Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem

Abstract Virulence is thought to be a driving force in host–pathogen coevolution. Theoretical models suggest that virulence is an unavoidable consequence of pathogens evolving towards a high rate of intrahost reproduction. These models predict a positive correlation between the reproductive fitness of a pathogen and its level of virulence. Theoretical models also suggest that the demography and genetic structure of a host population can influence the evolution of virulence. If evolution occurs faster in pathogen populations than in host populations, the predicted result is local adaptation of the pathogen population. In our studies, we used a combination of molecular and physiological markers to test these hypotheses in an agricultural system. We isolated five strains of the fungal pathogen Mycosphaerella graminicola from each of two wheat cultivars that differed in their level of resistance to this pathogen. Each of the 10 fungal strains had distinct genotypes as indicated by different DNA fingerprints. These fungal strains were re‐inoculated onto the same two host cultivars in a field experiment and their genotype frequencies were monitored over several generations of asexual reproduction. We also measured the virulence of these 10 fungal strains and correlated it to the reproductive fitness of each fungal strain. We found that host genotypes had a strong impact on the dynamics of the pathogen populations. The pathogen population collected from the moderately resistant cultivar Madsen showed greater stability, higher genotype diversity, and smaller selection coefficients than the pathogen populations collected from the susceptible cultivar Stephens or a mixture of the two host cultivars. The pathogen collection from the mixed host population was midway between the two pure lines for most parameters measured. Our results also revealed that the measures of reproductive fitness and virulence of a pathogen strain were not always correlated. The pathogen strains varied in their patterns of local adaptation, ranging from locally adapted to locally maladapted.     

Sexual Reproduction Plays a Major Role in the Genetic Structure of Populations of the Fungus Mycosphaerella Graminicola

The relative contributions of sexual and asexual reproduction to the genetic structure of populations can be difficult to determine for fungi that use a mixture of both types of propagation. Nuclear RFLPs and DNA fingerprints were used to make indirect and direct measures of departures from random mating in a population of the plant pathogenic fungus Mycosphaerella graminicola during the course of an epidemic cycle. DNA fingerprints resolved 617 different genotypes among 673 isolates sampled from a single field over a 3-month period. Only 7% of the isolates represented asexual clones that were found more than once in the sample. The most common clone was found four times. Genotypic diversity averaged 85% of its maximum possible value during the course of the epidemic. Analyses of multilocus structure showed that allelic distributions among RFLP loci were independent. Pairwise comparisons between individual RFLP loci showed that the majority of alleles at these loci were in gametic equilibrium. Though this fungus has the capacity for a significant level of asexual reproduction, each analysis suggested that M. graminicola populations maintain a genetic structure more consistent with random-mating over the course of an epidemic cycle.     

Alteration of pathogenicity-linked life-history traits by resistance of its host Solanum tuberosum impacts sexual reproduction of the plant pathogenic oomycete Phytophthora infestans

Although sexual reproduction implies a cost, it represents an evolutionary advantage for the adaptation and survival of facultative sexual pathogens. Understanding the maintenance of sex in pathogens requires to analyse how host resistance will impact their sexual reproduction through the alteration of their life-history traits. We explored this experimentally using potato (Solanum tuberosum) and one of its pathogens, the heterothallic oomycete Phytophthora infestans. Sexual reproduction was highest on hosts favouring asexual multiplication of the pathogen, suggesting similar nutritional requirements for both sexual and asexual sporulation. Sexual reproduction was also highest on hosts decreasing the latent period, probably because of a trade-off between growth and reproduction. Distinguishing host effects on each pathogenic trait remains however uneasy, as most life-history traits linked to pathogenicity were not independent of each other. We argue that sexual reproduction of P. infestans is an adaptation to survive when the host is susceptible and rapidly destroyed.     

