Publications by year
In Press
Williamson J, Matthews AC, Raymond B (In Press). Competition and co-association, but not phosphorous availability, shape the benefits of phosphate solubilising root bacteria for maize (Zea mays).
Abstract:
Competition and co-association, but not phosphorous availability, shape the benefits of phosphate solubilising root bacteria for maize (Zea mays).
Predicting the conditions under which rhizobacteria benefit plant growth remains challenging. Here we tested the hypothesis that benefits from inoculation with phosphate-solubilising rhizobacteria will depend upon two environmental conditions: phosphate availability and competition between bacteria. Maize-associated rhizobacteria with varying phosphate solubilisation ability were used in experiments in soil, sterilised soil and gnotobiotic microcosms under conditions of varying orthophosphate availability, while we manipulated intensity of competition by varying the number of isolates in plant inocula. Growth promotion by microbes did not depend on phosphate availability but was affected by interactions between inoculants: beneficial effects of one Serratia isolate were detectable only when plants were inoculated with a single strain and beneficial effects of a competition sensitive Rhizobium was only detectable in sterilised soil or in microcosms inoculated with single strains. Moreover, microcosm experiments suggested that facilitation of a parasitic isolate, not competitive interactions between bacteria, prevented plants from gaining benefits from a potential mutualist. Competition and facilitation affected colonization of plants in microcosms but growth promotion by Serratia was more affected by inoculation treatment than culturable densities on roots. Experimental manipulation of seed inocula can reveal whether plant growth stimulation is robust with respect to competition, as well as the ecological strategies of different rhizobacteria. From an applied perspective, phosphate solubilisation may not provide the mechanism for bacterial growth promotion but may indicate mutualistic potential due to phylogenetic associations. Importantly, benefits to plants are vulnerable to interactions between rhizobacteria and may not persist in mixed inoculations.
Abstract.
Erdos Z, Studholme DJ, Raymond B, Sharma M (In Press). De-novo genome assembly for Akanthomyces muscarius, a biocontrol agent of insect agricultural pests.
Abstract:
De-novo genome assembly for Akanthomyces muscarius, a biocontrol agent of insect agricultural pests
The entomopathogenic fungus Akanthomyces muscarius is used as a biological control agent for the management of insect pests in agriculture. It also presents a potential model for studying host-pathogen interactions and the evolution of virulence in a laboratory setting. Here, we present the first high-quality genome sequence for A. muscarius. We used long- and short-read sequencing to assemble a sequence of 36.1 Mb with an N50 of 4.9 Mb. Genome annotation predicts 12,347 genes, with 96.6 % completeness based on the core Hypocrealen gene set (Benchmarking Universal Single-Copy Orthologs). The first high-quality assembly and annotation of A. muscarius presented in this study provide a powerful tool for further research on this commercially important species.
Abstract.
Erdos Z, Studholme DJ, Raymond B, Sharma M (In Press). De-novo genome assembly for Akanthomyces muscarius, a biocontrol agent of insect agricultural pests.
Abstract:
De-novo genome assembly for Akanthomyces muscarius, a biocontrol agent of insect agricultural pests
The entomopathogenic fungus Akanthomyces muscarius is commonly used in agriculture to manage insect pests. Besides its use as a commercially important biological control agent, it also presents a potential model for studying host-pathogen interactions and virulence evolution in a laboratory setting. Here, we describe the first high-quality genome sequence for A. muscarius. We used long- and short-read sequencing to assemble a sequence of 36.1 Mb with an N50 of 4.9 Mb. Genome annotation predicts 12,347 genes, with 96.6 % completeness based on the core Hypocrealen gene set (Benchmarking Universal Single-Copy Orthologs). The high-quality assembly and annotation of A. muscarius presented in this study provide an essential tool for future research on this commercially important species.
Abstract.
Raymond B, Lewis GC (In Press). Evaluation of endophyte infection of Lolium perenne on molluscan herbivory. Annals of Applied Biology (Supplement- Tests of Agrochemicals & Cultivars), 126, 104-105.
Somerville J, Zhou L, Raymond B (In Press). Gnotobiotic Rearing and Controlled Infection with Gut Symbionts Improve Adult Fitness in Transgenic Diamondback Moth, <em>Plutella xylostella</em>.
Abstract:
Gnotobiotic Rearing and Controlled Infection with Gut Symbionts Improve Adult Fitness in Transgenic Diamondback Moth, <em>Plutella xylostella</em>
Mass insect rearing can have a range of applications, for example in biological control of insects. Since the performance of released biological control agents determines efficacy, the competitive fitness of insects post release is a key variable. Here, we tested whether inoculation with a gut symbiont, Enterobacter cloacae, and gnotobiotic rearing of larvae could improve insect growth and male competitive fitness of a transgenic diamondback moth, which has shown variation in fitness when reared in different insectaries. All larvae were readily infected with the focal symbiont. Under gnotobiotic rearing pupal weights were reduced and there was a marginal reduction in larval survival. However, gnotobiotic rearing substantially improved the fitness of transgenic males. In addition, in gnotobiotic conditions, inoculation with the gut symbiont increased pupal weights and male fitness, increasing the proportion of transgenic progeny from 20 to 30% relative to symbiont-free insects. Gnotobiotic conditions may improve the fitness of transgenic males by excluding microbial contaminants, while symbiont inoculation could further improve fitness by providing additional protection against infections, or by normalizing insect physiology. The simple innovation of incorporating antibiotic into diet, and inoculating insects with symbiotic bacteria that are resistant to that antibiotic, could provide a readily transferable tool for other insect rearing systems.
Abstract.
Erdos Z, Halswell P, Matthews A, Raymond B (In Press). Laboratory sprayer for testing of microbial biocontrol agents: design and calibration.
Abstract:
Laboratory sprayer for testing of microbial biocontrol agents: design and calibration
AbstractThe lack of commercially available low-cost laboratory spraying equipment for testing microbial control agents can hinder advancement in the field of biocontrol. This study presents an inexpensive, portable sprayer that is calibrated utilizing laboratory consumables. The computer aided design files are made available so that it is freely modifiable and can be used for machine routing or 3D printing. Bioassay data was obtained by spraying Myzus persicae with spores of entomopathogenic fungi. Observed variation in droplet deposition within tested pressure and volume settings, and spore deposition within sprayed concentrations were low. Bioassay results show reproducible mortality for the tested doses.
Abstract.
Zhou L, Slamti L, Lereclus D, Raymond B (In Press). Optimal response to quorum-sensing signals varies in different host environments with different pathogen group size.
Abstract:
Optimal response to quorum-sensing signals varies in different host environments with different pathogen group size
AbstractThe persistence of genetic variation in master regulators of gene expression, such as quorum-sensing systems, is hard to explain. Here, we investigated two alternative hypotheses for the prevalence of polymorphic quorum-sensing in Gram-positive bacteria,i.e. the use of different signal / receptor pairs (‘pherotypes’) to regulate the same functions. First, social interactions between pherotypes or ‘facultative cheating’ may favour rare variants that exploit the signals of others. Second, different pherotypes may increase fitness in different environments. We evaluated these hypotheses in the invertebrate pathogenBacillus thuringiensis, using three pherotypes expressed in a common genetic background. Facultative cheating occurred in homogenized hosts, in contrast, rare pherotypes had reduced fitness in naturalistic infections. There was clear support for environment-dependent fitness: pherotypes varied in responsiveness to signals and in mean competitive fitness. Notably, competitive fitness varied with group size: the pherotype with highest responsiveness to signals performed best in smaller hosts where infections have a lower pathogen group size. Less responsive pherotypes performed best in larger hosts. Results using homogenized insect media fit with the expectation of facultative cheating and social evolution theory, but results from naturalist oral infections do not fit many of the predictions from this body of theory. In this system, low signal abundance appears to limit fitness in hosts while the optimal level of response to signals varies in different host environments.ImportanceQuorum sensing describes the ability of microbes to alter gene regulation according to their local population size. Some successful theory suggests that this is a form of cooperation: investment in shared products is only worthwhile if there are sufficient bacteria making the same product. This theory can explain the genetic diversity in these signaling systems in Gram-positive bacteria such asBacillusandStaphylococcus. The possible advantages gained by rare genotypes (which can exploit the products of their more common neighbours) could explain why different genotypes can coexist. We show that while these social interactions can occur in simple laboratory experiments they do not occur in naturalistic infections using an invertabrate pathogen,Bacillus thuringiensis. Instead our results suggest that different genotypes are adapted to different-sized hosts. Overall, social models are not easily applied to this system implying that a new explanation for this form of quorum sensing is required.
Abstract.
Dimitriu T, Marchant L, Buckling A, Raymond B (In Press). Plasmid transfer is biased towards close kin in bacteria from natural populations.
Abstract:
Plasmid transfer is biased towards close kin in bacteria from natural populations
AbstractPlasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Here we investigate the importance of genetic similarity between naturally co-occurringEscherichia coliisolates in the transfer of two plasmids (narrow-host-range R1 and broad-host-range RP4). We uncovered extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive plasmids. Overall, transfer was strongly biased towards clone-mates, but not correlated to genetic distance between donors and recipients. Transfer was limited by the presence of a functional restriction-modification system in recipients, thus bias towards kin might be explained by sharing of identical restriction systems. Such conjugation within lineages sets the stage for longer-term pair-wise coevolutionary interactions between plasmids and bacterial hosts.
Abstract.
Dimitriu T, Souissi W, Morwool P, Darby A, Crickmore N, Raymond B (In Press). Re-inventing pathogen passage for social microbes.
Abstract:
Re-inventing pathogen passage for social microbes
AbstractPassage experiments that sequentially infect hosts with parasites have long been used to manipulate virulence. However, in many invertebrate pathogens passage has been applied naively without a full theoretical understanding of how best to select for increased virulence. This has led to very mixed results. Understanding the evolution of virulence is complex because selection on parasites occurs across multiple spatial scales with potentially different conflicts operating on parasites with different life-histories. For example, in social microbes, strong selection on replication rate within hosts can lead to cheating and loss of virulence, because investment in public goods virulence reduces replication rate. In contrast, selection acting at a between host scale maintains virulence by selecting on parasite population size. In this study we tested how different scales of selection and varying mutation supply affect evolution of virulence against resistant hosts in the specialist insect pathogen Bacillus thuringiensis. aiming to optimize methods for strain improvement against a difficult to kill insect target. We show that selection for infectivity using competition between sub-populations in a metapopulation prevents social cheating, acts to retain key virulence plasmids and facilitates increased virulence. Increased virulence was associated with reduced efficiency of sporulation, and loss of function in putative regulatory genes but not with altered expression of known virulence factors. Selection in a metapopulation provides a broadly applicable tool for improving the efficacy of biocontrol agents. Moreover, a structured host population can facilitate artificial selection on infectivity, while selection on life history traits such as faster replication or larger population sizes can reduce virulence can reduce virulence in social microbes.
Abstract.
Raymond B, Matthews A, Erdos Z, Egleton M (In Press). Relative efficacy of biological control and cultural management for control of mollusc pests in cool climate vineyards. Biocontrol Science and Technology
White H, Sheppard S, Raymond B, Vos M, Pascoe B (In Press). Signatures of selection in core and accessory genomes indicate different. ecological drivers of diversification among Bacillus cereus clades.
Molecular EcologyAbstract:
Signatures of selection in core and accessory genomes indicate different. ecological drivers of diversification among Bacillus cereus clades
Bacterial clades are often ecologically distinct, despite extensive horizontal gene transfer (HGT). How selection works on different parts of bacterial pan-genomes to drive and maintain the emergence of clades is unclear. Focussing on the three largest clades in the diverse and well-studied Bacillus cereus sensu lato group, we identified clade-specific core genes (present in all clade members) and then used clade-specific allelic diversity to identify genes under purifying and diversifying selection. Clade-specific accessory genes (present in a subset of strains within a clade) were characterized as being under selection using presence/absence in specific clades. Gene ontology analyses of genes under selection revealed that different core genes and gene functions were enriched in different clades. Furthermore, some gene functions were enriched only amongst clade-specific core or accessory genomes. Genes under purifying selection were often clade-specific, while genes under diversifying selection showed signs of frequent HGT. These patterns are consistent with different selection pressures acting on both the core and accessory genomes of different clades and can lead to ecological divergence in both cases. Examining variation in allelic diversity allows us to uncover genes under clade-specific selection, allowing ready identification of strains and their ecological niche.
