Small Fitness Costs Research Articles

The Battle between Bacteria and Bacteriophages: A Conundrum to Their Immune System.

Bacteria and their predators, bacteriophages, or phages are continuously engaged in an arms race for their survival using various defense strategies. Several studies indicated that the bacterial immune arsenal towards phage is quite diverse and uses different components of the host machinery. Most studied antiphage systems are associated with phages, whose genomic matter is double-stranded-DNA. These defense mechanisms are mainly related to either the host or phage-derived proteins and other associated structures and biomolecules. Some of these strategies include DNA restriction-modification (R-M), spontaneous mutations, blocking of phage receptors, production of competitive inhibitors and extracellular matrix which prevent the entry of phage DNA into the host cytoplasm, assembly interference, abortive infection, toxin-antitoxin systems, bacterial retrons, and secondary metabolite-based replication interference. On the contrary, phages develop anti-phage resistance defense mechanisms in consortium with each of these bacterial phage resistance strategies with small fitness cost. These mechanisms allow phages to undergo their replication safely inside their bacterial host's cytoplasm and be able to produce viable, competent, and immunologically endured progeny virions for the next generation. In this review, we highlight the major bacterial defense systems developed against their predators and some of the phage counterstrategies and suggest potential research directions.

Introduction: the secret lives of microbial mobile genetic elements.

Introduction: the secret lives of microbial mobile genetic elements.

Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli.

Plasmid-mediated antimicrobial resistance is a major contributor to the spread of resistance genes within bacterial communities. Successful plasmid spread depends upon a balance between plasmid fitness effects on the host and rates of horizontal transmission. While these key parameters are readily quantified in vitro, the influence of interactions with other microbiome members is largely unknown. Here, we investigated the influence of three genera of lactic acid bacteria (LAB) derived from the chicken gastrointestinal microbiome on the spread of an epidemic narrow-range ESBL resistance plasmid, IncI1 carrying blaCTX-M-1, in mixed cultures of isogenic Escherichia coli strains. Secreted products of LAB decreased E. coli growth rates in a genus-specific manner but did not affect plasmid transfer rates. Importantly, we quantified plasmid transfer rates by controlling for density-dependent mating opportunities. Parametrization of a mathematical model with our in vitro estimates illustrated that small fitness costs of plasmid carriage may tip the balance towards plasmid loss under growth conditions in the gastrointestinal tract. This work shows that microbial interactions can influence plasmid success and provides an experimental-theoretical framework for further study of plasmid transfer in a microbiome context.

A general model of biological signals, from cues to handicaps.

Organisms sometimes appear to use extravagant traits, or “handicaps”, to signal their quality to an interested receiver. Before they were used as signals, many of these traits might have been selected to increase with individual quality for reasons apart from conveying information, allowing receivers to use the traits as “cues” of quality. However, current theory does not explain when and why cues of individual quality become exaggerated into costly handicaps. We address this here, using a game‐theoretic model of adaptive signalling. Our model predicts that: (1) signals will honestly reflect signaler quality whenever there is a positive relationship between individual quality and the signalling trait's naturally selected, non‐informational optimum; and (2) the slope of this relationship will determine the amount of costly signal exaggeration, with more exaggeration favored when the slope is more shallow. A shallow slope means that a lower quality male would pay only a small fitness cost to have the same trait value as a higher quality male, and this drives the exaggeration of signals as high‐quality signalers are selected to distinguish themselves. Our model reveals a simple and potentially widespread mechanism for ensuring signal honesty and predicts a natural continuum of signalling strategies, from cost‐free cues to costly handicaps.

Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus.

CRISPR-Cas is a form of adaptive sequence-specific immunity in microbes. This system offers unique opportunities for the study of coevolution between bacteria and their viral pathogens, bacteriophages. A full understanding of the coevolutionary dynamics of CRISPR-Cas requires knowing the magnitude of the cost of resisting infection. Here, using the gram-positive bacterium Streptococcus thermophilus and its associated virulent phage 2972, a well-established model system harbouring at least two type II functional CRISPR-Cas systems, we obtained different fitness measures based on growth assays in isolation or in pairwise competition. We measured the fitness cost associated with different components of this adaptive immune system: the cost of Cas protein expression, the constitutive cost of increasing immune memory through additional spacers, and the conditional costs of immunity during phage exposure. We found that Cas protein expression is particularly costly, as Cas-deficient mutants achieved higher competitive abilities than the wild-type strain with functional Cas proteins. Increasing immune memory by acquiring up to four phage-derived spacers was not associated with fitness costs. In addition, the activation of the CRISPR-Cas system during phage exposure induces significant but small fitness costs. Together these results suggest that the costs of the CRISPR-Cas system arise mainly due to the maintenance of the defence system. We discuss the implications of these results for the evolution of CRISPR-Cas-mediated immunity.