Exploring the role of asexual multiplication in poplar rust epidemics: impact on diversity and genetic structure

Fungal plant pathogens, especially rust fungi (Pucciniales), are well known for their complex life cycles, which include phases of sexual and asexual reproduction. The effect of asexual multiplication on population genetic diversity has been investigated in the poplar rust fungus Melampsora larici‐populina using a nested hierarchical sampling scheme. Four hierarchical levels were considered: leaf, twig, tree and site. Both cultivated and wild poplar stands were sampled at two time points at the start and end of rust epidemics. A total of 641 fungal isolates was analysed using nine microsatellite markers. This study revealed that the genetic signature of asexual multiplication in the wild poplar stand was seen only at lower hierarchical levels (leaf and twig). Moreover, we observed an erosion of clonal structure through time, with an increase in both gene and genotypic diversity. New genotypes contributed to host infection over time, which demonstrates the importance of allo‐infection in the epidemic process in this host‐pathogen system. Compared with the wild stands, the nearly lack of detection of clonal structure in the cultivated stands reflects the higher infection level on cultivated poplars. More generally, this genetic analysis illustrates the utility of population genetics approach for elucidating the proportion of asexual reproduction in the multiplication of isolates during an epidemic, and for proper quantification of asexual dispersal in plant pathogens.     

Selfing versus outcrossing propensity of the fungal pathogen Microbotryumviolaceum across Silenelatifolia host plants

In the fungal pathogen Microbotryumviolaceum mating (i.e. conjugation between cells of opposite mating type) is indispensable for infection of its host plant Silenelatifolia. Since outcrossing opportunities are potentially rare, selfing may be appropriate to ensure reproduction. On the other hand, outcrossing may create genetic variability necessary in the coevolutionary arms race with its host. We investigated the propensity of M. violaceum to outcross vs. self in different host environments. We used haploid sporidia from each of three strains from five fungal populations for pairwise mixtures of opposite mating type, representing either selfing or outcrossing combinations. Mixtures were exposed to leaf extract from seven S. latifolia plants. The proportion of conjugated sporidia quantified mating propensity. The identity of both fungal strains and host influenced conjugation. First, individual strains differed in conjugation frequency by up to 30%, and strains differed in their performance across the different hosts. Second, selfing combinations produced, on average, more conjugations than did outcrossing combinations. Selfing appears to be the predominant mode of reproduction in this fungus, and selfing preference may have evolved as a mechanism of reproductive assurance. Third, individual strains varied considerably in conjugation frequency in selfing and outcrossing combinations across different hosts. This indicates that conjugation between outcrossing partners could be favoured at least in some hosts. Since the dikaryon resulting from conjugation is the infectious unit, conjugation frequency may correspond with infection probability. This assumption was supported by an inoculation experiment, where high infectious sporidial dosage resulted in higher infections success than did low dosage. We therefore predict that sexual recombination can provide this pathogen with novel genotypes able to infect local resistant hosts.     

Population Processes at Multiple Spatial Scales Maintain Diversity and Adaptation in the Linum marginale - Melampsora lini Association

Host-pathogen coevolution is a major driver of species diversity, with an essential role in the generation and maintenance of genetic variation in host resistance and pathogen infectivity. Little is known about how resistance and infectivity are structured across multiple geographic scales and what eco-evolutionary processes drive these patterns. Across southern Australia, the wild flax Linum marginale is frequently attacked by its rust fungus Melampsora lini. Here, we compare the genetic and phenotypic structure of resistance and infectivity among population pairs from two regions where environmental differences associate with specific life histories and mating systems. We find that both host and pathogen populations are genetically distinct between these regions. The region with outcrossing hosts and pathogens that go through asexual cycles followed by sexual reproduction showed greater diversity of resistance and infectivity phenotypes, higher levels of resistance and less clumped within-population spatial distribution of resistance. However, in the region where asexual pathogens infect selfing hosts, pathogens were more infective and better adapted to sympatric hosts. Our findings largely agree with expectations based on the distinctly different host mating systems in the two regions, with a likely advantage for hosts undergoing recombination. For the pathogen in this system, sexual reproduction may primarily be a survival mechanism in the region where it is observed. While it appears to potentially have adverse effects on local adaptation in the short term, it may be necessary for longer-term coevolution with outcrossing hosts.     