Abstract.
Mikonranta L, Buckling A, Jalasvuori M, Raymond B (In Press). Targeting antibiotic resistant bacteria with phages reduces bacterial density in an insect host.
Abstract:
Targeting antibiotic resistant bacteria with phages reduces bacterial density in an insect host
Phage therapy is attracting growing interest among clinicians as antibiotic resistance continues becoming harder to control. However, clinical trials and animal model studies on bacteriophage treatment are still scarce and results on the efficacy vary. Recent research suggests that using traditional antimicrobials in concert with phage could have desirable synergistic effects that hinder the evolution of resistance. Here, we present a novel insect gut model to study phage-antibiotic interaction in a system where antibiotic resistance initially exists in very low frequency and phage specifically targets the resistance bearing cells. We demonstrate that while phage therapy could not reduce the frequency of target bacteria in the population during positive selection by antibiotics, it alleviated the antibiotic induced blooming by lowering the overall load of resistant cells. The highly structured gut environment had pharmacokinetic effects on both phage and antibiotic dynamics compared to in vitro: antibiotics did not reduce the overall amount of bacteria, demonstrating a simple turnover of gut flora from non-resistant to resistant population with little cost. The results imply moderate potential for using phage as an aid to target antibiotic resistant gut infections, and question the usefulness of in vitro inferences.
Abstract.
2023
Dimitriu T, Souissi W, Morwool P, Darby A, Crickmore N, Raymond B (2023). Selecting for infectivity across metapopulations can increase virulence in the social microbe. <i>Bacillus thuringiensis</i>. Evolutionary Applications
2022
Raymond B, Erdos Z (2022). Passage and the evolution of virulence in invertebrate pathogens: Fundamental and applied perspectives.
J Invertebr Pathol,
187Abstract:
Passage and the evolution of virulence in invertebrate pathogens: Fundamental and applied perspectives.
Understanding the ecological and genetic factors that determine the evolution of virulence has broad value for invertebrate pathology. In addition to helping us understand the fundamental biology of our study organisms this body of theory has important applications in microbial biocontrol. Experimental tests of virulence theory are often carried out in invertebrate models and yet theory rarely informs applied passage experiments that aim to increase or maintain virulence. This review summarizes recent progress in this field with a focus on work most relevant to biological control: the virulence of invertebrate pathogens that are 'obligate killers' and which require cadavers for the production of infectious propagules. We discuss recent theory and fundamental and applied experimental evolution with bacteria, fungi, baculoviruses and nematodes. While passage experiments using baculoviruses have a long history of producing isolates with increased virulence, studies with other pathogens have not been so successful. Recent passage experiments that have applied evolution of virulence frameworks based on cooperation (kin selection) have produced novel methods and promising mutants with increased killing power. Evolution of virulence theory can provide plausible explanations for the varied results of passage experiments as well as a predictive framework for improving artificial selection.
Abstract.
Author URL.
Erdos Z (2022). Selection and improvement of insect pathogenic fungi for the control of multi-resistant aphids.
Abstract:
Selection and improvement of insect pathogenic fungi for the control of multi-resistant aphids
The entomopathogenic fungus (EPF) Akanthomyces muscarius has been used as a biocontrol agent for the management of insect pests in agriculture. Nevertheless, the licensing and commercial success of aphid biocontrol agents has been a challenge. This project had three main aims: test if this fungus could be used as a management tool for the control of insecticide resistant aphids (Myzus persicae); to test whether we could apply evolutionary theory to improve the properties of this species as biocontrol agents and finally to produce a high quality genome of this fungus as a resource for future use.
While we expected that pesticide resistant insects might have a fitness cost that would increase susceptibility to fungus, this proved not to be the case. In contrast, some susceptible clones, particularly those subject to decades of laboratory rearing, showed enhanced susceptibility to a fungal pathogen, but not reduced reproductive fitness, an observation consistent with down-regulation of costly immune functions in culture. Nevertheless, changes in susceptibility were small and overall, fungal pathogen control is compatible with insecticides and should not increase the selection pressure for resistance of M. persicae to chemical insecticides.
Experimental passage has been used to successfully increase virulence of insect pathogens. Passage experiments with EPF are relatively unexplored. Here we adopted a theory based approach and selected for speed of kill, pathogen yield and infectivity at different scales of competition in M. persicae. The selection experiment resulted in small but significant increases in virulence when compared to the ancestor, which also resulted in increased virulence against another aphid host, Brevicoryne brassicae. In addition, we also observed
increases in spore production on solid media and changes in timing of sporulation in some treatments. Changes in sporulation were unrelated to virulence showing that it is possible to produce more virulent mutants with improved sporulation characteristics.
We also present a new population genomic resource for A. muscarius comprising a high-quality genome assembly together with resequenced genomes of 13 experimentally selected lineages of this fungi.
The work presented here benefits industrial partners and stakeholders by providing novel methodologies for strain improvement of EPF and efficacy data of EPF on aphid genotypes resistant to synthetic insecticides. Increased use of biopesticides containing EPF can lead to a reduction in the use of chemical pesticides, increased biodiversity and reduced impacts on pollinators and other beneficial insects and could facilitate integrated biocontrol of difficult to manage aphid pests.
Abstract.
Forsyth J (2022). Use of lineage specific bacteriophage to counter antibiotic resistant Escherichia coli sequence type 131 (ST131).
Abstract:
Use of lineage specific bacteriophage to counter antibiotic resistant Escherichia coli sequence type 131 (ST131)
The emergence and rapid dissemination of multidrug resistant pathogens presents a huge and growing global concern. Escherichia coli (E. coli) sequence type (ST) 131, has been recognised as a major E. coli lineage responsible for the spread of multidrug resistance, and is a common cause of life-threatening infections in clinical settings. In recent years there has been increasing interest in the use of bacteriophages in the treatment of MDR infections. The use of bacteriophages with some breadth of host range can be desirable so that licensed products are able to target a range of clinical infections. Using a unique method of quantifying host range, we provide evidence that the type of environment sampled from, and the host strain used for isolation are both significant determinants of the host range of phages isolated. Using competition experiments we also provide evidence that by combining the selective pressure of phage predation with that imposed by the presence of a probiotic competitor, significant reductions in the fitness of the MDR pathogen ST131, can be achieved. Although fitness trade-offs resulting from bacteriophage resistance are predicted by life-history evolution, we demonstrate that resistant mutants do not pay a cost for resistance but instead appear to benefit from it with the relative fitness of resistant mutants greater than their susceptible counterparts. Overall, this study draws attention to the value of the environment as a source of naturally occurring antimicrobials, provides direction for future sampling attempts to promote the isolation of phage with the greatest therapeutic potential and demonstrates how the efficacy of such phage can be enhanced through their synergistic application with probiotic strains such as E. coli Nissle 1917. This study and those that follow will provide invaluable contributions to the ever-growing body of phage research that will ultimately form part of the solution in the fight against AMR.
Abstract.
2021
Erdos Z, Chandler D, Bass C, Raymond B (2021). Controlling insecticide resistant clones of the aphid, Myzus persicae, using the entomopathogenic fungus Akanthomyces muscarius: fitness cost of resistance under pathogen challenge.
Pest Manag Sci,
77(11), 5286-5293.
Abstract:
Controlling insecticide resistant clones of the aphid, Myzus persicae, using the entomopathogenic fungus Akanthomyces muscarius: fitness cost of resistance under pathogen challenge.
BACKGROUND: Biological control is a cornerstone of integrated pest management and could also play a key role in managing the evolution of insecticide resistance. Ecological theory predicts that the fitness cost of insecticide resistance can be increased under exposure to invertebrate natural enemies or pathogens, and can therefore increase the value of integrating biological control into pest management. In this study of the peach potato aphid, Myzus persicae, we aimed to identify whether insecticide resistance affected fitness and vulnerability of different aphid clones to the entomopathogenic fungus Akanthomyces muscarius. RESULTS: Insecticide resistant clones were found to be slightly less susceptible to the pathogen than susceptible clones. However, this pattern could also be explained by the influence of length of laboratory culture, which was longer in susceptible clones and was positively correlated with susceptibility to fungi. Furthermore, resistance status did not affect aphid development time or intrinsic rate of increase of aphids. Finally, in a cage trial the application of fungus did not increase the competitive fitness of insecticide resistant clone 'O'. CONCLUSION: We found no fitness cost in reproductive rate or pathogen susceptibility associated with chemical resistance in M. persicae. In contrast, some susceptible clones, particularly those subject to decades of laboratory rearing, showed enhanced susceptibility to a fungal pathogen, but not reduced reproductive fitness, an observation consistent with down-regulation of costly immune functions in culture. Overall, fungal pathogen control is compatible with insecticides and should not increase the selection pressure for resistance of M. persicae to chemical insecticides.
Abstract.
Author URL.
Matthews A, Raymond B (2021). Function is a better predictor of plant rhizosphere community membership than 16S phylogeny.
Abstract:
Function is a better predictor of plant rhizosphere community membership than 16S phylogeny
Rhizobacterial communities are important for plant health but we still have limited understanding of how they are constructed or how they can be manipulated. High throughput 16S rRNA sequencing provides good information on taxonomic composition, but remains an unreliable proxy for phenotypes. In this study, we tested the hypothesis that experimentally observed functional traits would be better predictors of community membership than phylogenetic origin. To test this hypothesis, we sampled communities on four plant species grown in two soil types and characterized 593 bacterial isolates in terms of antibiotic susceptibility, carbon metabolism, resource use, and plant growth-promoting traits. In support of our hypothesis we found that three of the four plant species had phylogenetically diverse, but functionally constrained communities. Notably communities did not grow best on complex media mimicking their host of origin, but were distinguished by variation in overall growth characteristics (copiotrophy/oligotrophy) and antibiotic susceptibility. These data, combined with variation in phylogenetic structure, suggest that different classes of traits (antagonistic competition or resource-based) are more important in different communities. This culture-based approach supports and complements the findings of a previous high-throughput 16S rRNA analysis of this experiment, and provides functional insights into the patterns observed with culture-independent methods.
Abstract.
Matthews A, Majeed A, Barraclough TG, Raymond B (2021). Function is a better predictor of plant rhizosphere community membership than 16S phylogeny.
Environ Microbiol,
23(10), 6089-6103.
Abstract:
Function is a better predictor of plant rhizosphere community membership than 16S phylogeny.
Rhizobacterial communities are important for plant health but we still have limited understanding of how they are constructed or how they can be manipulated. High-throughput 16S rRNA sequencing provides good information on taxonomic composition but remains an unreliable proxy for phenotypes. In this study, we tested the hypothesis that experimentally observed functional traits would be better predictors of community membership than phylogenetic origin. To test this hypothesis, we sampled communities on four plant species grown in two soil types and characterized 593 bacterial isolates in terms of antibiotic susceptibility, carbon metabolism, resource use and plant growth-promoting traits. In support of our hypothesis we found that three of the four plant species had phylogenetically diverse, but functionally constrained communities. Notably, communities did not grow best on complex media mimicking their host of origin but were distinguished by variation in overall growth characteristics (copiotrophy/oligotrophy) and antibiotic susceptibility. These data, combined with variation in phylogenetic structure, suggest that different classes of traits (antagonistic competition or resource-based) are more important in different communities. This culture-based approach supports and complements the findings of a previous high-throughput 16S rRNA analysis of this experiment and provides functional insights into the patterns observed with culture-independent methods.
Abstract.
Author URL.
Raymond B, Matthews A, Erdos Z, Egleton M (2021). Relative efficacy of biological control and cultural management for control of mollusc pests in cool climate vineyards: raw data and analysis code.
