Evolution of behavioural resistance in host-pathogen systems.
Ontology highlight
ABSTRACT:
SUBMITTER: Amoroso CR
PROVIDER: S-EPMC7532708 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Pathogens face a hostile and often novel environment when infecting a new host, and adaptation is likely to be an important determinant of the success in colonization and establishment. We hypothesized that resistant hosts will impose stronger selection on pathogens than susceptible hosts, which should accelerate pathogen evolution through selection biased toward effector genes. To test this hypothesis, we conducted an experimental evolution study on Xanthomonas citri subsp. citri (Xcc) in a susceptible plant species and a resistant plant species. We performed 55 rounds of repeated reinoculation of Xcc through susceptible host grapefruit (isolates G1, G2, G3) and resistant host kumquat (isolates K1, K2, K3). Consequently, only K1 and K3 isolates lost their ability to elicit a hypersensitive response (HR) in kumquat. Illumina sequencing of the parental and descendant strains P, G1, G2, G3, K1, K2 and K3 revealed that fixed mutations were biased toward type three secretion system effectors in isolates K1 and K3. Parallel evolution was observed in the K1 and K3 strains, suggesting that the mutations result from selection rather than by random drift. Our results support our hypothesis and suggest that repeated infection of resistant hosts by pathogens should be prevented to avoid selecting for adaptive pathogens.
| S-EPMC3930326 | biostudies-other
Project description:Host resistance consists of defences that limit pathogen burden, and can be classified as either adaptations targeting recovery from infection or those focused upon infection avoidance. Conventional theory treats avoidance as a fixed strategy which does not vary from one interaction to the next. However, there is increasing empirical evidence that many avoidance strategies are triggered by external stimuli, and thus should be treated as phenotypically plastic responses. Here, we consider the implications of avoidance plasticity for host-pathogen coevolution. We uncover a number of predictions challenging current theory. First, in the absence of pathogen trade-offs, plasticity can restrain pathogen evolution; moreover, the pathogen exploits conditions in which the host would otherwise invest less in resistance, causing resistance escalation. Second, when transmission trades off with pathogen-induced mortality, plasticity encourages avirulence, resulting in a superior fitness outcome for both host and pathogen. Third, plasticity ensures the sterilizing effect of pathogens has consequences for pathogen evolution. When pathogens castrate hosts, selection forces them to minimize mortality virulence; moreover, when transmission trades off with sterility alone, resistance plasticity is sufficient to prevent pathogens from evolving to fully castrate.
| S-EPMC4571713 | biostudies-literature
Project description:Metapopulation processes are important determinants of epidemiological and evolutionary dynamics in host-pathogen systems, and are therefore central to explaining observed patterns of disease or genetic diversity. In particular, the spatial scale of interactions between pathogens and their hosts is of primary importance because migration rates of one species can affect both spatial and temporal heterogeneity of selection on the other. In this study we developed a stochastic and discrete time simulation model to specifically examine the joint effects of host and pathogen dispersal on the evolution of pathogen specialisation in a spatially explicit metapopulation. We consider a plant-pathogen system in which the host metapopulation is composed of two plant genotypes. The pathogen is dispersed by air-borne spores on the host metapopulation. The pathogen population is characterised by a single life-history trait under selection, the infection efficacy. We found that restricted host dispersal can lead to high amount of pathogen diversity and that the extent of pathogen specialisation varied according to the spatial scale of host-pathogen dispersal. We also discuss the role of population asynchrony in determining pathogen evolutionary outcomes.
| S-EPMC4031062 | biostudies-literature
Project description:Understanding how habitat heterogeneity may affect the evolution of plant pathogens is essential to effectively predict new epidemiological landscapes and manage genetic diversity under changing global climatic conditions. In this study, we explore the effects of habitat heterogeneity, as determined by variation in host resistance and local temperature, on the evolution of Zymoseptoria tritici by comparing the aggressiveness development of five Z. tritici populations originated from different parts of the world on two wheat cultivars varying in resistance to the pathogen. Our results show that host resistance plays an important role in the evolution of Z. tritici. The pathogen was under weak, constraining selection on a host with quantitative resistance but under a stronger, directional selection on a susceptible host. This difference is consistent with theoretical expectations that suggest that quantitative resistance may slow down the evolution of pathogens and therefore be more durable. Our results also show that local temperature interacts with host resistance in influencing the evolution of the pathogen. When infecting a susceptible host, aggressiveness development of Z. tritici was negatively correlated to temperatures of the original collection sites, suggesting a trade-off between the pathogen's abilities of adapting to higher temperature and causing disease and global warming may have a negative effect on the evolution of pathogens. The finding that no such relationship was detected when the pathogen infected the partially resistant cultivars indicates the evolution of pathogens in quantitatively resistant hosts is less influenced by environments than in susceptible hosts.