Virulence phenotypes result from interactions between pathogen ploidy and genetic background

Studying fungal virulence is often challenging and frequently depends on many contexts, including host immune status and pathogen genetic background. However, the role of ploidy has often been overlooked when studying virulence in eukaryotic pathogens. Since fungal pathogens, including the human opportunistic pathogen Candida albicans, can display extensive ploidy variation, assessing how ploidy impacts virulence has important clinical relevance. As an opportunistic pathogen, C. albicans causes nonlethal, superficial infections in healthy individuals, but life‐threatening bloodstream infections in individuals with compromised immune function. Here, we determined how both ploidy and genetic background of C. albicans impacts virulence phenotypes in healthy and immunocompromised nematode hosts by characterizing virulence phenotypes in four near‐isogenic diploid and tetraploid pairs of strains, which included both laboratory and clinical genetic backgrounds. We found that C. albicans infections decreased host survival and negatively impacted host reproduction, and we leveraged these two measures to survey both lethal and nonlethal virulence phenotypes across the multiple C. albicans strains. In this study, we found that regardless of pathogen ploidy or genetic background, immunocompromised hosts were susceptible to fungal infection compared to healthy hosts. Furthermore, for each host context, we found a significant interaction between C. albicans genetic background and ploidy on virulence phenotypes, but no global differences between diploid and tetraploid pathogens were observed.     

Genetic variation of geminiviruses: comparison between sexual and asexual host plant populations

One of the most promising hypotheses for the evolution of sex is that sexual reproduction is advantageous because it increases the rate of adaptive evolution in response to parasites. To investigate this advantage of sex, we compared genetic variation of geminiviruses infecting sexual and asexual populations of Eupatorium (Asteraceae). The infection frequency was 37.5% in the sexual population and 87.8% in the asexual population. The lower infection frequency in the sexual population might be the result of higher genetic diversity of host plants. If geminiviruses have diverged to counter defence systems of genetically variable hosts, genetic diversity of viruses is expected to be higher in sexual host populations than in asexual host populations. To test this expectation, we used single-strand conformation polymorphism (SSCP) analysis to examine genetic diversity of the geminiviruses in a DNA region containing the open-reading frame (ORF) C4 gene, which is known to function as a host range determinant. As predicted, higher genetic diversity of viruses was observed in the sexual population: three SSCP types were found in the asexual population while six types were found in the sexual population. Sequencing of the polymerase chain reaction (PCR) products revealed further genetic diversity. Phylogenetic analysis of the sequences showed that the SSCP types belonged to four different clades. Several SSCP types from the same clade were found in the sexual population, whereas the asexual population included only one SSCP type from each clade. Amino acid replacements of ORF C4 are suggested to be accelerated in the sexual population. This evidence supports the hypothesis that sexual reproduction is advantageous as a defence against epidemic disease.     

THE JACK OF ALL TRADES IS MASTER OF NONE: A PATHOGEN'S ABILITY TO INFECT A GREATER NUMBER OF HOST GENOTYPES COMES AT A COST OF DELAYED REPRODUCTION

A trade‐off between a pathogen's ability to infect many hosts and its reproductive capacity on each host genotype is predicted to limit the evolution of an expanded host range, yet few empirical results provide evidence for the magnitude of such trade‐offs. Here, we test the hypothesis for a trade‐off between the number of host genotypes that a fungal pathogen can infect (host genotype range) and its reproductive capacity on susceptible plant hosts. We used strains of the oat crown rust fungus that carried widely varying numbers of virulence (avr) alleles known to determine host genotype range. We quantified total spore production and the expression of four pathogen life‐history stages: infection efficiency, time until reproduction, pustule size, and spore production per pustule. In support of the trade‐off hypothesis, we found that virulence level, the number of avr alleles per pathogen strain, was correlated with significant delays in the onset of reproduction and with smaller pustule sizes. Modeling from our results, we conclude that trade‐offs have the capacity to constrain the evolution of host genotype range in local populations. In contrast, long‐term trends in virulence level suggest that the continued deployment of resistant host lines over wide regions of the United States has generated selection for increased host genotype range.     

