful cooperator treatments. The highest virulence is found in the high starting frequency of nonspiteful cooperator, with similar virulence occurring in the intermediate and low nonspiteful cooperator treatments and high starting frequencies of spiteful cooperators.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC3795443&req=5

fig06: Bacterial density and virulence in a caterpillar host. (A) Bacterial density affected by starting frequency of spiteful and nonspiteful cooperators. Lowest densities were observed in low and intermediate spiteful cooperator treatments. High starting frequencies of spiteful cooperators reached similar densities to that of low and intermediate nonspiteful cooperators. The highest density was observed in the high nonspiteful cooperator frequency. Error bars represent ± 1 SE of the mean. (B) Average time to death of caterpillars infected with different starting frequencies of spiteful and nonspiteful cooperators. Lowest virulence (as measured by time to death) was observed in the low and intermediate spiteful cooperator treatments. The highest virulence is found in the high starting frequency of nonspiteful cooperator, with similar virulence occurring in the intermediate and low nonspiteful cooperator treatments and high starting frequencies of spiteful cooperators.
Mentions: We next determined the importance of spiteful interactions in driving the relationship between starting frequency of competing genotypes and virulence, when cooperating genotypes compete with cheats. We manipulated starting populations to give high (99%), intermediate (50%), and low (1%) frequencies of the spiteful cooperator (PAO1) relative to the susceptible cheats (O:9 siderophore mutants), and compared these results with those obtained for coinfections with the nonspiteful cooperator (PAO1150–2) and susceptible cheats (O:9 siderophore mutants). Our model suggests the reduction in virulence associated with intermediate frequencies of a spiteful genotype (as seen in both theoretical and empirical studies; Inglis et al. 2009) should be attenuated or removed when spiteful cooperators compete against cheats. Virulence models (including those cited above) typically assume that virulence is simply a positive function of within-host growth rate, and when we measured density of bacteria within caterpillars, our results were entirely consistent with our model prediction. Both cooperative strains (spiteful/nonspiteful) displayed a positive curvilinear relationship between starting frequency and bacterial density after 8 h growth when in competition with susceptible cheats (linear term F1, 95= 43.15, P < 0.0001; quadratic term F1, 93= 4.65, P < 0.034), with nonspiteful cooperators reaching overall higher densities (F1, 94= 75.56, P < 0.0001) (Fig. 6A). This positive monotonic relationship between in vivo growth rate and cooperator frequency is consistent with theory (including our model) (Brown et al. 2002; West and Buckling 2003) and experimental results (Harrison et al. 2006). Crucially, there was no evidence of reduced density at intermediate frequencies of spiteful cooperators, as has been observed under almost identical experimental conditions when the spiteful cooperator competed against the susceptible cooperator used in this study (Inglis et al. 2009).

Bottom Line: Social interactions have been shown to play an important role in bacterial evolution and virulence.These results confirm the ecological and evolutionary importance of considering multiple social traits simultaneously.Moreover, our results are consistent with recent theory regarding the invasion conditions for strong reciprocity (helping cooperators and harming noncooperators).

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oxford, Oxford, OX1 3PS, United Kingdom. fredrik.inglis@env.ethz.ch

Show MeSH