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Angus Buckling

Publications and source records attributed to Angus Buckling.

At least 19 recordsLinked to original sources

Differential impact of simultaneous migration on coevolving hosts and parasites.

BACKGROUND: The dynamics of antagonistic host-parasite coevolution are believed to be crucially dependent on the rate of migration between populations. We addressed how the rate of simultaneous migration of host and parasite affected resistance and infectivity evolution of coevolving meta-populations of the bacterium Pseudomonas fluorescens and a viral parasite (bacteriophage). The increase in genetic variation resulting from small amounts of migration is expected to increase rates of adaptation of both host and parasite. However, previous studies suggest phages should benefit more from migration than bacteria; because in the absence of migration, phages are more genetically limited and have a lower evolutionary potential compared to the bacteria. RESULTS: The results supported the hypothesis: migration increased the resistance of bacteria to their local (sympatric) hosts. Moreover, migration benefited phages more than hosts with respect to 'global' (measured with respect to the whole range of migration regimes) patterns of resistance and infectivity, because of the differential evolutionary responses of bacteria and phage to different migration regimes. Specifically, we found bacterial global resistance peaked at intermediate rates of migration, whereas phage global infectivity plateaued when migration rates were greater than zero. CONCLUSION: These results suggest that simultaneous migration of hosts and parasites can dramatically affect the interaction of host and parasite. More specifically, the organism with the lower evolutionary potential may gain the greater evolutionary advantage from migration.

Biological Evolution↗

Character displacement promotes cooperation in bacterial biofilms.

Resource competition within a group of cooperators is expected to decrease selection for cooperative behavior but can also result in diversifying selection for the use of different resources, which in turn could retard the breakdown of cooperation. Diverse groups are likely to be less susceptible to invasion by noncooperating social cheats: First, competition repression resulting from character displacement may provide less of a selective advantage to cheating; second, cheats may trade off the ability to exploit cooperators that specialize in one type of resource against cooperators that specialize in another ; third, diverse communities of any kind may have higher invasion resistance because there are fewer resources available for an invader to use . Furthermore, diverse groups are likely to be more productive than clonal groups if a wider range of total resources are being used . We addressed these issues by using the cooperative trait of biofilm formation in Pseudomonas fluorescens. Character displacement through resource competition evolved within biofilms; productivity increased with increasing character displacement, and diverse biofilms were less susceptible to invasion by cheats. These results demonstrate that diversification into different ecological niches can minimize selection against cooperation in the face of local resource competition.

Biofilms↗

Cooperation and virulence in acute Pseudomonas aeruginosa infections.

BACKGROUND: Efficient host exploitation by parasites is frequently likely to depend on cooperative behaviour. Under these conditions, mixed-strain infections are predicted to show lower virulence (host mortality) than are single-clone infections, due to competition favouring non-contributing social 'cheats' whose presence will reduce within-host growth. We tested this hypothesis using the cooperative production of iron-scavenging siderophores by the pathogenic bacterium Pseudomonas aeruginosa in an insect host. RESULTS: We found that infection by siderophore-producing bacteria (cooperators) results in more rapid host death than does infection by non-producers (cheats), and that mixtures of both result in intermediate levels of virulence. Within-host bacterial growth rates exhibited the same pattern. Crucially, cheats were more successful in mixed infections compared with single-clone infections, while the opposite was true of cooperators. CONCLUSION: These data demonstrate that mixed clone infections can favour the evolution of social cheats, and thus decrease virulence when parasite growth is dependent on cooperative behaviours.

Animals↗

Antagonistic coevolution with parasites increases the cost of host deleterious mutations.

The fitness consequences of deleterious mutations are sometimes greater when individuals are parasitized, hence parasites may result in the more rapid purging of deleterious mutations from host populations. The significance of host deleterious mutations when hosts and parasites antagonistically coevolve (reciprocal evolution of host resistance and parasite infectivity) has not previously been experimentally investigated. We addressed this by coevolving the bacterium Pseudomonas fluorescens and a parasitic bacteriophage in laboratory microcosms, using bacteria with high and low mutation loads. Directional coevolution between bacterial resistance and phage infectivity occurred in all populations. Bacterial population fitness, as measured by competition experiments with ancestral genotypes in the absence of phage, declined with time spent coevolving. However, this decline was significantly more rapid in bacteria with high mutation loads, suggesting the cost of bacterial resistance to phage was greater in the presence of deleterious mutations (synergistic epistasis). As such, resistance to phage was more costly to evolve in the presence of a high mutation load. Consistent with these data, bacteria with high mutation loads underwent less rapid directional coevolution with their phage populations, and showed lower levels of resistance to their coevolving phage populations. These data suggest that coevolution with parasites increases the rate at which deleterious mutations are purged from host populations.

