Most pathogens are generalists capable of infecting multiple host species or strains. Trade‐offs in performance among different hosts are expected to limit the evolution of generalism. Despite the ...commonness of generalism, the variation in infectivity, transmission, and trade‐offs in performance among host species have rarely been studied in the wild. To understand the ecological and evolutionary drivers of multi‐host pathogen infectivity and transmission potential, I studied disease severity, transmission dynamics, and infectivity variation of downy mildew pathogen Peronospora sparsa on its three host plants Rubus arcticus, R. chamaemorus, and R. saxatilis. In a survey of 20 wild and cultivated sites of the three host species, disease severity varied by host species and by host population size but not among wild and cultivated sites. To understand how alternative host presence and plant diversity affect transmission of the pathogen, I conducted a transmission experiment. In this experiment, alternative host abundance and plant diversity together modified P. sparsa transmission to trap plants. To understand how resistance to P. sparsa varies among host species and genotypes, I conducted an inoculation experiment using 10 P. sparsa strains from different locations and 20 genotypes of the three host species. Significant variation in infectivity was found among host genotypes but not among host species. When trade‐offs for infectivity were tested, high infectivity in one host species correlated with high infectivity in another host species. However, when pathogen transmission‐related life‐history correlations were tested, a positive correlation was found in R. arcticus but not in R. saxatilis. The results suggest that host resistance may shape pathogen life‐history evolution with epidemiological consequences in a multi‐host pathogen.
Infection by multiple pathogens of the same host is ubiquitous in both natural and managed habitats. While intraspecific variation in disease resistance is known to affect pathogen occurrence, how ...differences among host genotypes affect the assembly of pathogen communities remains untested. In our experiment using cloned replicates of naive Plantago lanceolata plants as sentinels during a seasonal virus epidemic, we find non-random co-occurrence patterns of five focal viruses. Using joint species distribution modelling, we attribute the non-random virus occurrence patterns primarily to differences among host genotypes and local population context. Our results show that intraspecific variation among host genotypes may play a large, previously unquantified role in pathogen community structure.
Summary
Human alteration of natural habitats may change the processes governing species interactions in wild communities. Wild populations are increasingly impacted by agricultural intensification, ...yet it is unknown whether this alters biodiversity mediation of disease dynamics.
We investigated the association between plant diversity (species richness, diversity) and infection risk (virus richness, prevalence) in populations of Plantago lanceolata in natural landscapes as well as those occurring at the edges of cultivated fields. Altogether, 27 P. lanceolata populations were surveyed for population characteristics and sampled for PCR detection of five recently characterized viruses.
We find that plant species richness and diversity correlated negatively with virus infection prevalence. Virus species richness declined with increasing plant diversity and richness in natural populations while in agricultural edge populations species richness was moderately higher, and not associated with plant richness. This difference was not explained by changes in host richness between these two habitats, suggesting potential pathogen spill‐over and increased transmission of viruses across the agro‐ecological interface. Host population connectivity significantly decreased virus infection prevalence.
We conclude that human use of landscapes may change the ecological laws by which natural communities are formed with far reaching implications for ecosystem functioning and disease.
See also the Commentary on this article by Lacroix, 230: 2094–2096.
Ecological theory predicts that disease incidence increases with increasing density of host networks, yet evolutionary theory suggests that host resistance increases accordingly. To test the combined ...effects of ecological and evolutionary forces on host-pathogen systems, we analyzed the spatiotemporal dynamics of a plant (Plantago Ianceolata)–fungal pathogen (Podosphaera plantaginis) relationship for 12 years in over 4000 host populations. Disease prevalence at the metapopulation level was low, with high annual pathogen extinction rates balanced by frequent (re-)colonizations. Highly connected host populations experienced less pathogen colonization and higher pathogen extinction rates than expected; a laboratory assay confirmed that this phenomenon was caused by higher levels of disease resistance in highly connected host populations.