Abstract:
Relative efficacy of biological control and cultural management for control of mollusc pests in cool climate vineyards: raw data and analysis code
Restrictions on the use of synthetic molluscicides highlight the importance of developing alternative control methods. Nevertheless, biocontrol agents can be costlier and less effective than synthetic counterparts. One mean of increasing the efficacy of population suppression is to combine inundative biological control with habitat management to reduce population growth of target pests. Vineyards in the cool, wet climate of western England can suffer from outbreak densities of mollusc pests that damage expanding shoots, developing grapes and promote the transmission of fungal pathogens. In this study we combined the biocontrol agent Nemaslug - Phasmarhabditis hermaphrodita (Schneider) -with a simple habitat management approach (regular mowing) to suppress mollusc pests in vineyards in South Western England. Two sites were treated with NemaSlug and or mowing in a factorial design in early spring coinciding with bud burst and the start of mollusc growth and feeding. Mowing was effective management and resulted in the reduction of slug and snail populations and significantly less damaged vines. Nemaslug did not reduce slug numbers overall but did reduce bud damage, snail numbers and lowered the proportion of susceptible Deroceras spp in treated plot. However, effect sizes of nematode biocontrol were small, potentially because this product could not be applied to bare soil. Management practice for cool climate vineyards varies considerably from site to site. This study shows the value of simple habitat management for controlling a novel target and emphasizes how consideration of pest biology can lead to effective alternatives.
Abstract.
Hartley S, Smith RDJ, Kokotovich A, Opesen C, Habtewold T, Ledingham K, Raymond B, Rwabukwali CB (2021). Ugandan stakeholder hopes and concerns about gene drive mosquitoes for malaria control: new directions for gene drive risk governance. Malaria Journal, 20
2020
Manktelow CJ, White H, Crickmore N, Raymond B (2020). Divergence in environmental adaptation between terrestrial clades of the Bacillus cereus group.
FEMS Microbiol Ecol,
97(1).
Abstract:
Divergence in environmental adaptation between terrestrial clades of the Bacillus cereus group.
The Bacillus cereus group encompasses beneficial and harmful species in diverse niches and has a much debated taxonomy. Investigating whether selection has led to ecological divergence between phylogenetic clades can help understand the basis of speciation, and has implications for predicting biological safety across this group. Using three most terrestrial species in this group (B. cereus, Bacillus thuringiensis and Bacillus mycoides) we charactererized ecological specialization in terms of resource use, thermal adaptation and fitness in different environmental conditions and tested whether taxonomic species or phylogenetic clade best explained phenotypic variation. All isolates grew vigorously in protein rich media and insect cadavers, but exploitation of soil or plant derived nutrients was similarly weak for all. For B. thuringiensis and B. mycoides, clade and taxonomic species were important predictors of relative fitness in insect infections. Fully psychrotolerant isolates could outcompete B. thuringiensis in insects at low temperature, although psychrotolerance predicted growth in artificial media better than clade. In contrast to predictions, isolates in the Bacillus anthracis clade had sub-optimal growth at 37°C. The common ecological niche in these terrestrial B. cereus species is the ability to exploit protein rich resources such as cadavers. However, selection has led to different phylogenetic groups developing different strategies for accessing this resource. Thus, clades, as well as traditional taxonomic phenotypes, predict biologically important traits.
Abstract.
Author URL.
Zhou L, Slamti L, Lereclus D, Raymond B (2020). Optimal Response to Quorum-Sensing Signals Varies in Different Host Environments with Different Pathogen Group Size.
mBio,
11(3).
Abstract:
Optimal Response to Quorum-Sensing Signals Varies in Different Host Environments with Different Pathogen Group Size
. Quorum sensing describes the ability of microbes to alter gene regulation according to their local population size. Some successful theory suggests that this is a form of cooperation, namely, investment in shared products is only worthwhile if there are sufficient bacteria making the same product. This theory can explain the genetic diversity in these signaling systems in Gram-positive bacteria, such as
. Bacillus
. and
. Staphylococcus
. sp. The possible advantages gained by rare genotypes (which can exploit the products of their more common neighbors) could explain why different genotypes can coexist. We show that while these social interactions can occur in simple laboratory experiments, they do not occur in naturalistic infections using an invertebrate pathogen,
. Bacillus thuringiensis
. Instead, our results suggest that different genotypes are adapted to differently sized hosts. Overall, social models are not easily applied to this system, implying that a different explanation for this form of quorum sensing is required.
.
Abstract.
Manktelow CJ, Penkova E, Scott L, Matthews AC, Raymond B (2020). Strong Environment-Genotype Interactions Determine the Fitness Costs of Antibiotic Resistance. <i>In Vitro</i>. and in an Insect Model of Infection.
Antimicrobial Agents and Chemotherapy,
64(10).
Abstract:
Strong Environment-Genotype Interactions Determine the Fitness Costs of Antibiotic Resistance. In Vitro. and in an Insect Model of Infection
. The acquisition of antibiotic resistance commonly imposes fitness costs, a reduction in the fitness of bacteria in the absence of drugs. These costs have been quantified primarily using
. in vitro
. experiments and a small number of
. in vivo
. studies in mice, and it is commonly assumed that these diverse methods are consistent. Here, we used an insect model of infection to compare the fitness costs of antibiotic resistance
. in vivo
. to those
. in vitro
.
.
Abstract.
Raymond B, Manktelow J, Matthews A, Penkova E, Scott L (2020). Strong environment X genotype interactions determine the fitness costs of antibiotic resistance in vitro and in an insect model of infection.
Abstract:
Strong environment X genotype interactions determine the fitness costs of antibiotic resistance in vitro and in an insect model of infection
The acquisition of antibiotic resistance commonly imposes fitness costs, a reduction in the fitness of bacteria in the absence of drugs. These costs have been primarily quantified using in vitro experiments and a small number of in vivo studies in mice, and it is commonly assumed that these diverse methods are consistent. Here, we used an insect model of infection to compare the fitness costs of antibiotic resistance in vivo relative to in vitro conditions. Experiments explored diverse mechanisms of resistance in a Gram-positive pathogen, Bacillus thuringiensis, and a Gram-negative intestinal symbiont, Enterobacter cloacae. Rifampicin resistance in B. thuringiensis showed fitness costs that were typically elevated in vivo, although these were modulated by genotype-environment interactions. In contrast, resistance to cefotaxime via de-repression of AmpC β-lactamase in E. cloacae resulted in undetectable costs in vivo or in vitro, while spontaneous resistance to nalidixic acid, and carriage of the IncP plasmid RP4, imposed costs that increased in vivo. Overall, fitness costs in vitro were a poor predictor of fitness costs in vivo because of strong genotype environment interactions throughout this study. Insect infections provide a cheap and accessible means of assessing fitness consequences of resistance mutations, data that is important to understand the evolution and spread of resistance. This study emphasizes that the fitness costs imposed by particular mutations or different modes of resistance are extremely variable, and that only a subset of these mutations are likely to be prevalent outside of the laboratory.
Abstract.
2019
Raymond BD, Zhou L, Somerville J (2019). Aseptic Rearing and Infection with Gut Bacteria Improve the Fitness of Transgenic Diamondback Moth, Plutella xylostella. Insects
Dimitriu T, Marchant L, Buckling A, Raymond B (2019). Bacteria from natural populations transfer plasmids mostly towards their kin. Proceedings of the Royal Society B: Biological Sciences, 286
Amanatidou E, Matthews AC, Kuhlicke U, Neu TR, McEvoy JP, Raymond B (2019). Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli.
npj Biofilms and Microbiomes,
5(1).
Abstract:
Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli
AbstractGram-negative bacteria such as Escherichia coli commonly resist β-lactam antibiotics using plasmid-encoded β-lactamase enzymes. Bacterial strains that express β-lactamases have been found to detoxify liquid cultures and thus to protect genetically susceptible strains, constituting a clear laboratory example of social protection. These results are not necessarily general; on solid media, for instance, the rapid bactericidal action of β-lactams largely prevents social protection. Here, we tested the hypothesis that the greater tolerance of biofilm bacteria for β-lactams would facilitate social interactions. We used a recently isolated E. coli strain, capable of strong biofilm formation, to compare how cooperation and exploitation in colony biofilms and broth culture drives the dynamics of a non-conjugative plasmid encoding a clinically important β-lactamase. Susceptible cells in biofilms were tolerant of ampicillin—high doses and several days of exposure were required to kill them. In support of our hypothesis, we found robust social protection of susceptible E. coli in biofilms, despite fine-scale physical separation of resistant and susceptible cells and lower rates of production of extracellular β-lactamase. In contrast, social interactions in broth were restricted to a relatively narrow range of ampicillin doses. Our results show that β-lactam selection pressure on Gram-negative biofilms leads to cooperative resistance characterized by a low equilibrium frequency of resistance plasmids, sufficient to protect all cells.
Abstract.
Raymond B, Amanatidou E, Matthews A, McEvoy J, Neu T (2019). Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli - raw data.
Abstract:
Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli - raw data
Gram-negative bacteria such as Escherichia coli commonly resist β-lactam antibiotics using plasmid-encoded β-lactamase enzymes. Bacterial strains that express β-lactamases have been found to detoxify liquid cultures and thus to protect genetically susceptible strains, constituting a clear laboratory example of social protection. These results are not necessarily general; on solid media, for instance, the rapid bactericidal action of β-lactams largely prevents social protection. Here we tested the hypothesis that the greater tolerance of biofilm bacteria for β-lactams would facilitate social interactions. We used a recently isolated E. coli strain, capable of strong biofilm formation, to compare how cooperation and exploitation in colony biofilms and broth culture drives the dynamics of a non-conjugative plasmid encoding a clinically important β-lactamase. Susceptible cells in biofilms were tolerant of ampicillin - high doses and several days of exposure were required to kill them. In support of our hypothesis, we found robust social protection of susceptible E. coli in biofilms, despite fine-scale physical separation of resistant and susceptible cells and lower rates of production of extracellular β-lactamase. In contrast, social interactions in broth were restricted to a relatively narrow range of ampicillin doses. Our results show that β-lactam selection pressure on Gram-negative biofilms leads to cooperative resistance characterized by a low equilibrium frequency of resistance plasmids, sufficient to protect all cells.
Abstract.
Amanatidou E, Matthews AC, Kuhlicke U, Neu TR, McEvoy JP, Raymond B (2019). Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli.
NPJ Biofilms Microbiomes,
5(1).
Abstract:
Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli.
Gram-negative bacteria such as Escherichia coli commonly resist β-lactam antibiotics using plasmid-encoded β-lactamase enzymes. Bacterial strains that express β-lactamases have been found to detoxify liquid cultures and thus to protect genetically susceptible strains, constituting a clear laboratory example of social protection. These results are not necessarily general; on solid media, for instance, the rapid bactericidal action of β-lactams largely prevents social protection. Here, we tested the hypothesis that the greater tolerance of biofilm bacteria for β-lactams would facilitate social interactions. We used a recently isolated E. coli strain, capable of strong biofilm formation, to compare how cooperation and exploitation in colony biofilms and broth culture drives the dynamics of a non-conjugative plasmid encoding a clinically important β-lactamase. Susceptible cells in biofilms were tolerant of ampicillin-high doses and several days of exposure were required to kill them. In support of our hypothesis, we found robust social protection of susceptible E. coli in biofilms, despite fine-scale physical separation of resistant and susceptible cells and lower rates of production of extracellular β-lactamase. In contrast, social interactions in broth were restricted to a relatively narrow range of ampicillin doses. Our results show that β-lactam selection pressure on Gram-negative biofilms leads to cooperative resistance characterized by a low equilibrium frequency of resistance plasmids, sufficient to protect all cells.
Abstract.
Author URL.
Patel M, Raymond B, Bonsall MB, West SA (2019). Crystal toxins and the volunteer's dilemma in bacteria.
J Evol Biol,
32(4), 310-319.
Abstract:
Crystal toxins and the volunteer's dilemma in bacteria.
The growth and virulence of the bacteria Bacillus thuringiensis depend on the production of Cry toxins, which are used to perforate the gut of its host. Successful invasion of the host relies on producing a threshold amount of toxin, after which there is no benefit from producing more toxin. Consequently, the production of Cry toxin appears to be a different type of social problem compared with the public goods scenarios that bacteria usually encounter. We show that selection for toxin production is a volunteer's dilemma. We make specific predictions that (a) selection for toxin production depends upon an interplay between the number of bacterial cells that each host ingests and the genetic relatedness between those cells; (b) cheats that do not produce toxin gain an advantage when at low frequencies, and at high bacterial density, allowing them to be maintained in a population alongside toxin-producing cells. More generally, our results emphasize the diversity of the social games that bacteria play.
Abstract.
Author URL.
Raymond B (2019). Five rules for resistance management in the antibiotic apocalypse, a road map for integrated microbial management.
Evolutionary Applications,
12(6), 1079-1091.