Development of disease-resistant rice using regulatory components of induced disease resistance.

Infectious diseases cause huge crop losses annually. In response to pathogen attacks, plants activate defense systems that are mediated through various signaling pathways. The salicylic acid (SA) signaling pathway is the most powerful of these pathways. Several regulatory components of the SA signaling pathway have been identified, and are potential targets for genetic manipulation of plants’ disease resistance. However, the resistance associated with these regulatory components is often accompanied by fitness costs; that is, negative effects on plant growth and crop yield. Chemical defense inducers, such as benzothiadiazole and probenazole, act on the SA pathway and induce strong resistance to various pathogens without major fitness costs, owing to their ‘priming effect.’ Studies on how benzothiadiazole induces disease resistance in rice have identified WRKY45, a key transcription factor in the branched SA pathway, and OsNPR1/NH1. Rice plants overexpressing WRKY45 were extremely resistant to rice blast disease caused by the fungus Magnaporthe oryzae and bacterial leaf blight disease caused by Xanthomonas oryzae pv. oryzae (Xoo), the two major rice diseases. Disease resistance is often accompanied by fitness costs; however, WRKY45 overexpression imposed relatively small fitness costs on rice because of its priming effect. This priming effect was similar to that of chemical defense inducers, although the fitness costs were amplified by some environmental factors. WRKY45 is degraded by the ubiquitin–proteasome system, and the dual role of this degradation partly explains the priming effect. The synergistic interaction between SA and cytokinin signaling that activates WRKY45 also likely contributes to the priming effect. With a main focus on these studies, I review the current knowledge of SA-pathway-dependent defense in rice by comparing it with that in Arabidopsis, and discuss potential strategies to develop disease-resistant rice using signaling components.

Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission

Genetic manipulations of insect populations for pest control have been advocated for some time, but there are few cases where manipulated individuals have been released in the field and no cases where they have successfully invaded target populations. Population transformation using the intracellular bacterium Wolbachia is particularly attractive because this maternally-inherited agent provides a powerful mechanism to invade natural populations through cytoplasmic incompatibility. When Wolbachia are introduced into mosquitoes, they interfere with pathogen transmission and influence key life history traits such as lifespan. Here we describe how the wMel Wolbachia infection, introduced into the dengue vector Aedes aegypti from Drosophila melanogaster, successfully invaded two natural A. aegypti populations in Australia, reaching near-fixation in a few months following releases of wMel-infected A. aegypti adults. Models with plausible parameter values indicate that Wolbachia-infected mosquitoes suffered relatively small fitness costs, leading to an unstable equilibrium frequency <30% that must be exceeded for invasion. These findings demonstrate that Wolbachia-based strategies can be deployed as a practical approach to dengue suppression with potential for area-wide implementation.

Transgenes for insect resistance reduce herbivory and enhance fecundity in advanced generations of crop-weed hybrids of rice.

Gene flow from transgenic crops allows novel traits to spread to sexually compatible weeds. Traits such as resistance to insects may enhance the fitness of weeds, but few studies have tested for these effects under natural field conditions. We created F2 and F3 crop–weed hybrid lineages of genetically engineered rice (Oryza sativa) using lines with two transgene constructs, cowpea trypsin inhibitor (CpTI) and a Bt transgene linked to CpTI (Bt/CpTI). Experiments conducted in Fuzhou, China, demonstrated that CpTI alone did not significantly affect fecundity, although it reduced herbivory. In contrast, under certain conditions, Bt/CpTI conferred up to 79% less insect damage and 47% greater fecundity relative to nontransgenic controls, and a 44% increase in fecundity relative to the weedy parent. A small fitness cost was detected in F3 progeny with Bt/CpTI when grown under low insect pressure and direct competition with transgene-negative controls. We conclude that Bt/CpTI transgenes may introgress into co-occurring weedy rice populations and contribute to greater seed production when target insects are abundant. However, the net fitness benefits that are associated with Bt/CpTI could be ephemeral if insect pressure is lacking, for example, because of widespread planting of Bt cultivars that suppress target insect populations.