Directed Molecular Evolution↗

Hypermutability impedes cooperation in pathogenic bacteria.

When the supply of beneficial mutations limits adaptation, bacterial mutator alleles can reach high frequencies by hitchhiking with advantageous mutations. However, when populations are well adapted to their environments, the increased rate of deleterious mutations makes hypermutability selectively disadvantageous. Here, we consider a further cost of hypermutability: its potential to break down cooperation (group-beneficial behavior that is costly to the individual). This probably occurs for three reasons. First, an increased rate at which 'cheating' genotypes are generated; second, an increased probability of producing efficient cheats; and third, a decrease in relatedness (not addressed in the present study). We used Pseudomonas aeruginosa's production of extracellular iron-scavenging molecules, siderophores, to determine if cheating evolved more readily in mutator populations. Siderophore production is costly to individual bacteria but benefits all nearby cells. Siderophore-deficient cheats therefore have a selective advantage within populations. We observed the de novo evolution and subsequent increase in frequency of siderophore cheats within both wild-type and mutator populations for 200 generations. Cheats appeared and increased in frequency more rapidly in mutator populations. The presence of cheats was costly to the group, as shown by a negative correlation between cheat frequency and population density.

Colony Count, Microbial↗

The effect of migration on local adaptation in a coevolving host-parasite system.

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites; that is, the greater infectivity of local parasites than foreign parasites on local hosts. Such parasite specialization on local hosts has implications for human health and agriculture. By contrast with classic single-species population-genetic models, theory indicates that parasite migration between subpopulations might increase parasite local adaptation, as long as migration does not completely homogenize populations. To test this hypothesis we developed a system-specific mathematical model and then coevolved replicate populations of the bacterium Pseudomonas fluorescens and a parasitic bacteriophage with parasite only, with host only or with no migration. Here we show that patterns of local adaptation have considerable temporal and spatial variation and that, in the absence of migration, parasites tend to be locally maladapted. However, in accord with our model, parasite migration results in parasite local adaptation, but host migration alone has no significant effect.

Adaptation, Physiological↗

The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa.

Pseudomonas aeruginosa is an opportunistic human pathogen that colonizes the lungs of cystic fibrosis (CF) patients. CF lungs often contain a diverse range of P. aeruginosa phenotypes, some of which are likely to contribute to the persistence of infection, yet the causes of diversity are unclear. While the ecological heterogeneity of the lung environment and therapeutic regimes are probable factors, a role for parasitic bacteriophage cannot be ruled out. Parasites have been implicated as a key ecological variable driving the evolution of diversity in host populations. PP7 drove cycles of morphological diversification in host populations of P. aeruginosa due to the de novo evolution of small-rough colony variants that coexisted with large diffuse colony morph bacteria. In the absence of phage, bacteria only displayed the large diffuse colony morphology of the wild-type. Further assays revealed there to be two distinct types of resistant bacteria; these had very different ecological phenotypes, yet each carried a cost of resistance.

Colony Count, Microbial↗

Surface plasmon resonance shows that type IV pili are important in surface attachment by Pseudomonas aeruginosa.

Type IV pili have been shown to play a role in the early stages of bacterial biofilm formation, but not in initial bacterial attachment. Here, using the surface analytical technique, surface plasmon resonance (SPR), we follow the attachment of the bacterium Pseudomonas aeruginosa in real time. In contrast to previous studies, we show that type IV pili mutants are defective in attachment. Both mutants lacking pili (pilA), and those possessing an overabundance of pili (pilT), showed reduced SPR measured attachment compared with the wild-type PAO1 strain. Both pil mutants also showed reduced pathogenicity in a model insect host, as measured by percentage mortality after 24h. SPR revealed differences in the kinetics of attachment between pilA and pilT, differences obscured by endpoint assays using crystal violet stain. These results highlight the power of SPR in monitoring bacterial attachment in real time and also demonstrate an additional role for type IV pili beyond bacterial aggregation and micro-colony formation.

Fimbriae, Bacterial↗

Microbial experiments on adaptive landscapes.

The adaptive landscape is one of the most widely used metaphors in evolutionary biology. It is created by plotting fitness against phenotypes or genotypes in a given environment. The shape of the landscape is crucial in predicting the outcome of evolution: whether evolution will result in populations reaching predictable end points, or whether multiple evolutionary outcomes are more likely. In a more applied sense, the landscape will determine whether organisms will evolve to lose 'costly' resistance to antibiotics, herbicides or pesticides when the use of the control agent is stopped. Laboratory populations of microbes allow evolution to be observed in real time and, as such, provide key insights into the topology of adaptive landscapes.

Adaptation, Biological↗

Cooperation and competition in pathogenic bacteria.