Wild plant populations may harbour a myriad of unknown viruses. As the majority of research efforts have targeted economically important plant species, the diversity and prevalence of viruses in the ...wild has remained largely unknown. However, the recent shift towards metagenomics-based sequencing methodologies, especially those targeting small RNAs, is finally enabling virus discovery from wild hosts. Understanding this diversity of potentially pathogenic microbes in the wild can offer insights into the components of natural biodiversity that promotes long-term coexistence between hosts and parasites in nature, and help predict when and where risks of disease emergence are highest. Here, we used small RNA deep sequencing to identify viruses in
populations, and to understand the variation in their prevalence and distribution across the Åland Islands, South-West Finland. By subsequent design of PCR primers, we screened the five most common viruses from two sets of
plants: 164 plants collected from 12 populations irrespective of symptoms, and 90 plants collected from five populations showing conspicuous viral symptoms. In addition to the previously reported species
(PlLV), we found four potentially novel virus species belonging to
and
genera. Our results show that virus prevalence and diversity varied among the sampled host populations. In six of the virus infected populations only a single virus species was detected, while five of the populations supported between two to five of the studied virus species. In 20% of the infected plants, viruses occurred as coinfections. When the relationship between conspicuous viral symptoms and virus infection was investigated, we found that plants showing symptoms were usually infected (84%), but virus infections were also detected from asymptomatic plants (44%). Jointly, these results reveal a diverse virus community with newly developed tools and protocols that offer exciting opportunities for future studies on the eco-evolutionary dynamics of viruses infecting plants in the wild.
A priority for research on infectious disease is to understand how epidemiological and evolutionary processes interact to influence pathogen population dynamics and disease outcomes. However, little ...is understood about how population adaptation changes across time, how sexual vs. asexual reproduction contribute to the spread of pathogens in wild populations and how diversity measured with neutral and selectively important markers correlates across years. Here, we report results from a long-term study of epidemiological and genetic dynamics within several natural populations of the Linum marginale-Melampsora lini plant-pathogen interaction. Using pathogen isolates collected from three populations of wild flax (L. marginale) spanning 16 annual epidemics, we probe links between pathogen population dynamics, phenotypic variation for infectivity and genomic polymorphism. Pathogen genotyping was performed using 1567 genome-wide SNP loci and sequence data from two infectivity loci (AvrP123, AvrP4). Pathogen isolates were phenotyped for infectivity using a differential set. Patterns of epidemic development were assessed by conducting surveys of infection prevalence in one population (Kiandra) annually. Bayesian clustering analyses revealed host population and ecotype as key predictors of pathogen genetic structure. Despite strong fluctuations in pathogen population size and severe annual bottlenecks, analysis of molecular variance revealed that pathogen population differentiation was relatively stable over time. Annually, varying levels of clonal spread (0-44.8%) contributed to epidemics. However, within populations, temporal genetic composition was dynamic with rapid turnover of pathogen genotypes, despite the dominance of only four infectivity phenotypes across the entire study period. Furthermore, in the presence of strong fluctuations in population size and migration, spatial selection may maintain pathogen populations that, despite being phenotypically stable, are genetically highly dynamic.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Maternal effects of pathogen infection on progeny development and disease resistance may be adaptive and have important consequences for population dynamics. However, these effects are often ...context‐dependent and examples of adaptive transgenerational responses from perennials are scarce, although they may be a particularly important mechanism generating variation in the offspring of long‐lived species.
Here, we studied the effect of maternal infection of Plantago lanceolata by Podosphaera plantaginis, a fungal parasite, on the growth, flower production and resistance of the progeny of six maternal genotypes in nutrient‐rich and nutrient‐poor environments. For this purpose, we combined a common garden study with automated phenotyping measurements of early life stages, and an inoculation experiment.
Our results show that the effects of infection on the mother plants transcend to impact their progeny. Although maternal infection decreased total leaf and flower production of the progeny by the end of the growing season, it accelerated early growth and enhanced resistance to the pathogen P. plantaginis.
We also discovered that the effects of maternal infection affected progeny development and resistance through a three way‐interaction between maternal genotype, maternal infection status and nutrient availability.
Synthesis. Our results emphasize the importance of maternal effects mediated through genotypic and environmental factors in long‐living perennials and suggest that maternal infection can create a layer of phenotypic diversity in resistance. These results may have important implications for both epidemiological and evolutionary dynamics of host–parasite interactions in the wild.
Maternal effects are often context dependent and examples of adaptive transgenerational responses from perennials are scarce. We combined a common garden study, automated phenotyping measurements and an inoculation experiment to study the effect of maternal infection of Plantago lanceolata by Podosphaera plantaginis. Our results emphasize the importance of maternal effects mediated through genotypic and environmental factors in long living perennials and suggest that maternal infection can create a layer of phenotypic diversity in resistance.
Molecular tools may greatly improve our understanding of pathogen evolution and epidemiology but technical constraints have hindered the development of genetic resources for parasites compared to ...free-living organisms. This study aims at developing molecular tools for Podosphaera plantaginis, an obligate fungal pathogen of Plantago lanceolata. This interaction has been intensively studied in the Åland archipelago of Finland with epidemiological data collected from over 4,000 host populations annually since year 2001.