Impact of Small Fitness Costs on Pest Adaptation to Crop Varieties with Multiple Toxins: A Heuristic Model

A deterministic two-locus model was used to examine how small fitness costs to individuals carrying resistance alleles could impact the risk of panmictic insect pest populations adapting to crop varieties that produced two distinct toxins. Parameters examined were (1) level of toxicity of each toxin, (2) initial frequencies of alleles for adaptation to the toxins, (3) percentage of population feeding on nontoxic plants, and (4) level of fitness cost associated with adaptation to each of the two toxins. Resistance to each toxin was assumed to be biochemically independent, controlled by a resistance coding allele at a single locus, and inherited as a partially recessive trait in the field. When plants are extremely toxic to the pest, effective refuge size is 10%, and there is a fitness cost to resistance alleles only when in homozygous form (5%), the pest population is never predicted to adapt to either toxin as long as the initial frequencies of the resistance alleles are below 0.05. Even if the initial frequency of the allele for adapting to one toxin is 0.95 when a two-toxin cultivar completely replaces a one-toxin cultivar, the model predicts that a low equilibrium allelic frequency will develop for both resistance alleles, as long as the frequency of the allele for adapting to the second toxin is initially 0.001 or less. If cultivars with one and two toxins are planted, the model predicts that resistance will develop. Nonrandom mating and stochastic variation within subpopulations also could lead to evolution of resistance.

Impact of Small Fitness Costs on Pest Adaptation to Crop Varieties with Multiple Toxins: A Heuristic Model

A deterministic two-locus model was used to examine how small fitness costs to individuals carrying resistance alleles could impact the risk of panmictic insect pest populations adapting to crop varieties that produced two distinct toxins. Parameters examined were 1) level of toxicity of each toxin, 2) initial frequencies of alleles for adaptation to the toxins, 3) percentage of population feeding on nontoxic plants, and 4) level of fitness cost associated with adaptation to each of the two toxins. Resistance to each toxin was assumed to be biochemically independent, controlled by a resistance coding allele at a single locus, and inherited as a partially recessive trait in the field. When plants are extremely toxic to the pest, effective refuge size is 10%, and there is a fitness cost to resistance alleles only when in homozygous form (5%), the pest population is never predicted to adapt to either toxin as long as the initial frequencies of the resistance alleles are below 0.05. Even if the initial frequency of the allele for adapting to one toxin is 0.95 when a two-toxin cultivar completely replaces a one-toxin cultivar, the model predicts that a low equilibrium allelic frequency will develop for both resistance alleles, as long as the frequency of the allele for adapting to the second toxin is initially 0.001 or less. If cultivars with one and two toxins are planted, the model predicts that resistance will develop. Nonrandom mating and stochastic variation within subpopulations also could lead to evolution of resistance.

Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element

Little is known of the fitness cost that antibiotic resistance exerts on wild-type bacteria, especially in their natural environments. We therefore examined the fitness costs that several antibiotic resistance elements imposed on a wild-type Escherichia coli isolate, both in the laboratory and in a pig gut colonization model. Plasmid R46, Tn1 and Tn7 and a K42R RpsL substitution were separately introduced into E. coli 345-2 RifC, a rifampicin-resistant derivative of a recent porcine isolate. The insertion site of Tn1 was determined by DNA sequencing. The fitness cost of each resistance element was assessed in vitro by pairwise growth competition and in vivo by regularly monitoring the recovery of strains from faeces for 21 days following oral inoculation of organic piglets. Each derivative of 345-2 RifC carrying a resistance element was grown in antibiotic-free broth for 200 generations and the experiments to assess fitness were repeated. RpsL K42R was found to impose a small fitness cost on E. coli 345-2 RifC in vitro but did not compromise survival in vivo. R46 imposed a cost both before and after laboratory passage in vitro, but only the pre-passage strain was at a disadvantage in vivo. The post-passage isolate had an advantage in pigs. Acquisition of Tn7 had no impact on the fitness of E. coli 345-2 RifC. Two derivatives containing Tn1 were isolated and, in both cases, the transposon inserted into the same cryptic chromosomal sequence. Acquisition of Tn1 improved fitness of E. coli 345-2 RifC in vitro and in vivo in the case of the first derivative, but in the case of a second, independent derivative, Tn1 had a neutral effect on fitness. The fitness impact imposed on E. coli 345-2 RifC by carriage of antibiotic resistance elements was generally low or non-existent, suggesting that once established, resistance may be difficult to eliminate through reduction in prescribing alone.

Fitness cost of chromosomal drug resistance-conferring mutations.