| S-EPMC5487519 | biostudies-literature
Project description:As human population density and antibiotic exposure increase, specialised bacterial subtypes have begun to emerge. Arising among species that are common commensals and infrequent pathogens, antibiotic-resistant 'high-risk clones' have evolved to better survive in the modern human. Here, we show that the major matrix porin (OmpK35) of Klebsiella pneumoniae is not required in the mammalian host for colonisation, pathogenesis, nor for antibiotic resistance, and that it is commonly absent in pathogenic isolates. This is found in association with, but apparently independent of, a highly specific change in the co-regulated partner porin, the osmoporin (OmpK36), which provides enhanced antibiotic resistance without significant loss of fitness in the mammalian host. These features are common in well-described 'high-risk clones' of K. pneumoniae, as well as in unrelated members of this species and similar adaptations are found in other members of the Enterobacteriaceae that share this lifestyle. Available sequence data indicate evolutionary convergence, with implications for the spread of lethal antibiotic-resistant pathogens in humans.
| S-EPMC6436753 | biostudies-literature
Project description:There is growing interest in the role that life-history traits of hosts, such as their 'pace-of-life', play in the evolution of resistance and tolerance to parasites. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible re-orderings of the three fastest or slowest paced species, and various measurements of tolerance. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.
| S-EPMC4857767 | biostudies-literature
Project description:The evolution of host immunity occurs in the context of the microbiome, but little theory exists to predict how resistance against pathogens might be influenced by the need to tolerate and regulate commensal microbiota. We present a general model to explore the optimal investment in host immunity under conditions in which the host can, versus cannot easily distinguish among commensal versus pathogenic bacteria, and when commensal microbiota can, versus cannot protect the host against the impacts of pathogen infection. We find that a loss of immune vigilance associated with innate immunity over evolutionary time can occur due to the challenge of discriminating between pathogenic and other microbe species. Further, we find the greater the protective effect of microbiome species, acting either directly or via competition with a pathogen, or the higher the costs of immunity, the more likely the loss of immune vigilance is. Conversely, this effect can be reversed when pathogens increase host mortality. Generally, the magnitude of costs of immunity required to allow evolution of decreased immune vigilance are predicted to be lowest when microbiome and pathogen species most resemble each other (in terms of host recognition), and when immune effects on the pathogen are weak. Our model framework makes explicit the core trade-offs likely to shape the evolution of immunity in the context of microbiome/pathogen discrimination. We discuss how this informs interpretation of patterns and process in natural systems, including vulnerability to pathogen emergence.
| S-EPMC6791398 | biostudies-literature
Project description:Impact of host quantitative resistance on pathogen evolution is still poorly documented. In our study, we characterized the adaptation of the pathogenic fungus Colletotrichum gloeosporioides, to the quantitative resistance of its host, the water yam (Dioscorea alata). Genetic and pathogenic diversities of C. gloeosporioides populations were specified at the field scale. We used nuclear markers to describe fungal population structuring within and between six fields of three cultivars differently susceptible to the fungus. Strain aggressiveness was then quantified in the laboratory through cross-inoculation tests. The high level of genetic diversity and significant linkage disequilibrium revealed a significant influence of clonal reproduction in the C. gloeosporioides evolution. The recorded fungal migration between fields was weak (evidence for a dispersion mode via tubers rather than splashing dispersal), which provides the first molecular evidence for limited C. gloeosporioides migration via yam tuber exchanges. C. gloeosporioides's populations are adapted to their host resistance. The aggressiveness of the fungal clones seems to have evolved toward an accumulation of components specific to each host cultivar. Despite the remaining marks of adaptation to the former widely cultivated host, adaptation to current cultivars was clearly depicted.
| S-EPMC6220312 | biostudies-literature
Project description:Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (immune priming), whereby sublethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle (Tribolium castaneum) populations, infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt evolved high basal resistance against multiple Bt strains. By contrast, populations injected only with a high dose of live Bt evolved a less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance versus specific immune memory) with potentially distinct mechanisms.
| S-EPMC5745399 | biostudies-literature
Project description:Spatial interactions are known to promote stability and persistence in enemy-victim interactions if instability and extinction occur in well-mixed settings. We investigate the effect of spatial interactions in the opposite case, where populations can persist in well-mixed systems. A stochastic agent-based model of host-pathogen dynamics is considered that describes nearest-neighbor interactions in an undivided habitat. Contrary to previous notions, we find that in this setting, spatial interactions in fact promote extinction. The reason is that, in contrast to the mass-action system, the outcome of the nearest-neighbor model is governed by dynamics in small "local neighborhoods." This is an abstraction that describes interactions in a minimal grid consisting of an individual plus its nearest neighbors. The small size of this characteristic scale accounts for the higher extinction probabilities. Hence, nearest-neighbor interactions in a continuous habitat lead to outcomes reminiscent of a fragmented habitat, which is underlined further with a metapopulation model that explicitly assumes habitat fragmentation. Beyond host-pathogen dynamics, axiomatic modeling shows that our results hold for generic enemy-victim interactions under specified assumptions. These results are used to interpret a set of published experiments that provide a first step toward model testing and are discussed in the context of the literature.
| S-EPMC4762454 | biostudies-literature