Abstract:
Five rules for resistance management in the antibiotic apocalypse, a road map for integrated microbial management
Resistance to new antimicrobials can become widespread within 2–3 years. Resistance problems are particularly acute for bacteria that can experience selection as both harmless commensals and pathogenic hospital-acquired infections. New drugs, although welcome, cannot tackle the antimicrobial resistance crisis alone: new drugs must be partnered with more sustainable patterns of use. However, the broader experience of resistance management in other disciplines, and the assumptions on which resistance rests, is not widely appreciated in clinical and microbiological disciplines. Improved awareness of the field of resistance management could improve clinical outcomes and help shape novel solutions. Here, the aim is to develop a pragmatic approach to developing a sustainable integrated means of using antimicrobials, based on an interdisciplinary synthesis of best practice, recent theory and recent clinical data. This synthesis emphasizes the importance of pre-emptive action and the value of reducing the supply of genetic novelty to bacteria under selection. The weight of resistance management experience also cautions against strategies that over-rely on the fitness costs of resistance or low doses. The potential (and pitfalls) of shorter courses, antibiotic combinations and antibiotic mixing or cycling are discussed in depth. Importantly, some of variability in the success of clinical trials of mixing approaches can be explained by the number and diversity of drugs in a trial, as well as whether trials encompass single wards or the wider transmission network that is a hospital. Consideration of the importance of data, and of the initially low frequency of resistance, leads to a number of additional recommendations. Overall, reduction in selection pressure, interference with the transmission of problematic genotypes and multidrug approaches (combinations, mixing or cycling) are all likely to be required for sustainability and the protection of forthcoming drugs.
Abstract.
Ayra-Pardo C, Ochagavía ME, Raymond B, Gulzar A, Rodríguez-Cabrera L, Rodríguez de la Noval C, Morán Bertot I, Terauchi R, Yoshida K, Matsumura H, et al (2019). HT-SuperSAGE of the gut tissue of a Vip3Aa-resistant Heliothis virescens (Lepidoptera: Noctuidae) strain provides insights into the basis of resistance.
Insect Sci,
26(3), 479-498.
Abstract:
HT-SuperSAGE of the gut tissue of a Vip3Aa-resistant Heliothis virescens (Lepidoptera: Noctuidae) strain provides insights into the basis of resistance.
Multitoxin Bt-crops expressing insecticidal toxins with different modes of action, for example, Cry and Vip, are expected to improve resistance management in target pests. While Cry1A resistance has been relatively well characterized in some insect species, this is not the case for Vip3A, for which no mechanism of resistance has yet been identified. Here we applied HT-SuperSAGE to analyze the transcriptome of the gut tissue of tobacco budworm Heliothis virescens (F.) laboratory-selected for Vip3Aa resistance. From a total of 1 324 252 sequence reads, 5 895 126-bp tags were obtained representing 17 751 nonsingleton unique transcripts (UniTags) from genetically similar Vip3Aa-resistant (Vip-Sel) and susceptible control (Vip-Unsel) strains. Differential expression was significant (≥2.5 fold or ≤0.4; P < 0.05) for 1989 sequences (11.2% of total UniTags), where 420 represented overexpressed (OE) and 1569 underexpressed (UE) genes in Vip-Sel. BLASTN searches mapped 419 UniTags to H. virescens sequence contigs, of which, 416 (106 OE and 310 UE) were unambiguously annotated to proteins in NCBI nonredundant protein databases. Gene Ontology distributed 345 of annotated UniTags in 14 functional categories with metabolism (including serine-type hydrolases) and translation/ribosome biogenesis being the most prevalent. A UniTag homologous to a particular member of the REsponse to PAThogen (REPAT) family was found among most overexpressed, while UniTags related to the putative Vip3Aa-binding ribosomal protein S2 (RpS2) were underexpressed. qRT-PCR of a subset of UniTags validated the HT-SuperSAGE data. This study is the first providing lepidopteran gut transcriptome associated with Vip3Aa resistance and a foundation for future attempts to elucidate the resistance mechanism.
Abstract.
Author URL.
Dimitriu T, Medaney F, Amanatidou E, Forsyth J, Ellis RJ, Raymond B (2019). Negative frequency dependent selection on plasmid carriage and low fitness costs maintain extended spectrum β-lactamases in Escherichia coli.
Scientific Reports,
9(1).
Abstract:
Negative frequency dependent selection on plasmid carriage and low fitness costs maintain extended spectrum β-lactamases in Escherichia coli
AbstractPlasmids may maintain antibiotic resistance genes in bacterial populations through conjugation, in the absence of direct selection pressure. However, the costs and benefits of conjugation for plasmid and bacterial fitness are not well understood. Using invasion and competition experiments with plasmid mutants we explicitly tested how conjugation contributes to the maintenance of a plasmid bearing a single extended-spectrum ß-lactamase (ESBL) gene (blaCTX-M-14). Surprisingly, conjugation had little impact on overall frequencies, although it imposed a substantial fitness cost. Instead, stability resulted from the plasmid conferring fitness benefits when rare. Frequency dependent fitness did not require a functional blaCTX-M-14 gene, and was independent of culture media. Fitness benefits when rare are associated with the core plasmid backbone but are able to drive up frequencies of antibiotic resistance because fitness burden of the blaCTX-M-14 gene is very low. Negative frequency dependent fitness can contribute to maintaining a stable frequency of resistance genes in the absence of selection pressure from antimicrobials. In addition, persistent, low cost resistance has broad implications for antimicrobial stewardship.
Abstract.
Raymond B, Dimitriu T (2019). Negative frequency dependent selection on plasmid carriage and low fitness costs maintain extended spectrum β-lactamases in Escherichia coli.
Abstract:
Negative frequency dependent selection on plasmid carriage and low fitness costs maintain extended spectrum β-lactamases in Escherichia coli.
Plasmids may maintain antibiotic resistance genes in bacterial populations through conjugation, in the absence of direct selection pressure. However, the costs and benefits of conjugation for plasmid and bacterial fitness are not well understood. Using invasion and competition experiments with plasmid mutants we explicitly tested how conjugation contributes to the maintenance of a plasmid bearing a single extended-spectrum ß-lactamase (ESBL) gene (blaCTX-M-14). Surprisingly, conjugation had little impact on overall frequencies, although it imposed a substantial fitness cost. Instead, stability resulted from the plasmid conferring fitness benefits when rare. Frequency dependent fitness did not require a functional blaCTX-M-14 gene, and was independent of culture media. Fitness benefits when rare are associated with the core plasmid backbone but are able to drive up frequencies of antibiotic resistance because fitness burden of the blaCTX-M-14 gene is very low. Negative frequency dependent fitness can contribute to maintaining a stable frequency of resistance genes in the absence of selection pressure from antimicrobials. In addition, persistent, low cost resistance has broad implications for antimicrobial stewardship.
Abstract.
Raymond B (2019). Optimal response to quorum-sensing signals varies in different host environments with different pathogen group size.
Abstract:
Optimal response to quorum-sensing signals varies in different host environments with different pathogen group size.
The persistence of genetic variation in master regulators of gene expression, such as quorum-sensing systems, is hard to explain. Here, we investigated two alternative hypotheses for the prevalence of polymorphic quorum-sensing in Gram-positive bacteria, i.e. the use of different signal. / receptor pairs (‘pherotypes’) to regulate the same functions. First, social interactions between pherotypes or ‘facultative cheating’ may favour rare variants that exploit the signals of others. Second, different pherotypes may increase fitness in different environments. We evaluated these hypotheses in the invertebrate pathogen Bacillus thuringiensis, using three pherotypes expressed in a common genetic background. Facultative cheating occurred in homogenized hosts, in contrast, rare pherotypes had reduced fitness in naturalistic infections. There was clear support for environment-dependent fitness: pherotypes varied in responsiveness to signals and in mean competitive fitness. Notably, competitive fitness varied with group size: the pherotype with highest responsiveness to signals performed best in smaller hosts where infections have a lower pathogen group size. Less responsive pherotypes performed best in larger hosts. In this system, low signal abundance can limit fitness in hosts while the optimal level of response to signals varies in different host environments.
Abstract.
Matthews A, Pierce S, Hipperson H, Raymond B (2019). Rhizobacterial Community Assembly Patterns Vary Between Crop Species.
FRONTIERS IN MICROBIOLOGY,
10 Author URL.
Matthews AC, Mikonranta L, Raymond B (2019). Shifts along the parasite-mutualist continuum are opposed by fundamental trade-offs.
Proceedings of the Royal Society B: Biological Sciences,
286(1900).
Abstract:
Shifts along the parasite-mutualist continuum are opposed by fundamental trade-offs
Theory suggests that symbionts can readily evolve more parasitic or mutualistic strategies with respect to hosts. However, many symbionts have stable interactions with hosts that improve nutrient assimilation or confer protection from pathogens. We explored the potential for evolution of increased parasitism or decreased parasitism and mutualism in a natural gut symbiosis between larvae of Plutella xylostella and the microbe Enterobacter cloacae. We focused on interactions with the pathogen, Bacillus thuringiensis: Selecting for parasitism in terms of facilitating pathogen infection, or increased mutualism in terms of host protection. Selection for parasitism led to symbionts increasing pathogen-induced mortality but reduced their competitive ability with pathogens and their in vitro growth rates. Symbionts did not evolve to confer protection from pathogens. However, several lineages evolved reduced parasitism, primarily in terms of moderating impacts on host growth, potentially because prudence pays dividends through increased host size. Overall, the evolution of increased parasitism was achievable but was opposed by trade-offs likely to reduce fitness. The evolution of protection may not have occurred because suppressing growth of B. thuringiensis in the gut might provide only weak protection or because evolution towards protective interactions was opposed by the loss of competitive fitness in symbionts.
Abstract.
Mikonranta L, Buckling A, Jalasvuori M, Raymond B (2019). Targeting antibiotic resistant bacteria with phage reduces bacterial density in an insect host.
Biol Lett,
15(3).
Abstract:
Targeting antibiotic resistant bacteria with phage reduces bacterial density in an insect host.
Phage therapy is attracting growing interest among clinicians as antibiotic resistance continues becoming harder to control. However, clinical trials and animal model studies on bacteriophage treatment are still scarce and results on the efficacy vary. Recent research suggests that using traditional antimicrobials in concert with phage could have desirable synergistic effects that hinder the evolution of resistance. Here, we present a novel insect gut model to study phage-antibiotic interaction in a system where antibiotic resistance initially exists in very low frequency and phage specifically targets the resistance bearing cells. We demonstrate that while phage therapy could not reduce the frequency of target bacteria in the population during positive selection by antibiotics, it alleviated the antibiotic induced blooming by lowering the overall load of resistant cells. The highly structured gut environment had pharmacokinetic effects on both phage and antibiotic dynamics compared with in vitro: antibiotics did not reduce the overall amount of bacteria, demonstrating a simple turnover of gut microbiota from non-resistant to resistant population with little cost. The results imply moderate potential for using phage as an aid to target antibiotic resistant gut infections, and question the usefulness of in vitro inferences.
Abstract.
Author URL.
Zhou L, Alphey N, Walker AS, Travers LM, Morrison NI, Bonsall MB, Raymond B (2019). The application of self-limiting transgenic insects in managing resistance in experimental metapopulations.
Journal of Applied Ecology,
56(3), 688-698.
Abstract:
The application of self-limiting transgenic insects in managing resistance in experimental metapopulations
The mass release of transgenic insects carrying female lethal self-limiting genes can reduce pest insect populations. Substantial releases are also a novel resistance management tool, since wild type alleles conferring susceptibility to pesticides can dilute resistance alleles in target populations. However, a potential barrier is the need for large-scale area-wide releases. Here, we address whether localized releases of transgenic insects could provide an alternative means of population suppression and resistance management, without serious loss of efficacy. We used experimental mesocosms constituting insect metapopulations to explore the evolution of resistance to the Bacillus thuringiensis toxin Cry1Ac in a high-dose/refugia landscape in the insect Plutella xylostella. We ran two selection experiments, the first compared the efficacy of “everywhere” releases and negative controls to a spatially density-dependent or “whack-a-mole” strategy that concentrated release of transgenic insects in subpopulations with elevated resistance. The second experiment tested the relative efficacy of whack-a-mole and everywhere releases under spatially homogenous and heterogeneous selection pressure. The whack-a-mole releases were less effective than everywhere releases in terms of slowing the evolution of resistance, which, in the first experiment, largely prevented the evolution of resistance. In contrast to predictions, heterogeneous whack-a-mole releases were no more effective under heterogeneous selection pressure. Heterogeneous selection pressure did, however, reduce total insect population sizes. Whack-a-mole releases provided early population suppression, indistinguishable from homogeneous everywhere releases. However, insect population densities tracked the evolution of resistance in this system, as phenotypic resistance provides access to additional diet containing the toxin Cry1Ac. Thus, as resistance levels diverged between treatments, carrying capacities and population sizes increased under the whack-a-mole approach. Synthesis and applications. Spatially density-dependent releases of transgenic insects, particularly those targeting source populations at a landscape level, could suppress pest populations in the absence of blanket area-wide releases. The benefits of self-limiting transgenic insects were reduced in spatially localized releases, suggesting that they are not ideal for “spot” treatment of resistance problems. Nevertheless, spatially homogeneous or heterogeneous releases could be used to support other resistance management interventions.