Explaining altruistic cooperation is one of the greatest challenges for evolutionary biology. One solution to this problem is if costly cooperative behaviours are directed towards relatives. This idea of kin selection has been hugely influential and applied widely from microorganisms to vertebrates. However, a problem arises if there is local competition for resources, because this leads to competition between relatives, reducing selection for cooperation. Here we use an experimental evolution approach to test the effect of the scale of competition, and how it interacts with relatedness. The cooperative trait that we examine is the production of siderophores, iron-scavenging agents, in the pathogenic bacterium Pseudomonas aeruginosa. As expected, our results show that higher levels of cooperative siderophore production evolve in the higher relatedness treatments. However, our results also show that more local competition selects for lower levels of siderophore production and that there is a significant interaction between relatedness and the scale of competition, with relatedness having less effect when the scale of competition is more local. More generally, the scale of competition is likely to be of particular importance for the evolution of cooperation in microorganisms, and also the virulence of pathogenic microorganisms, because cooperative traits such as siderophore production have an important role in determining virulence.

Altruism↗

Bacteriocins, spite and virulence.

There has been much interest in using social evolution theory to predict the damage to a host from parasite infection, termed parasite virulence. Most of this work has focused on how high kinship between the parasites infecting a host can select for more prudent exploitation of the host, leading to a negative relationship between virulence and parasite kinship. However, it has also been shown that if parasites can cooperate to overcome the host, then high parasite kinship within hosts can select for greater cooperation and higher growth rates, hence leading to a positive relationship between virulence and parasite kinship. We examine the impact of a spiteful behaviour, chemical (bacteriocin) warfare between microbes, on the evolution of virulence, and find a new relationship: virulence is maximized when the frequency of kin among parasites' social partners is low or high, and is minimized at intermediate values. This emphasizes how biological details can fundamentally alter the qualitative nature of theoretical predictions made by models of parasite virulence.

Bacteria↗

Interference competition and parasite virulence.

Within-host competition between parasites, a consequence of infection by multiple strains, is predicted to favour rapid host exploitation and greater damage to hosts (virulence). However, the inclusion of biological variables can drastically change this relationship. For example, if competing parasite strains produce toxins that kill each other (interference competition), their growth rates and virulence may be reduced relative to single-strain infections. Bacteriocins are antimicrobial toxins produced by bacteria that target closely related strains and species, and to which the producing strain is immune. We investigated competition between bacteriocin-producing, insect-killing bacteria (Photorhabdus and Xenorhabdus) and how this competition affected virulence in caterpillars. Where one strain could kill the other, and not vice versa, the non-killing strain was competitively excluded, and insect mortality was the same as that of the killing strain alone. However, when caterpillars were multiply infected by strains that could kill each other, we did not observe competitive exclusion and their virulence was less than single-strain infections. The ubiquity and diversity of bacteriocins among pathogenic bacteria suggest mixed infections will be, on average, less virulent than single infections.

Animals↗

The effect of spatial heterogeneity and parasites on the evolution of host diversity.

Both spatial heterogeneity and exploiters (parasites and predators) have been implicated as key ecological factors driving population diversification. However, it is unclear how these factors interact. We addressed this question using the common plant-colonizing bacterium Pseudomonas fluorescens, which has been shown to diversify rapidly into spatial niche-specialist genotypes when propagated in laboratory microcosms. Replicate populations were evolved in spatially homogeneous and heterogeneous environments (shaken and static microcosms, respectively) with and without viral parasites (bacteriophage) for approximately 60 bacterial generations. Consistent with previous findings, exploiters reduced diversity in heterogeneous environments by relaxing the intensity of resource competition. By contrast, exploiters increased diversity in homogeneous environments where there was little diversification through resource competition. Competition experiments revealed this increase in diversity to be the result of fitness trade-offs between exploiter resistance and competitive ability. In both environments, exploiters increased allopatric diversity, presumably as a result of divergent selection for resistance between populations. Phage increased total diversity in homogeneous environments, but had no net effect in heterogeneous environments. Such interactions between key ecological variables need to be considered when addressing diversification and coexistence in future studies.

Animals↗

Big questions, small worlds: microbial model systems in ecology.

Although many biologists have embraced microbial model systems as tools to address genetic and physiological questions, the explicit use of microbial communities as model systems in ecology has traditionally been more restricted. Here, we highlight recent studies that use laboratory-based microbial model systems to address ecological questions. Such studies have significantly advanced our understanding of processes that have proven difficult to study in field systems, including the genetic and biochemical underpinnings of traits involved in ecological interactions, and the ecological differences driving evolutionary change. It is the simplicity of microbial model systems that makes them such powerful tools for the study of ecology. Such simplicity enables the high degrees of experimental control and replication that are necessary to address many questions that are inaccessible through field observation or experimentation.

Journal Article↗