Detection of Genetic Variability in Pearl Millet Downy Mildew (Sclerospora graminicola) by AFLP

Downy mildew, caused by Sclerospora graminicola, is an economically important disease of pearl millet in the semiarid regions of Asia and Africa. Amplified restriction fragment length polymorphism (AFLP) was used to detect the extent of genomic variation among 19 fungal isolates from different cultivars of pearl millet grown in various regions of India. Fourteen AFLP primer combinations produced 184 polymorphic bands. An unweighted pair-group method of averages cluster analysis represented by dendrogram and principal coordinate analysis separated the mildew collections into four distinct groups. Isolates having characteristic opposite mating abilities, geographic relatedness, virulence, common host cultivars, and changes through asexual generations reflected heterogeneity of the pathogen. The use of AFLP to detect genetic variation is particularly important in selecting mildew isolates to screen breeding material for identification of resistant millet and monitoring changes in S. graminicola in relation to changes in host for effective disease management.     

Phenotypic and genetic analysis of the Triticum monococcum-Mycosphaerella graminicola interaction

Here, the aim was to understand the cellular and genetic basis of the Triticum monococcum-Mycosphaerella graminicola interaction. Testing for 5 yr under UK field conditions revealed that all 24 T. monococcum accessions exposed to a high level of natural inocula were fully resistant to M. graminicola. When the accessions were individually inoculated in the glasshouse using an attached leaf seeding assay and nine previously characterized M. graminicola isolates, fungal sporulation was observed in only three of the 216 interactions examined. Microscopic analyses revealed that M. graminicola infection was arrested at four different stages post-stomatal entry. When the inoculated leaves were detached 30 d post inoculation and incubated at 100% humidity, abundant asexual sporulation occurred within 5 d in a further 61 interactions. An F(2) mapping population generated from a cross between T. monococcum accession MDR002 (susceptible) and MDR043 (resistant) was inoculated with the M. graminicola isolate IPO323. Both resistance and in planta fungal growth were found to be controlled by a single genetic locus designated as TmStb1 which was linked to the microsatellite locus Xbarc174 on chromosome 7A(m). Exploitation of T. monococcum may provide new sources of resistance to septoria tritici blotch disease.     

The maintenance of sex in parasites

The maintenance of sex is an unresolved paradox in evolutionary biology, given the inherent twofold fitness advantage for asexuals. Parasitic helminths offer a unique opportunity to address this enigma. Parasites that can create novel antigenic strains are able to escape pre-existing host immunity. Viruses produce diversity through mutation with rapid clonal proliferation. The long generation times of helminth parasites prevent them from adopting this strategy. Instead, we argue that sexual reproduction enables parasitic helminths to rapidly generate strain diversity. We use both a stochastic, individual-based model and a simple analytical model to assess the selective value of sexual versus asexual reproduction in helminth parasites. We demonstrate that sexual reproduction can more easily produce and maintain strain diversity than asexual reproduction for long-lived parasites. We also show that sexual parasite populations are resistant to invasion by rare asexual mutants. These results are robust to high levels of cross-immunity between strains. We suggest that the enhancement of strain diversity, despite stochastic extinction of strains, may be critical to the evolutionary success of sex in long-lived parasites.     