Abstract.
Manktelow J (2019). Virulence and Evolutionary Ecology in the Entomopathogen Bacillus thuringiensis.
Abstract:
Virulence and Evolutionary Ecology in the Entomopathogen Bacillus thuringiensis
Bacillus thuringiensis is an entomopathogen in the Bacillus cereus species group, and has been used as a biopesticide for over 50 years. Despite extensive use of B. thuringiensis, there remain questions over its specific ecology compared to other members of the B. cereus group which poses problems for its continued applied use. Tying entomopathogenic ecology to a specific clade within the B. cereus group will limit confusion between B. thuringiensis used in agriculture and more harmful strains. Better understanding of B. thuringiensis ecology can also be used to combat resistance in pest species through selective passaging.
The ecology of B. thuringiensis was explored through competitions in Plutella xylostella (diamondback moth) larvae, which showed clade 2 B. thuringiensis have improved fitness in insects compared to clade 1 strains. Additionally, growth rates were compared in vitro, giving different thermal profiles for the two clades. Growth media preference was assessed for B. cereus group species with all favouring protein media over soil-based ones.
Selective passaging explored the effects of relatedness and host background on virulence evolution. For relatedness, B. thuringiensis subsp. aizawai was passaged for five rounds in P. xylostella larvae with none, one or two bottlenecking events. These treatments failed to produce any increase in virulence. In the second, B. thuringiensis subsp. entomocidus was passaged either in Cry1Ac-resistant, Cry1Ac-susceptible, alternating rounds of each or coevolved P. xylostella, with all containing a mutagenesis step with ethyl methanesulfonate. Virulence increased in the resistant and coevolved treatments, confirming that resistance is best overcome by passaging in harder-to-kill hosts.
The ecological and genetic distinctiveness of clade 2 B. thuringiensis suggests the species should be reclassified to solely this clade, which will limit safety concerns. Selective passaging can improve the virulence of strains, even if the underlying interactions are unknown; it can also provide insight into virulence evolution which would be lost when improving only at the protein level.
Abstract.
Raymond B, Powell N (2019). We must follow these five rules to avert an antimicrobial resistance crisis. Pharmaceutical Journal, 303(7931).
2018
Raymond B, Federici BA (2018). An appeal for a more evidence based approach to biopesticide safety in the EU.
FEMS Microbiol Ecol,
94(1).
Abstract:
An appeal for a more evidence based approach to biopesticide safety in the EU.
EFSA responded to our perspective article on the safe use of the insect pathogen Bacillus thrurigiensis (Bt). In doing so they admitted that there is no direct evidence to suggest that B. thuringiensis can cause diarrhoea. They nevertheless continue to repeat the assertion that Bt cannot be distinguished from Bacillus cereus, even though nearly all Bt strains, and certainly all biopesticide strains, can be distinguished from B. cereus using multi-locus sequencing typing. EFSA also continue to repeat the unsupported and speculative hypothesis that Bt strains could be capable of causing cryptic infections in humans. This hypothesis is very much against the weight of all available safety and epidemiological data. Moreover, genotyping schemes of B. cereus group clinical infections also show that biopesticide strains have never been associated with human infections. Our position that Bt biopesticides and Bt isolates from the clade dominated by invertebrate pathogens are incapable of causing infections in humans is well supported by the international community of scientists familiar with the data on the safety of Bt after more than four decades of extensive use in agriculture and forestry.
Abstract.
Author URL.
Zhou L, Alphey N, Walker AS, Travers LM, Hasan F, Morrison NI, Bonsall MB, Raymond B (2018). Combining the high-dose/refuge strategy and self-limiting transgenic insects in resistance management-A test in experimental mesocosms.
Evol Appl,
11(5), 727-738.
Abstract:
Combining the high-dose/refuge strategy and self-limiting transgenic insects in resistance management-A test in experimental mesocosms.
The high-dose/refuge strategy has been the primary approach for resistance management in transgenic crops engineered with Bacillus thuringiensis toxins. However, there are continuing pressures from growers to reduce the size of Bt toxin-free refugia, which typically suffer higher damage from pests. One complementary approach is to release male transgenic insects with a female-specific self-limiting gene. This technology can reduce population sizes and slow the evolution of resistance by introgressing susceptible genes through males. Theory predicts that it could be used to facilitate smaller refugia or reverse the evolution of resistance. In this study, we used experimental evolution with caged insect populations to investigate the compatibility of the self-limiting system and the high-dose/refuge strategy in mitigating the evolution of resistance in diamondback moth, Plutella xylostella. The benefits of the self-limiting system were clearer at smaller refuge size, particularly when refugia were inadequate to prevent the evolution of resistance. We found that transgenic males in caged mesocosms could suppress population size and delay resistance development with 10% refugia and 4%-15% initial resistance allele frequency. Fitness costs in hemizygous transgenic insects are particularly important for introgressing susceptible alleles into target populations. Fitness costs of the self-limiting gene in this study (P. xylostella OX4139 line L) were incompletely dominant, and reduced fecundity and male mating competitiveness. The experimental evolution approach used here illustrates some of the benefits and pitfalls of combining mass release of self-limiting insects and the high-dose/refuge strategy, but does indicate that they can be complementary.
Abstract.
Author URL.
Patel M, Raymond B, Bonsall MB, West SA (2018). Crystal Toxins and the volunteer’s dilemma in bacteria.
Méric G, Mageiros L, Pascoe B, Woodcock DJ, Mourkas E, Lamble S, Bowden R, Jolley KA, Raymond B, Sheppard SK, et al (2018). Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group.
Molecular Ecology,
27(7), 1524-1540.
Abstract:
Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group
Bacterial plasmids can vary from small selfish genetic elements to large autonomous replicons that constitute a significant proportion of total cellular DNA. By conferring novel function to the cell, plasmids may facilitate evolution but their mobility may be opposed by co-evolutionary relationships with chromosomes or encouraged via the infectious sharing of genes encoding public goods. Here, we explore these hypotheses through large-scale examination of the association between plasmids and chromosomal DNA in the phenotypically diverse Bacillus cereus group. This complex group is rich in plasmids, many of which encode essential virulence factors (Cry toxins) that are known public goods. We characterized population genomic structure, gene content and plasmid distribution to investigate the role of mobile elements in diversification. We analysed coding sequence within the core and accessory genome of 190 B. cereus group isolates, including 23 novel sequences and genes from 410 reference plasmid genomes. While cry genes were widely distributed, those with invertebrate toxicity were predominantly associated with one sequence cluster (clade 2) and phenotypically defined Bacillus thuringiensis. Cry toxin plasmids in clade 2 showed evidence of recent horizontal transfer and variable gene content, a pattern of plasmid segregation consistent with transfer during infectious cooperation. Nevertheless, comparison between clades suggests that co-evolutionary interactions may drive association between plasmids and chromosomes and limit wider transfer of key virulence traits. Proliferation of successful plasmid and chromosome combinations is a feature of specialized pathogens with characteristic niches (Bacillus anthracis, B. thuringiensis) and has occurred multiple times in the B. cereus group.
Abstract.
Geng LL, Shao GX, Raymond B, Wang ML, Sun XX, Shu CL, Zhang J (2018). Subterranean infestation by Holotrichia parallela larvae is associated with changes in the peanut (Arachis hypogaea L.) rhizosphere microbiome.
Microbiological Research,
211, 13-20.
Abstract:
Subterranean infestation by Holotrichia parallela larvae is associated with changes in the peanut (Arachis hypogaea L.) rhizosphere microbiome
Rhizosphere microorganisms contribute to the health and development of crops and these beneficial microbes are recruited to the root-zone when plants experience biotic/abiotic stress. The subterranean pests Holotrichia parallela cause severe crop loss in peanut (Arachis hypogaea L.) fields. Hypothesizing that infestation by H. parallela larva may influence the composition of rhizosphere microbial communities, deep sequencing of V3 and V4 hypervariable regions of 16S rRNA gene was used to characterize the rhizosphere bacteria of infested and uninfested peanuts. A total of 2,673,656 reads were generated and an average of 2558 OTUs were obtained for each sample. Comparisons of rhizosphere bacterial community structure of peanuts with those infested by H. parallela larva revealed that the relative abundance of Proteobacteria and Bacteroidetes increased, while that of Actinobacteria decreased in the rhizosphere with infestation. A significant shift in bacterial communities was observed within 24 h after infestation by principal coordinate analysis. For the 332 genera identified in 24 h treatment, infestation of white grubs led to the significant changes of abundance of 67 genera. An increase in the Pseudomonas genus of infested-samples for 24 h was verified by real-time qPCR. Our results indicate H. parallela larvae infestation can quickly leads to the change of peanut rhizosphere microbiome and enrichment of specific bacterial species. But the effects were not persistent. This study provides the insight into the function of rhizosphere microbiome in the interaction between subterranean pests and crops.
Abstract.
2017
Zheng J, Gao Q, Liu L, Liu H, Wang Y, Peng D, Ruan L, Raymond B, Sun M (2017). Comparative Genomics of Bacillus thuringiensis Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts.
mBio,
8(4).
Abstract:
Comparative Genomics of Bacillus thuringiensis Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts.
Understanding the genetic basis of host shifts is a key genomic question for pathogen and parasite biology. The Bacillus cereus group, which encompasses Bacillus thuringiensis and Bacillus anthracis, contains pathogens that can infect insects, nematodes, and vertebrates. Since the target range of the essential virulence factors (Cry toxins) and many isolates is well known, this group presents a powerful system for investigating how pathogens can diversify and adapt to phylogenetically distant hosts. Specialization to exploit insects occurs at the level of the major clade and is associated with substantial changes in the core genome, and host switching between insect orders has occurred repeatedly within subclades. The transfer of plasmids with linked cry genes may account for much of the adaptation to particular insect orders, and network analysis implies that host specialization has produced strong associations between key toxin genes with similar targets. Analysis of the distribution of plasmid minireplicons shows that plasmids with orf156 and orf157, which carry genes encoding toxins against Lepidoptera or Diptera, were contained only by B. thuringiensis in the specialized insect clade (clade 2), indicating that tight genome/plasmid associations have been important in adaptation to invertebrate hosts. Moreover, the accumulation of multiple virulence factors on transposable elements suggests that cotransfer of diverse virulence factors is advantageous in terms of expanding the insecticidal spectrum, overcoming insect resistance, or through gains in pathogenicity via synergistic interactions between toxins.IMPORTANCE Population genomics have provided many new insights into the formation, evolution, and dynamics of bacterial pathogens of humans and other higher animals, but these pathogens usually have very narrow host ranges. As a pathogen of insects and nematodes, Bacillus thuringiensis, which produces toxins showing toxicity to many orders of insects and other invertebrates, can be used as a model to study the evolution of pathogens with wide host ranges. Phylogenomic analysis revealed that host specialization and switching occur at the level of the major clade and subclade, respectively. A toxin gene co-occurrence network indicates that multiple toxins with similar targets were accumulated by the same cell in the whole species. This accumulation may be one of the strategies that B. thuringiensis has used to fight against host resistance. This kind of formation and evolution of pathogens represents a different path used against multiple invertebrate hosts from that used against higher animals.
Abstract.
Author URL.
Raymond B, Federici BA (2017). In defence of Bacillus thuringiensis, the safest and most successful microbial insecticide available to humanity—a response to EFSA. FEMS Microbiology Ecology, 93(7).
2016
Medaney F, Ellis RJ, Raymond B (2016). Ecological and genetic determinants of plasmid distribution in Escherichia coli.
