Protist predation can favour cooperation within bacterial species

Here, we studied how protist predation affects cooperation in the opportunistic pathogen bacterium Pseudomonas aeruginosa, which uses quorum sensing (QS) cell-to-cell signalling to regulate the production of public goods. By competing wild-type bacteria with QS mutants (cheats), we show that a functioning QS system confers an elevated resistance to predation. Surprisingly, cheats were unable to exploit this resistance in the presence of cooperators, which suggests that resistance does not appear to result from activation of QS-regulated public goods. Instead, elevated resistance of wild-type bacteria was related to the ability to form more predation-resistant biofilms. This could be explained by the expression of QS-regulated resistance traits in densely populated biofilms and floating cell aggregations, or alternatively, by a pleiotropic cost of cheating where less resistant cheats are selectively removed from biofilms. These results show that trophic interactions among species can maintain cooperation within species, and have further implications for P. aeruginosa virulence in environmental reservoirs by potentially enriching the cooperative and highly infective strains with functional QS system

Evolutionary temperature compensation of carbon fixation in marine phytoplankton

The efficiency of carbon sequestration by the biological pump could decline in the coming decades because respiration tends to increase more with temperature than photosynthesis. Despite these differences in the short-term temperature sensitivities of photosynthesis and respiration, it remains unknown whether the long-term impacts of global warming on metabolic rates of phytoplankton can be modulated by evolutionary adaptation. We found that respiration was consistently more temperature dependent than photosynthesis across 18 diverse marine phytoplankton, resulting in universal declines in the rate of carbon fixation with short-term increases in temperature. Long-term experimental evolution under high temperature reversed the short-term stimulation of metabolic rates, resulting in increased rates of carbon fixation. Our findings suggest that thermal adaptation may therefore have an ameliorating impact on the efficiency of phytoplankton as primary mediators of the biological carbon pump

Competition and dispersal in Pseudomonas aeruginosa

Dispersal plays a crucial role in a range of evolutionary and ecological processes; hence there is strong motivation to understand its evolution. One key prediction is that the relative benefits of dispersal should be greater when dispersing away from close relatives, because in this case dispersal has the additional benefit of alleviating competition with individuals who share the same dispersal alleles. We tested this prediction for the first time using experimental populations of the opportunistic pathogen Pseudomonas aeruginosa. We measured the fitness of isogenic genotypes that differed only in their dispersal behaviors in both clonal and mixed populations. Consistent with theory, the benefit of dispersal was much higher in clonal populations, and this benefit decreased with increasing growth rate costs associated with dispersal

Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited

Population mixing promotes arms race host-parasite coevolution

Open access article. Please cite the published version available on the Royal Society web site by following the DOI above.The consequences of host-parasite coevolution are highly contingent on the qualitative coevolutionary dynamics: whether selection fluctuates (fluctuating selection dynamic; FSD), or is directional towards increasing infectivity/resistance (arms race dynamic; ARD). Both genetics and ecology can play an important role in determining whether coevolution follows FSD or ARD, but the ecological conditions under which FSD shifts to ARD, and vice versa, are not well understood. The degree of population mixing is thought to increase host exposure to parasites, hence selecting for greater resistance and infectivity ranges, and we hypothesize this promotes ARD. We tested this by coevolving bacteria and viruses in soil microcosms and found that population mixing shifted bacteria-virus coevolution from FSD to ARD. A simple theoretical model produced qualitatively similar results, showing that mechanisms that increase host exposure to parasites tend to push dynamics towards ARD. The shift from FSD to ARD with increased population mixing may help to explain variation in coevolutionary dynamics between different host-parasite systems, and more specifically the observed discrepancies between laboratory and field bacteria-virus coevolutionary studies.Natural Environment Research Council (NERC)Marie Curie Intra-European Fellowship (FP7)The Royal Societ