A cDNA library of a pooled sample of fungal conidia was sequenced on the 454 GS-FLX platform. Over 549,411 reads were obtained and annotated into 45,245 contigs. Annotation data was acquired for 65.2% of the assembled sequences. The transcriptome assembly was screened for SNP loci, as well as for functionally important genes (mating-type genes and potential effector proteins). A genotyping assay of 27 SNP loci was designed and tested on 380 infected leaf samples from 80 populations within the Åland archipelago. With this panel we identified 85 multilocus genotypes (MLG) with uneven frequencies across the pathogen metapopulation. Approximately half of the sampled populations contain polymorphism. Our genotyping protocol revealed mixed-genotype infection within a single host leaf to be common. Mixed infection has been proposed as one of the main drivers of pathogen evolution, and hence may be an important process in this pathosystem.
The developed SNP panel offers exciting research perspectives for future studies in this well-characterized pathosystem. Also, the transcriptome provides an invaluable novel genomic resource for powdery mildews, which cause significant yield losses on commercially important crops annually. Furthermore, the features that render genetic studies in this system a challenge are shared with the majority of obligate parasitic species, and hence our results provide methodological insights from SNP calling to field sampling protocols for a wide range of biological systems.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The trade‐off between within‐host infection rate and transmission to new hosts is predicted to constrain pathogen evolution, and to maintain polymorphism in pathogen populations. Pathogen ...life‐history stages and their correlations that underpin infection development may change under coinfection with other parasites as they compete for the same limited host resources. Cross‐kingdom interactions are common among pathogens in both natural and cultivated systems, yet their impacts on disease ecology and evolution are rarely studied. The host plant Plantago lanceolata is naturally infected by both Phomopsis subordinaria, a seed killing fungus, as well as Plantago lanceolata latent virus (PlLV) in the Åland Islands, SW Finland. We performed an inoculation assay to test whether coinfection with PlLV affects performance of two P. subordinaria strains, and the correlation between within‐host infection rate and transmission potential. The strains differed in the measured life‐history traits and their correlations. Moreover, we found that under virus coinfection, within‐host infection rate of P. subordinaria was smaller but transmission potential was higher compared to strains under single infection. The negative correlation between within‐host infection rate and transmission potential detected under single infection became positive under coinfection with PlLV. To understand whether within‐host and between‐host dynamics are correlated in wild populations, we surveyed 260 natural populations of P. lanceolata for P. subordinaria infection occurrence. When infections were found, we estimated between‐hosts dynamics by determining pathogen population size as the proportion of infected individuals, and within‐host dynamics by counting the proportion of infected flower stalks in 10 infected plants. In wild populations, the proportion of infected flower stalks was positively associated with pathogen population size. Jointly, our results suggest that the trade‐off between within‐host infection load and transmission may be strain specific, and that the pathogen life‐history that underpin epidemics may change depending on the diversity of infection, generating variation in disease dynamics.
We found that under virus coinfection, within‐host infection load of Phomopsis subordinaria was lower but transmission potential was higher compared to strains under single infection. The negative correlation between within‐host infection load and transmission potential detected under single infection became positive under coinfection with virus. In wild populations, within‐host infection load was positively associated with within‐population disease prevalence.
Recent methodological advances have uncovered tremendous microbial diversity cohabiting in the same host plant, and many of these microbes cause disease. In this review we highlight how the presence ...of other pathogen species, or other pathogen genotypes, within a plant can affect key components of host–pathogen interactions: (i) within-plant virulence and pathogen accumulation, through direct and host-mediated mechanisms; (ii) evolutionary trajectories of pathogen populations, through virulence evolution, generation of novel genetic combinations, and maintenance of genetic diversity; and (iii) disease dynamics, with multiple infection likely to render epidemics more devastating. The major future challenges are to couple a community ecology approach with a molecular investigation of the mechanisms operating under coinfection and to evaluate the evolution and effectiveness of resistance within a coinfection framework.
Molecular tools are becoming readily available for the study of parasites. These technical advances have shown that multiple infection is common in the wild and in agriculture, with the same host individual simultaneously infected by several pathogen genotypes or species (i.e., coinfection).
Under coinfection, pathogens may interact either directly (mechanical or chemical interactions) or indirectly through host resources or defenses.
These direct or host-mediated interactions under coinfection can change virulence, within-host pathogen accumulation, and transmission.
Such plant-level effects can also be seen at the population level, with coinfection rendering epidemics more devastating.
Coinfection may drive the evolutionary trajectories of pathogen populations through its effects on virulence evolution and on the generation and maintenance of genetic diversity in pathogen populations.
PDF