Environ Microbiol,
18(11), 4230-4239.
Abstract:
Ecological and genetic determinants of plasmid distribution in Escherichia coli.
Bacterial plasmids are important carriers of virulence and antibiotic resistance genes. Nevertheless, little is known of the determinants of plasmid distribution in bacterial populations. Here the factors affecting the diversity and distribution of the large plasmids of Escherichia coli were explored in cattle grazing on semi-natural grassland, a set of populations with low frequencies of antibiotic resistance genes. Critically, the population genetic structure of bacterial hosts was chararacterized. This revealed structured E. coli populations with high diversity between sites and individuals but low diversity within cattle hosts. Plasmid profiles, however, varied considerably within the same E. coli genotype. Both ecological and genetic factors affected plasmid distribution: plasmid profiles were affected by site, E. coli diversity, E. coli genotype and the presence of other large plasmids. Notably 3/26 E. coli serotypes accounted for half the observed plasmid-free isolates indicating that within species variation can substantially affect carriage of the major conjugative plasmids. The observed population structure suggest that most of the opportunities for within species plasmid transfer occur between different individuals of the same genotype and support recent experimental work indicating that plasmid-host coevolution, and epistatic interactions on fitness costs are likely to be important in determining occupancy.
Abstract.
Author URL.
Shapiro-Ilan D, Raymond B (2016). Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes.
Evolutionary Applications,
9(3), 462-470.
Abstract:
Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes
Cooperative secretion of virulence factors by pathogens can lead to social conflict when cheating mutants exploit collective secretion, but do not contribute to it. If cheats outcompete cooperators within hosts, this can cause loss of virulence. Insect parasitic nematodes are important biocontrol tools that secrete a range of significant virulence factors. Critically, effective nematodes are hard to maintain without live passage, which can lead to virulence attenuation. Using experimental evolution, we tested whether social cheating might explain unstable virulence in the nematode Heterorhabditis floridensis by manipulating relatedness via multiplicity of infection (MOI), and the scale of competition. Passage at high MOI, which should reduce relatedness, led to loss of fitness: virulence and reproductive rate declined together and all eight independent lines suffered premature extinction. As theory predicts, relatedness treatments had more impact under stronger global competition. In contrast, low MOI passage led to more stable virulence and increased reproduction. Moreover, low MOI lineages showed a trade-off between virulence and reproduction, particularly for lines under stronger between-host competition. Overall, this study indicates that evolution of virulence theory is valuable for the culture of biocontrol agents: effective nematodes can be improved and maintained if passage methods mitigate possible social conflicts.
Abstract.
Medaney F, Dimitriu T, Ellis RJ, Raymond B (2016). Live to cheat another day: Bacterial dormancy facilitates the social exploitation of β-lactamases.
ISME Journal,
10(3), 778-787.
Abstract:
Live to cheat another day: Bacterial dormancy facilitates the social exploitation of β-lactamases
The breakdown of antibiotics by β-lactamases may be cooperative, since resistant cells can detoxify their environment and facilitate the growth of susceptible neighbours. However, previous studies of this phenomenon have used artificial bacterial vectors or engineered bacteria to increase the secretion of β-lactamases from cells. Here, we investigated whether a broad-spectrum β-lactamase gene carried by a naturally occurring plasmid (pCT) is cooperative under a range of conditions. In ordinary batch culture on solid media, there was little or no evidence that resistant bacteria could protect susceptible cells from ampicillin, although resistant colonies could locally detoxify this growth medium. However, when susceptible cells were inoculated at high densities, late-appearing phenotypically susceptible bacteria grew in the vicinity of resistant colonies. We infer that persisters, cells that have survived antibiotics by undergoing a period of dormancy, founded these satellite colonies. The number of persister colonies was positively correlated with the density of resistant colonies and increased as antibiotic concentrations decreased. We argue that detoxification can be cooperative under a limited range of conditions: if the toxins are bacteriostatic rather than bacteridical; or if susceptible cells invade communities after resistant bacteria; or if dormancy allows susceptible cells to avoid bactericides. Resistance and tolerance were previously thought to be independent solutions for surviving antibiotics. Here, we show that these are interacting strategies: the presence of bacteria adopting one solution can have substantial effects on the fitness of their neighbours.
Abstract.
Raymond BD (2016). The biology, ecology and taxonomy of Bacillus thuringiensis and related bacteria. In Fiuza L, Polancyk RA, Crickmore N (Eds.)
Bacillus thuringiensis and Lysinibacillus sphaericus: Characterization and use in the field of biocontrol, Springer.
Abstract:
The biology, ecology and taxonomy of Bacillus thuringiensis and related bacteria
Abstract.
2015
Cornforth DM, Matthews A, Brown SP, Raymond B (2015). Bacterial Cooperation Causes Systematic Errors in Pathogen Risk Assessment due to the Failure of the Independent Action Hypothesis.
PLoS Pathogens,
11(4).
Abstract:
Bacterial Cooperation Causes Systematic Errors in Pathogen Risk Assessment due to the Failure of the Independent Action Hypothesis
The Independent Action Hypothesis (IAH) states that pathogenic individuals (cells, spores, virus particles etc.) behave independently of each other, so that each has an independent probability of causing systemic infection or death. The IAH is not just of basic scientific interest; it forms the basis of our current estimates of infectious disease risk in humans. Despite the important role of the IAH in managing disease interventions for food and water-borne pathogens, experimental support for the IAH in bacterial pathogens is indirect at best. Moreover since the IAH was first proposed, cooperative behaviors have been discovered in a wide range of microorganisms, including many pathogens. A fundamental principle of cooperation is that the fitness of individuals is affected by the presence and behaviors of others, which is contrary to the assumption of independent action. In this paper, we test the IAH in Bacillus thuringiensis (B.t), a widely occurring insect pathogen that releases toxins that benefit others in the inoculum, infecting the diamondback moth, Plutella xylostella. By experimentally separating B.t. spores from their toxins, we demonstrate that the IAH fails because there is an interaction between toxin and spore effects on mortality, where the toxin effect is synergistic and cannot be accommodated by independence assumptions. Finally, we show that applying recommended IAH dose-response models to high dose data leads to systematic overestimation of mortality risks at low doses, due to the presence of synergistic pathogen interactions. Our results show that cooperative secretions can easily invalidate the IAH, and that such mechanistic details should be incorporated into pathogen risk analysis.
Abstract.
Deng C, Slamti L, Raymond B, Liu G, Lemy C, Gominet M, Yang J, Wang H, Peng Q, Zhang J, et al (2015). Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain.
ISME Journal,
9(2), 286-296.
Abstract:
Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain
A major challenge in bacterial developmental biology has been to understand the mechanisms underlying cell fate decisions. Some differentiated cell types display cooperative behaviour. Cooperation is one of the greatest mysteries of evolutionary biology and microbes have been considered as an excellent system for experimentally testing evolution theories. Bacillus thuringiensis (Bt) is a spore-forming bacterium, which is genetically closely related to B. anthracis, the agent of anthrax, and to B. cereus, an opportunistic human pathogen. The defining feature that distinguishes Bt from its relatives is its ability to produce crystal inclusions in the sporulating cells. These toxins are solubilized after ingestion and are cooperative public goods in insect hosts. In this study, we describe a Bt strain LM1212 that presents the unique ability to terminally differentiate into crystal producers and spore formers. Transcriptional analysis based on lacZ and gfp reporter genes suggested that this phenotype is the consequence of a new type of cell differentiation associated with a novel regulation mode of cry gene expression. The differentiating crystal-producer phenotype has higher spore productivity than a typical Bt strain and is better able to compete with Cry toxin null 'cheaters'. Potentially, this division of labour provides additional fitness benefits in terms of spore viability or durability of Cry toxin.
Abstract.
van Leeuwen E, O'Neill S, Matthews A, Raymond B (2015). Erratum: Making pathogens sociable: the emergence of high relatedness through limited host invasibility. The ISME Journal: Multidisciplinary Journal of Microbial Ecology, 9(10), 2328-2328.
Van Leeuwen E, O'Neill S, Matthews A, Raymond B (2015). Making pathogens sociable: the emergence of high relatedness through limited host invasibility.
ISME Journal,
9(10), 2315-2323.
Abstract:
Making pathogens sociable: the emergence of high relatedness through limited host invasibility
Cooperation depends upon high relatedness, the high genetic similarity of interacting partners relative to the wider population. For pathogenic bacteria, which show diverse cooperative traits, the population processes that determine relatedness are poorly understood. Here, we explore whether within-host dynamics can produce high relatedness in the insect pathogen Bacillus thuringiensis. We study the effects of host/pathogen interactions on relatedness via a model of host invasion and fit parameters to competition experiments with marked strains. We show that invasibility is a key parameter for determining relatedness and experimentally demonstrate the emergence of high relatedness from well-mixed inocula. We find that a single infection cycle results in a bottleneck with a similar level of relatedness to those previously reported in the field. The bottlenecks that are a product of widespread barriers to infection can therefore produce the population structure required for the evolution of cooperative virulence.
Abstract.
Ayra-Pardo C, Raymond B, Gulzar A, Rodríguez-Cabrera L, Morán-Bertot I, Crickmore N, Wright DJ (2015). Novel genetic factors involved in resistance to Bacillus thuringiensis in Plutella xylostella.
Insect Molecular Biology,
24(6), 589-600.
Abstract:
Novel genetic factors involved in resistance to Bacillus thuringiensis in Plutella xylostella
The widespread and sustainable exploitation of the entomopathogen Bacillus thuringiensis (Bt) in pest control is threatened by the evolution of resistance. Although resistance is often associated with loss of binding of the Bt toxins to the insect midgut cells, other factors have been implicated. Here we used suppressive subtractive hybridization and gene expression suppression to identify additional molecular components involved in Bt-resistance in Plutella xylostella. We isolated transcripts from genes that were differentially expressed in the midgut of larvae from a resistant population, following ingestion of a Bt kurstaki HD1 strain-based commercial formulation (DiPel), and compared with a genetically similar susceptible population. Quantitative real-time polymerase-chain reaction (RT-PCR) analysis confirmed the differential basal expression of a subset of these genes. Gene expression suppression of three of these genes (P. xylostella cyclin-dependent kinase 5 regulatory subunit associated protein 1-like 1, stromal cell-derived factor 2-like 1 and hatching enzyme-like 1) significantly increased the pathogenicity of HD1 to the resistant population. In an attempt to link the multitude of factors reportedly influencing resistance to Bt with the well-characterized loss of toxin binding, we also considered Bt-resistance models in P. xylostella and other insects.
Abstract.
2014
Tellez-Rodriguez P, Raymond B, Moran-Bertot I, Rodriguez-Cabrera L, Wright DJ, Borroto CG, Ayra-Pardo C (2014). Strong oviposition preference for Bt over non-Bt maize in Spodoptera frugiperda and its implications for the evolution of resistance.
BMC BIOLOGY,
12 Author URL.
Zhou L, Slamti L, Nielsen-LeRoux C, Lereclus D, Raymond B (2014). The social biology of quorum sensing in a naturalistic host pathogen system.
Current Biology,
24(20), 2417-2422.
Abstract:
The social biology of quorum sensing in a naturalistic host pathogen system
Many microorganisms cooperate by secreting products that are commonly available to neighboring cells. These "public goods" include autoinduced, quorum-sensing (QS) molecules and the virulence factors activated by these signals [1-4]. Public goods cooperation is exploitable by cheaters, cells that avoid the costs of production but gain an advantage by freeloading on the products of others [5-8]. QS signals and responses can be cooperative under artificial laboratory conditions [1-4, 9], but it remains unclear whether QS is cooperative in nature: little is known about the frequency of cheaters in natural populations [10, 11], and cheaters may do poorly because of the importance of QS in major transcriptional networks [12-14]. Here, we investigate the cooperative nature of QS in a natural system: the Gram-positive insect pathogen Bacillus thuringiensis and the larvae of the diamondback moth, Plutella xylostella. Although we find evidence of cooperation, QS null mutants are not effective cheats in vivo and cannot outcompete wild-type strains. We show that spatial structure limits mutant fitness and that well-separated microcolonies occur in vivo because of the strong population bottlenecks occurring during natural infection. We argue that spatial structure and low densities are the norm in early-stage infections, and this can explain why QS cheaters are rare in B. thuringiensis and its relatives [10]. These results contrast with earlier experiments describing the high fitness of Gram-negative QS cheaters and suggest that QS suppression ("quorum quenching") can be clinically effective without having negative impacts on the evolution of virulence.