To study the cost of chromosomal drug resistance mutations to bacteria, we investigated the fitness cost of mutations that confer resistance to different classes of antibiotics affecting bacterial protein synthesis (aminocyclitols, 2-deoxystreptamines, macrolides). We used a model system based on an in vitro competition assay with defined Mycobacterium smegmatis laboratory mutants; selected mutations were introduced by genetic techniques to address the possibility that compensatory mutations ameliorate the resistance cost. We found that the chromosomal drug resistance mutations studied often had only a small fitness cost; compensatory mutations were not involved in low-cost or no-cost resistance mutations. When drug resistance mutations found in clinical isolates were considered, selection of those mutations that have little or no fitness cost in the in vitro competition assay seems to occur. These results argue against expectations that link decreased levels of antibiotic consumption with the decline in the level of resistance.

Adoption of Chicks by the Pied Avocet

Data on the occurrence and frequency of adoption of chicks by adult Pied Avocets (Recurvirostra avosetta) were collected by monitoring individually color-banded chicks on alkaline lakes in the Kiskunság National Park in central Hungary between 1998 and 2000. Fifty-three adoptions were observed, and 22% of the resighted broods (N = 244) contained on average 1.7 (range 1-6) adopted chicks. Ninety-two chicks, or 13% of the color-banded chicks (N = 697) were adopted. The frequency of adoption was similar among years and was positively related to the number of pairs within a colony. At least 60% of the adoptions occurred in the nesting colonies, whereas adoptions during brood movements or in the brood-rearing areas, as well as brood amalgamations, were rare. More than two-thirds (68%) of the adopted chicks in the colony left the natal brood and joined other broods voluntarily. The remaining adopted chicks were the last to hatch in their own brood and were adopted into another brood after being left behind by their parents. Adults did not behave aggressively toward young alien chicks and always accepted them. Adoption appears to be initiated by chicks in Pied Avocets, and it may be associated with small fitness costs, or may even provide benefits, for the adoptees or the adopting adults.

Female multiple mating as a genetic bet‐hedging strategy when mate choice criteria are unreliable

Female multiple mating (or polyandry) is considered to act as a genetic bet‐hedging mechanism, by which females can reduce the assessment error in regard to mates’ genetic quality when only uncertain information is available. In spite of frequent verbal arguments, no theoretical examination has been carried out to determine the effectiveness of bet‐hedging by multiple mating. In the present paper, I show that three factors, female population size, remating costs and environmental fluctuation, all affect the effectiveness of bet‐hedging. A mathematical model predicts that bet‐hedging effectively works only in small populations, and computer simulations were used to confirm this prediction. The results of simulations differed according to the degree of environmental fluctuation. In relatively stable environments, if there is no remating cost, the fixation probability of a multiple mating strategy is slightly higher than that of a single mating strategy, independent of female population size. However, with very slight fitness costs, multiple mating drastically loses its advantage as population size increases, and almost always becomes extinct within large populations. This means that the evolution of polyandry solely by the mechanism of bet‐hedging is unlikely in stable environments. However, in unpredictable environments, or when negative frequency‐dependent selection on fitness‐related loci is introduced, a multiple mating strategy is sometimes successful against a single mating strategy, even if it entails a small fitness cost. Therefore, female multiple mating may possibly evolve only in these limited conditions. In most cases, some deterministic mechanisms such as postcopulatory sperm selection by multiply mated females (or direct ‘material’ benefits) are more reasonable as the evolutionary causes of polyandry.

Large genetic change at small fitness cost in large populations of Drosophila melanogaster selected for wind tunnel flight: rethinking fitness surfaces.

The fitness effects of extreme genetic change by selection were studied in large populations subjected to prolonged, intense selection. Two replicate populations of Drosophila melanogaster, with estimated effective sizes 500 < or = Ne < or = 1000, were selected for increased performance in a wind tunnel, selecting on average the fastest 4.5% of flies. The mean apparent flying speed of both lines increased from approximately 2 to 170 cm/sec and continued to respond at diminishing rates, without reaching a plateau, for 100 generations. Competitive fitness tests in generations 50 and 85 showed minimal or no fitness loss in selected lines compared to controls. Sublines relaxed in generations 65 and 85 showed minimal or no regression in apparent flying speed. Hybrid lines, from a cross of selected x control lines in generation 75, responded to reselection saltationally, showing that the chromosomes of the selected lines had been assembled from alleles at many loci, from many different chromosomes in the base population. Thus, major genetic change was achieved, but without the costs usually associated with strong directional selection. Large population size has been interpreted, in opposing models, as either a brake or an accelerator in its effects on long-term change by selection. These results favor the second model, and challenge the concept of rugged fitness surfaces underlying the first model.