Virus satellites drive viral evolution and ecology

Virus satellites are widespread subcellular entities, present both in eukaryotic and in prokaryotic cells. Their modus vivendi involves parasitism of the life cycle of their inducing helper viruses, which assures their transmission to a new host. However, the evolutionary and ecological implications of satellites on helper viruses remain unclear. Here, using staphylococcal pathogenicity islands (SaPIs) as a model of virus satellites, we experimentally show that helper viruses rapidly evolve resistance to their virus satellites, preventing SaPI proliferation, and SaPIs in turn can readily evolve to overcome phage resistance. Genomic analyses of both these experimentally evolved strains as well as naturally occurring bacteriophages suggest that the SaPIs drive the coexistence of multiple alleles of the phage-coded SaPI inducing genes, as well as sometimes selecting for the absence of the SaPI depressing genes. We report similar (accidental) evolution of resistance to SaPIs in laboratory phages used for Staphylococcus aureus typing and also obtain the same qualitative results in both experimental evolution and phylogenetic studies of Enterococcus faecalis phages and their satellites viruses. In summary, our results suggest that helper and satellite viruses undergo rapid coevolution, which is likely to play a key role in the evolution and ecology of the viruses as well as their prokaryotic hosts

Selection on non-social traits limits the invasion of social cheats

While the conditions that favour the maintenance of cooperation have been extensively investigated, the significance of non-social selection pressures on social behaviours has received little attention. In the absence of non-social selection pressures, patches of cooperators are vulnerable to invasion by cheats. However, we show both theoretically, and experimentally with the bacterium Pseudomonas fluorescens, that cheats may be unable to invade patches of cooperators under strong non-social selection (both a novel abiotic environment and to a lesser extent, the presence of a virulent parasite). This is because beneficial mutations are most likely to arise in the numerically dominant cooperator population. Given the ubiquity of novel selection pressures on microbes, these results may help to explain why cooperation is the norm in natural populations of microbes

Spatial heterogeneity lowers rather than increases host-parasite specialization

Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host–parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ϕ2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host–parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host–parasite specialization

The impact of resource availability on bacterial resistance to phages in soil

This is the final version of the article. Available from Public Library of Science via the DOI in this recordResource availability can affect the coevolutionary dynamics between host and parasites, shaping communities and hence ecosystem function. A key finding from theoretical and in vitro studies is that host resistance evolves to greater levels with increased resources, but the relevance to natural communities is less clear. We took two complementary approaches to investigate the effect of resource availability on the evolution of bacterial resistance to phages in soil. First, we measured the resistance and infectivity of natural communities of soil bacteria and phage in the presence and absence of nutrient-providing plants. Second, we followed the real-time coevolution between defined bacteria and phage populations with resource availability manipulated by the addition or not of an artificial plant root exudate. Increased resource availability resulted in increases in bacterial resistance to phages, but without a concomitant increase in phage infectivity. These results suggest that phages may have a reduced impact on the control of bacterial densities and community composition in stable, high resource environments.The work was supported by NERC, the AXA research fund, BBSRC, the Royal Society (A.B.), and European Research Council funding under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 268504 (K.J.G.)

Host-parasite fluctuating selection in the absence of specificity

Fluctuating selection driven by coevolution between hosts and parasites is important for the generation of host and parasite diversity across space and time. Theory has focused primarily on infection genetics, with highly specific ‘matching allele’ frameworks more likely to generate fluctuating selection dynamics (FSD) than ‘gene-for-gene’ (generalist-specialist) frameworks. However, the environment, ecological feedbacks, and life-history characteristics may all play a role in determining when FSD occurs. Here, we develop eco- evolutionary models with explicit ecological dynamics to explore the ecological, epidemiological and host life-history drivers of FSD. Our key result is to demonstrate for the first time that specificity between hosts and parasites is not required to generate FSD. Furthermore, highly specific host-parasite interactions produce unstable, less robust stochastic fluctuations in contrast to interactions that lack specificity altogether or those that vary from generalist to specialist, which produce predictable limit cycles. Given the ubiquity of ecological feedbacks and the variation in the nature of specificity in host parasite interactions, our work emphasizes the underestimated potential for host- parasite coevolution to generate fluctuating selection