Abstract.
2013
Raymond B, Bonsall MB (2013). Cooperation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system.
BioEssays,
35(8), 706-716.
Abstract:
Cooperation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system
How significant is social evolution theory for the maintenance of virulence in natural populations? We assume that secreted, distantly acting virulence factors are highly likely to be cooperative public goods. Using this assumption, we discuss and critically assess the potential importance of social interactions for understanding the evolution, diversity and distribution of virulence in the Bacillus cereus group, a novel study system for microbial social biology. We conclude that dynamic equilibria in Cry toxin production, as well as strong spatial structure and population bottlenecks in hosts are the main ecological factors maintaining the cooperative secretion of virulence factors and argue that collective action has contributed to the evolution of narrow host range. Non-linearities in the benefits associated with public goods, as well as the lack of private secretion systems in the Firmicutes may also explain the prevalence and importance of distantly acting virulence factors in B. cereus and its relatives. © 2013 WILEY Periodicals, Inc.
Abstract.
Raymond B, Wright DJ, Crickmore N, Bonsall MB (2013). The impact of strain diversity and mixed infections on the evolution of resistance to Bacillus thuringiensis.
Proceedings of the Royal Society B: Biological Sciences,
280(1769).
Abstract:
The impact of strain diversity and mixed infections on the evolution of resistance to Bacillus thuringiensis
Pesticide mixtures can reduce the rate at which insects evolve pesticide resistance. However, with live biopesticides such as the naturally abundant pathogen Bacillus thuringiensis (Bt), a range of additional biological considerations might affect the evolution of resistance. These can include ecological interactions in mixed infections, the different rates of transmission postapplication and the impact of the native biodiversity on the frequency of mixed infections. Using multi-generation selection experiments, we tested how applications of single and mixed strains of Bt from diverse sources (natural isolates and biopesticides) affected the evolution of resistance in the diamondback moth, Plutella xylostella, to a focal strain. Therewas no significant difference in the rate of evolution of resistance between single and mixed-strain applications although the latter did result in lower insect populations. The relative survivorship of Bt-resistant genotypes was higher in the mixed-strain treatment, in part owing to elevated mortality of susceptible larvae in mixtures. Resistance evolved more quickly with treatments that contained natural isolates, and biological differences in transmission rate may have contributed to this. Our data indicate that the use of mixtures can have unexpected consequences on the fitness of resistant and susceptible insects. © 2013 the Authors.
Abstract.
2012
Raymond B, West SA, Griffin AS, Bonsall MB (2012). The dynamics of cooperative bacterial virulence in the field.
Science,
336(6090), 85-88.
Abstract:
The dynamics of cooperative bacterial virulence in the field
Laboratory experiments have shown that the fitness of microorganisms can depend on cooperation between cells. Although this insight has revolutionized our understanding of microbial life, results from artificial microcosms have not been validated in complex natural populations. We investigated the sociality of essential virulence factors (crystal toxins) in the pathogen Bacillus thuringiensis using diamondback moth larvae (Plutella xylostella) as hosts. We show that toxin production is cooperative, and in a manipulative field experiment, we observed persistent high relatedness and frequency- and density-dependent selection, which favor stable cooperation. Conditions favoring social virulence can therefore persist in the face of natural population processes, and social interactions (rapid cheat invasion) may account for the rarity of natural disease outbreaks caused by B. thuringiensis.
Abstract.
2011
Garbutt J, Bonsall MB, Wright DJ, Raymond B (2011). Antagonistic competition moderates virulence in Bacillus thuringiensis.
ECOLOGY LETTERS,
14(8), 765-772.
Author URL.
Raymond B, Wright DJ, Bonsall MB (2011). Effects of host plant and genetic background on the fitness costs of resistance to Bacillus thuringiensis.
Heredity,
106(2), 281-288.
Abstract:
Effects of host plant and genetic background on the fitness costs of resistance to Bacillus thuringiensis
Novel resistance to pathogens and pesticides is commonly associated with a fitness cost. However, measurements of the fitness costs of insecticide resistance have used diverse methods to control for genetic background and rarely assess the effects of environmental variation. Here, we explored how genetic background interacts with resource quality to affect the expression of the fitness costs associated with resistance. We used a serially backcrossed line of the diamondback moth, Plutella xylostella, resistant to the biopesticide Bacillus thuringiensis, to estimate the costs of resistance for insects feeding on two Brassica species. We found that fitness costs increased on the better-defended Brassica oleracea cultivars. These data were included in two meta-analyses of fitness cost experiments that used standardized protocols (and a common resistant insect stock) but which varied in the methodology used to control for the effects of genetic background. The meta-analysis confirmed that fitness costs were higher on the low-quality host (B. oleracea); and experimental methodology did not influence estimates of fitness costs on that plant species. In contrast, fitness costs were heterogeneous in the Brassica pekinensis studies: fitness costs in genetically homogenized lines were significantly higher than in studies using revertant insects. We hypothesize that fitness modifiers can moderate fitness costs on high-quality plants but may not affect fitness when resource quality is low. © 2011 Macmillan Publishers Limited all rights reserved.
Abstract.
2010
Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N (2010). Bacillus thuringiensis: an impotent pathogen?.
TRENDS IN MICROBIOLOGY,
18(5), 189-194.
Author URL.
Raymond B, Wyres KL, Sheppard SK, Ellis RJ, Bonsall MB (2010). Environmental factors determining the epidemiology and population genetic structure of the bacillus cereus group in the field.
PLoS Pathogens,
6(5), 1-13.
Abstract:
Environmental factors determining the epidemiology and population genetic structure of the bacillus cereus group in the field
Bacillus thuringiensis (Bt) and its insecticidal toxins are widely exploited in microbial biopesticides and genetically modified crops. Its population biology is, however, poorly understood. Important issues for the safe, sustainable exploitation of Bt include understanding how selection maintains expression of insecticidal toxins in nature, whether entomopathogenic Bt is ecologically distinct from related human pathogens in the Bacillus cereus group, and how the use of microbial pesticides alters natural bacterial populations. We addressed these questions with a MLST scheme applied to a field experiment in which we excluded/added insect hosts and microbial pesticides in a factorial design. The presence of insects increased the density of Bt/B. cereus in the soil and the proportion of strains expressing insecticidal toxins. We found a near-epidemic population structure dominated by a single entomopathogenic genotype (ST8) in sprayed and unsprayed enclosures. Biopesticidal ST8 proliferated in hosts after spraying but was also found naturally associated with leaves more than any other genotype. In an independent experiment several ST8 isolates proved better than a range of non-pathogenic STs at endophytic and epiphytic colonization of seedlings from soil. This is the first experimental demonstration of Bt behaving as a specialized insect pathogen in the field. These data provide a basis for understanding both Bt ecology and the influence of anthropogenic factors on Bt populations. This natural population of Bt showed habitat associations and a population structure that differed markedly from previous MLST studies of less ecologically coherent B. cereus sample collections. The host-specific adaptations of ST8, its close association with its toxin plasmid and its high prevalence within its clade are analogous to the biology of Bacillus anthracis. This prevalence also suggests that selection for resistance to the insecticidal toxins of ST8 will have been stronger than for other toxin classes. © 2010 Raymond et al.
Abstract.
Martinou AF, Raymond B, Milonas PG, Wright DJ (2010). Impact of intraguild predation on parasitoid foraging behaviour.
Ecological Entomology,
35(2), 183-189.
Abstract:
Impact of intraguild predation on parasitoid foraging behaviour
Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host-parasitoid dynamics. © 2010 the Authors. Journal compilation © 2010 the Royal Entomological Society.
Abstract.
2009
Raymond B, Johnston PR, Wright DJ, Ellis RJ, Crickmore N, Bonsall MB (2009). A mid-gut microbiota is not required for the pathogenicity of Bacillus thuringiensis to diamondback moth larvae.
ENVIRONMENTAL MICROBIOLOGY,
11(10), 2556-2563.
Author URL.
Raymond B, Ellis RJ, Bonsall MB (2009). Moderation of pathogen-induced mortality: the role of density in Bacillus thuringiensis virulence.
BIOLOGY LETTERS,
5(2), 218-220.
Author URL.
Raymond B, Wright DJ (2009). Resistance management of transgenic insect-Resistant crops: Ecological factors. In (Ed)
Environmental Impact of Genetically Modified Crops, 101-114.
Abstract:
Resistance management of transgenic insect-Resistant crops: Ecological factors
Abstract.
2008
Raymond B, Lijek RS, Griffiths RI, Bonsall MB (2008). Ecological consequences of ingestion of Bacillus cereus on Bacillus thuringiensis infections and on the gut flora of a lepidopteran host.
JOURNAL OF INVERTEBRATE PATHOLOGY,
99(1), 103-111.
Author URL.
Bonsall MB, Raymond B (2008). Lethal pathogens, non-lethal synergists and the evolutionary ecology of resistance.
JOURNAL OF THEORETICAL BIOLOGY,
254(2), 339-349.
Author URL.
Raymond B, Elliot SL, Ellis RJ (2008). Quantifying the reproduction of Bacillus thuringiensis HD1 in cadavers and live larvae of Plutella xylostella.
Journal of Invertebrate Pathology,
98(3), 307-313.
Abstract:
Quantifying the reproduction of Bacillus thuringiensis HD1 in cadavers and live larvae of Plutella xylostella
The Bacillus cereus group comprises a range of micro-organisms with diverse habits, including gut commensals, opportunistic pathogens and soil saprophytes. Using quantitative microbiological methods we tested whether Bacillus thuringiensis (Bt) could reproduce in cadavers of Plutella xylostella killed by Bt, or in the gut of live insects, or be transmitted vertically from females to their offspring. We also tested whether diverse Bt strains could grow in high nutrient broth at a pH similar to that in the larval midgut. Low levels of reproduction were found in insect cadavers but there was no evidence of vertical transmission, or of significant reproduction in live insects. Four strains of B. thuringiensis var. kurstaki and one of B. thuringiensis var. tenebrionis were found to be capable of growth at high pH. Greater spore recovery rates in frass were found in hosts that were resistant or tolerant of infection. We concluded that that spores recovered in frass represent, in general, an ungerminated fraction of ingested inoculum and that germination rates are reduced in unsuitable hosts. © 2008 Elsevier Inc. All rights reserved.
Abstract.
2007
Raymond B, Davis D, Bonsall MB (2007). Competition and reproduction in mixed infections of pathogenic and non-pathogenic Bacillus spp.
JOURNAL OF INVERTEBRATE PATHOLOGY,
96(2), 151-155.
Author URL.
Raymond B, Sayyed AH, Hails RS, Wright DJ (2007). Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis.
JOURNAL OF APPLIED ECOLOGY,
44(4), 768-780.
Author URL.
Raymond B, Sayyed AH, Wright DJ (2007). Host plant and population determine the fitness costs of resistance to Bacillus thuringiensis.
Biol Lett,
3(1), 82-85.
Abstract:
Host plant and population determine the fitness costs of resistance to Bacillus thuringiensis.
Novel adaptations often cause pleiotropic reductions in fitness. Under optimal conditions individual organisms may be able to compensate for, or reduce, these fitness costs. Declining environmental quality may therefore lead to larger costs. We investigated whether reduced plant quality would increase the fitness costs associated with resistance to Bacillus thuringiensis in two populations of the diamondback moth Plutella xylostella. We also measured the rate of decline in resistance on two host-plant (Brassica) species for one insect population (Karak). Population X plant species interactions determined the fitness costs in this study. Poor plant quality increased the fitness costs in terms of development time for both populations. However, fitness costs seen in larval survival did not always increase as plant quality declined. Both the fitness and the stability experiment indicated that fitness costs were higher on the most suitable plant for one population. Theoretically, if the fitness cost of a mutation interacts additively with environmental factors, the relative fitness of resistant insects will decrease with environmental quality. However, multiplicative costs do not necessarily increase with declining quality and may be harder to detect when fitness parameters are more subject to variation in poorer environments.
Abstract.
Author URL.
Raymond B, Hails RS (2007). Variation in plant resource quality and the transmission and fitness of the winter moth, Operophtera brumata nucleopolyhedrovirus.