The Ratchet and the Red Queen: the maintenance of sex in parasites

The adaptive significance of sexual reproduction remains as an unsolved problem in evolutionary biology. One promising hypothesis is that frequency‐dependent selection by parasites selects for sexual reproduction in hosts, but it is unclear whether such selection on hosts would feed back to select for sexual reproduction in parasites. Here we used individual‐based computer simulations to explore this possibility. Specifically, we tracked the dynamics of asexual parasites following their introduction into sexual parasite populations for different combinations of parasite virulence and transmission. Our results suggest that coevolutionary interactions with hosts would generally lead to a stable coexistence between sexual parasites and a single parasite clone. However, if multiple mutations to asexual reproduction were allowed, we found that the interaction led to the accumulation of clonal diversity in the asexual parasite population, which led to the eventual extinction of the sexual parasites. Thus, coevolution with sexual hosts may not be generally sufficient to select for sex in parasites. We then allowed for the stochastic accumulation of mutations in the finite parasite populations (Muller's Ratchet). We found that, for higher levels of parasite virulence and transmission, the population bottlenecks resulting from host–parasite coevolution led to the rapid accumulation of mutations in the clonal parasites and their elimination from the population. This result may explain the observation that sexual reproduction is more common in parasitic animals than in their free‐living relatives.     

Local genetic structure in a North American epiphytic lichen, Ramalina menziesii (Ramalinaceae)

Epiphytic lichens possess unique life history traits that can have conflicting effects on genetic structure: symbiotic mutualism between a fungus with its algal or cyanobacterial photobiont, association with a host plant, and ability to reproduce sexually and asexually. Our study species, Ramalina menziesii, has small ascospores that can facilitate long-distance gene movement, and it is capable of clonal reproduction. The goals of this study are to test whether different haplotypes were differentially distributed across host plant species, to look for evidence of asexual vs. sexual reproduction, and to assess the local genetic structure of the population. We sampled individuals from multiple trees of three oak species in four lichen subpopulations within a savanna ecosystem. Using DNA sequence data from four fungal nuclear loci, we found no tendency for host specialization. Alleles were randomly distributed across subpopulations. The frequency of multilocus genotypes was consistent with a randomly mating population. Sexual reproduction involving relichenization appeared to be the predominant mode of reproduction of R. menziesii at this study site. We found no significant local genetic structure suggesting widespread gene flow at the local scale. The genetic structure of this lichen is comparable to that of widely distributed epiphytic plants.     

Population genetics of complex life-cycle parasites: an illustration with trematodes

Accurate inferences on population genetics data require a sound underlying theoretical null model. Organisms alternating sexual and asexual reproduction during their life-cycle have been largely neglected in theoretical population genetic models, thus limiting the biological interpretation of population genetics parameters measured in natural populations. In this article, we derive the expectations of those parameters for the life-cycle of monoecious trematodes, a group comprising several important human and livestock parasites that obligatorily alternate sexual and asexual reproduction during their life-cycle. We model how migration rates between hosts, sexual and asexual mutation rates, adult selfing rate and the variance in reproductive success of parasites during the clonal phase affect the amount of neutral genetic diversity of the parasite (effective population size) and its apportionment within and between definitive hosts (using F-statistics). We demonstrate, in particular, that variance in reproductive success of clones, a parameter that has been completely overlooked in previous population genetics models, is very important in shaping the distribution of the genetic variability both within and among definitive hosts. Within definitive hosts, the parameter F(IS) (a measure of the deviation from random mating) is decreased by high variance in clonal reproductive success of larvae but increased by high adult self-fertilisation rates. Both clonal multiplication and selfing have similar effects on between-host genetic differentiation (F(ST)). Migration occurring before and after asexual reproduction can have different effects on the patterns of F(IS), depending on values of the other parameters such as the mutation rate. While the model applies to any hermaphroditic organism alternating sexual and clonal reproduction (e.g. many plants), the results are specifically discussed in the light of the limited population genetic data on monoecious trematodes available to date and their previous interpretation. We hope that our model will encourage more empirical population genetics studies on monoecious trematodes and other organisms with similar life-cycles.     