BIOLOGICAL CONTROL,
41(2), 237-245.
Author URL.
2006
Raymond B, Sayyed AH, Wright DJ (2006). The compatibility of a nucleopolyhedrosis virus control with resistance management for Bacillus thuringiensis: Co-infection and cross-resistance studies with the diamondback moth, Plutella xylostella.
Journal of Invertebrate Pathology,
93(2), 114-120.
Abstract:
The compatibility of a nucleopolyhedrosis virus control with resistance management for Bacillus thuringiensis: Co-infection and cross-resistance studies with the diamondback moth, Plutella xylostella
The use of genetically modified crops expressing Bacillus thuringiensis (Bt) toxins can lead to the reduction in application of broad-spectrum pesticides and an increased opportunity for supplementary biological control. Bt microbial sprays are also used by organic growers or as part of integrated pest management programs that rely on the use of natural enemies. In both applications the evolution of resistance to Bt toxins is a potential problem. Natural enemies (pathogens or insects) acting in combination with toxins can accelerate or decelerate the evolution of resistance to Bt. In the present study we investigated whether the use of a nucleopolyhedrovirus (AcMNPV) could potentially affect the evolution of resistance to the Bt toxin Cry1Ac in Plutella xylostella. At low toxin doses there was evidence for antagonistic interactions between AcMNPV and Cry1Ac resistant and susceptible insects. However, this antagonism was much stronger and more widespread for susceptible larvae; interactions were generally not distinguishable from additive for resistant larvae. Selection for resistance to Cry1Ac in two populations of P. xylostella with differing resistance mechanisms did not produce any correlated changes in resistance to AcMNPV. Stronger antagonistic interactions between Bt and AcMNPV on susceptible rather than resistant larvae can decrease the relative fitness between Bt-resistant and susceptible larvae. These interactions and the lack of cross-resistance between virus and toxin suggest that the use of NPV is compatible with resistance management to Bt products. © 2006 Elsevier Inc. All rights reserved.
Abstract.
2005
Raymond B, Sayyed AH, Wright DJ (2005). Genes and environment interact to determine the fitness costs of resistance to Bacillus thuringiensis.
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES,
272(1571), 1519-1524.
Author URL.
Raymond B, Hartley SE, Cory JS, Hails RS (2005). The role of food plant and pathogen-induced behaviour in the persistence of a nucleopolyhedrovirus.
Journal of Invertebrate Pathology,
88(1), 49-57.
Abstract:
The role of food plant and pathogen-induced behaviour in the persistence of a nucleopolyhedrovirus
Insect baculoviruses can survive between epidemics as infectious particles external to the host. Many pathogens persist in reservoirs, i.e. microhabitats where survival is enhanced, for example due to protection from the degrading effects of UV irradiation. However, the probability of infecting new susceptible hosts is usually reduced. Persistence of pathogens and their movement in and out of reservoirs is an important, albeit little understood, aspect of insect pathogen ecology. This study investigated interactions between the behaviour of infected insect hosts, virus distribution and plant species on the persistence of the winter moth (Operophtera brumata) nucleopolyhedrovirus. Habitat influenced the persistence of infectious baculovirus in the field: virus on Sitka spruce (Picea sitchensis) and oak (Quercus robur) in forested areas retained more infectivity than virus on heather (Calluna vulgaris) in an unshaded habitat. Plant species per se did not directly affect the persistence of virus on the foliage of potted seedlings. Virally infected insects had altered behaviour and moved down plants relative to control insects, whereas in other systems larvae show height-seeking behaviour. Consequently, the majority of virus particles were distributed on plant stems. In two experiments (one using winter moth NPV and one Mamestra brassicae NPV) virus persisted better on plant stems relative to foliage. Neonate larvae were shown to be able to acquire infections from tree stems contaminated with a low level of virus. These data suggest that plant stems may be important reservoirs for between-year persistence of this pathogen. The observed virus-induced changes in host behaviour in winter moth could enhance the viral persistence by increasing the deposition of occlusion bodies in these reservoirs. © 2004 Elsevier Inc. All rights reserved.
Abstract.
2004
Sayyed AH, Raymond B, Ibiza-Palacios MS, Escriche B, Wright DJ (2004). Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac in the diamondback moth, Plutella xylostella.
Applied and Environmental Microbiology,
70(12), 7010-7017.
Abstract:
Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac in the diamondback moth, Plutella xylostella
The long-term usefulness of Bacillus thuringiensis Cry toxins, either in sprays or in transgenic crops, may be compromised by the evolution of resistance in target insects. Managing the evolution of resistance to B. thuringiensis toxins requires extensive knowledge about the mechanisms, genetics, and ecology of resistance genes. To date, laboratory-selected populations have provided information on the diverse genetics and mechanisms of resistance to B. thuringiensis, highly resistant field populations being rare. However, the selection pressures on field and laboratory populations are very different and may produce resistance genes with distinct characteristics. In order to better understand the genetics, biochemical mechanisms, and ecology of field-evolved resistance, a diamondback moth (Plutella xylostella) field population (Karak) which had been exposed to intensive spraying with B. thuringiensis subsp. kurstaki was collected from Malaysia. We detected a very high level of resistance to Cry1Ac; high levels of resistance to B. thuringiensis subsp. kurstaki Cry1Aa, Cry1Ab, and Cry1Fa; and a moderate level of resistance to Cry1Ca. The toxicity of Cry1Ja to the Karak population was not significantly different from that to a standard laboratory population (LAB-UK). Notable features of the Karak population were that field-selected resistance to B. thuringiensis subsp. kurstaki did not decline at all in unselected populations over 11 generations in laboratory microcosm experiments and that resistance to Cry1Ac declined only threefold over the same period. This finding may be due to a lack of fitness costs expressed by resistance strains, since such costs can be environmentally dependent and may not occur under ordinary laboratory culture conditions. Alternatively, resistance in the Karak population may have been near fixation, leading to a very slow increase in heterozygosity. Reciprocal genetic crosses between Karak and LAB-UK populations indicated that resistance was autosomal and recessive. At the highest dose of CrylAc tested, resistance was completely recessive, while at the lowest dose, it was incompletely dominant. A direct test of monogenic inheritance based on a backcross of F1 progeny with the Karak population suggested that resistance to Cry1Ac was controlled by a single locus. Binding studies with 125I-labeled Cry1Ab and Cry1Ac revealed greatly reduced binding to brush border membrane vesicles prepared from this field population.
Abstract.
2003
Vanbergen AJ, Raymond B, Pearce ISK, Watt AD, Hails RS, Hartley SE (2003). Host shifting by Operophtera brumata into novel environments leads to population differentiation in life-history traits.
ECOLOGICAL ENTOMOLOGY,
28(5), 604-612.
Author URL.
2002
Raymond B, Vanbergen A, Watt A, Hartley SE, Cory JS, Hails RS (2002). Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata.
Oikos,
98(2), 219-228.
Abstract:
Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata
The winter moth, Operophtera brumata, shows varying population dynamics in different host plant habitats. Populations in Sitka spruce, Picea sitchensis, plantations and in Scottish moorlands have a tendency to outbreak that is not shown by winter moth in lowland oak woods. Since pupal predators have previously been identified as being important for the regulation of winter moth in a lowland oak wood it was hypothesized that invertebrate pupal predators were failing to control winter moth in outbreak populations. This hypothesis was tested by comparing the abundance of invertebrate predators and patterns of spatially density dependent pupal predation across habitats. Several results supported this hypothesis. Carabid predators of winter moth were one or two orders of magnitude more abundant in oak woods than in moorland or spruce habitats. Staphylinid predators were also more abundant in high winter moth density oak woods than in any other habitat. Beetle predation of tagged cocoons in the field was inversely density dependent in Highland moors in experiments in 1999 and 2000, and in Sitka spruce in 1999. However, in opposition to our hypothesis, pupal predation was also inversely density dependent in oak woods in 2000, although this result may be explained by the low range of winter moth densities in the field that year. These results are discussed in relation to the role of natural enemies in regulating winter moth populations and the differences in life-history of the beetle predators in different habitats.
Abstract.
Raymond B, Vanbergen A, Pearce I, Hartley SE, Cory JS, Hails RS (2002). Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus.
Oecologia,
131(4), 533-541.
Abstract:
Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus
Plants can have a significant impact on the fitness and efficacy of natural enemies. These interactions are widespread and suggest that the influences on the population dynamics of insect herbivores cannot be simply divided into "bottom up" and "top down". Several questions remain little studied in this field. Firstly, to what extent can plants affect the interactions between insects and their pathogens? Secondly, what are the effects of variation within natural enemy species on host/enemy/plant interactions? Finally, if plant/pathogen interactions can occur, do pathogens have increased fitness on the locally abundant food plant of their host? This study explored the influence of three host plant species of the polyphagous winter moth, Operophtera brumata, on infections caused by two geographic isolates of the winter moth nucleopolyhedrovirus (NPV) collected from distinct winter moth habitats. Insects were infected on excised leaf tissue of common oak, Quercus robur, Sitka spruce, Picea sitchenis, and heather, Calluna vulgaris. Parameters fundamental to the basic reproductive rate of the pathogen were estimated: these being infectivity, speed of kill and the yield of virus per insect. Leaf nitrogen and phenolic content were measured as indicators of host plant quality for the three plant species: oak had the highest levels of nitrogen and also the highest levels of phenolic compounds. Heather had higher levels of phenolic compounds than Sitka spruce. Host plant did not affect the infectivity of either isolate but insects that ingested virus on oak foliage died sooner and yielded more virus than insects that ingested virus on Sitka spruce or heather. The effect of host plant species on pathogen yield varied between the two isolates of the NPV but not as predicted by our adaptive hypothesis. The interactions between virus and food plant are discussed in relation to host and pathogen population dynamics.
Abstract.
2001
Raymond B, Searle JB, Douglas AE (2001). On the processes shaping reproductive isolation in aphids of the Aphis fabae (Scop.) complex (Aphididae: Homoptera).
Biological Journal of the Linnean Society,
74(2), 205-215.
Abstract:
On the processes shaping reproductive isolation in aphids of the Aphis fabae (Scop.) complex (Aphididae: Homoptera)
Models of sympatric speciation for phytophagous insects are based on the premise that ecological specialization on different host plants can indirectly result in significant reproductive isolation. A candidate example of host plant shift is provided by the partially reproductively-isolated aphids Aphis fabae fabae and A. f. mordwilkoi, which utilize different hosts for sexual reproduction. However, unexpected isolation based on mating behaviour was found for these two aphids. In olfactometer trials, males responded to the pheromones of females of both subspecies when presented a subspecies in isolation but preferentially to females of the same subspecies in choice tests. On contact, the incidence or duration of between-subspecies copulations was significantly lower than same-subspecies copulations, and spermatozoa were transferred during 88% of the same-subspecies copulations, but only 19% of between-subspecies copulations. These data are indicative of strong pre-zygotic isolation between the subspecies. Complementary restriction analysis of mitochondrial DNA and a plasmid (pAFEleu) in an obligate symbiotic bacterium (Buchnera) revealed a paraphyletic relationship among four subspecies of A. fabae (A. f. fabae, A. f. mordwilkoi, A. f. cirsiiacanthoidis and A. f. solanella). We discuss how the lack of clear genetic differentiation between A. f. fabae and A. f. mordwilkoi, despite substantial pre-zygotic isolation, may be a consequence of reinforcement. © 2001 the Linnean Society of London.
Abstract.
2000
Raymond B, Darby AC, Douglas AE (2000). Intraguild predators and the spatial distribution of a parasitoid.
OECOLOGIA,
124(3), 367-372.
Author URL.
Raymond B, Darby AC, Douglas AE (2000). The olfactory responses of coccinellids to aphids on plants.
ENTOMOLOGIA EXPERIMENTALIS ET APPLICATA,
95(1), 113-117.
Author URL.
1999
Raymond B (1999). Biological determinism unwarranted.
Psycoloquy,
10Abstract:
Biological determinism unwarranted
Jensen (1998) does not present any evidence for the external validity of g other than through biological correlations with IQ. Hence it is impossible to assess the validity of g in comparison with competing theories from this book. The author's interpretation of heritability estimates of IQ and of racial differences in IQ adoption studies ignores any potential maternal effects on IQ. His insistence that the primary cause of variation in IQ within and between races is genetic does not seem warranted by the evidence presented.
Abstract.