Costs of resistance and infection by a generalist pathogen

Pathogen infection is typically costly to hosts, resulting in reduced fitness. However, pathogen exposure may also come at a cost even if the host does not become infected. These fitness reductions, referred to as “resistance costs”, are inducible physiological costs expressed as a result of a trade‐off between resistance to a pathogen and aspects of host fitness (e.g., reproduction). Here, we examine resistance and infection costs of a generalist fungal pathogen (Metschnikowia bicuspidata) capable of infecting a number of host species. Costs were quantified as reductions in host lifespan, total reproduction, and mean clutch size as a function of pathogen exposure (resistance cost) or infection (infection cost). We provide empirical support for infection costs and modest support for resistance costs for five Daphnia host species. Specifically, only one host species examined incurred a significant cost of resistance. This species was the least susceptible to infection, suggesting the possibility that host susceptibility to infection is associated with the detectability and size of resistance cost. Host age at the time of pathogen exposure did not influence the magnitude of resistance or infection cost. Lastly, resistant hosts had fitness values intermediate between unexposed control hosts and infected hosts. Although not statistically significant, this could suggest that pathogen exposure does come at some marginal cost. Taken together, our findings suggest that infection is costly, resistance costs may simply be difficult to detect, and the magnitude of resistance cost may vary among host species as a result of host life history or susceptibility.     

Microsatellite and single‐nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite

Assessing the mode of reproduction of microparasites remains a difficult task because direct evidence for sexual processes is often absent and the biological covariates of sex and asex are poorly known. Species with geographically divergent modes of reproduction offer the possibility to explore some of these covariates, for example, the influence of life‐history traits, mode of transmission and life‐cycle complexity. Here, we present a phylogeographical study of a microsporidian parasite, which allows us to relate population genetic structure and mode of reproduction to its geographically diverged life histories. We show that in microsporidians from the genus Hamiltosporidium, that use the cladoceran Daphnia as host, an epidemic population structure has evolved, most probably since the last Ice Age. We partially sequenced three housekeeping genes (alpha tubulin, beta tubulin and hsp70) and genotyped seven microsatellite loci in 51 Hamiltosporidium isolates sampled within Europe and the Middle East. We found two phylogenetically related asexual parasite lines, one each from Fennoscandia and Israel, which share the unique ability of being transmitted both vertically and horizontally from Daphnia to Daphnia. The sexual forms cannot transmit horizontally among Daphnia, but presumably have a complex life cycle with a second host species. In spite of the similarities between the two asexual lineages, a clustering analysis based on microsatellite polymorphisms shows that asexual Fennoscandian parasites do not share ancestry with any other Hamiltosporidium that we have sampled. Moreover, allele sequence divergence at the hsp70 locus is twice as large in Fennoscandian than in Israeli parasites. Our results indicate that asexual reproduction evolved twice independently, first in Fennoscandian and more recently in the Israeli parasites. We conclude that the independent origin of asexuality in these two populations is associated with the altered parasite mode of transmission and the underlying dynamics of host populations.     

Both mating types of the wheat pathogen Mycosphaerella graminicola are present in Morocco

Septoria tritici blotch caused by the heterothallic ascomycete Mycosphaerella graminicola is one of the most currently damaging diseases on wheat crops worldwide. So far, no information was reported about the status of sexual reproduction of this pathogen under Moroccan conditions. We investigated here for the first time the occurrence of the two mating types (MAT1-1 and MAT1-2) of M. graminicola in Morocco by sampling 141 single-conidial isolates from 4 important wheat producing regions (Gharb, Sa?s, Chaouia and Tadla). The mating type of each isolate was determined by amplification with multiplex PCR of a partial sequence from the corresponding idiomorph. Overall, 43% out of the assessed isolates were MAT1-1 and 57 % were MAT1-2. Both mating types were identified within the 3 sampled regions Gharb, Sa?s and Chaouia, but not in Tadla, where only MAT1-2 isolates were found. The presence of the two mating types highlighted here offers a suitable genetic condition for M. graminicola to occur sexual reproduction in Morocco. The potential of sexual recombination will be examined by the study of mating type frequencies using a large sample size as well as by searching and quantification of pseudothecia in the field.     

Pyrenophora teres: Population structure,virulence and aggressiveness in Southern Russia

The barley net blotch agent Pyrenophora teres (Died) Drechs. is one of the dominant fungal pathogens in agricultural crops worldwide. Here we aim to study the aggressiveness and virulence of P. teres populations collected at different ontogenesis stages (BBCH 30 and BBCH 47) from winter barley cultivars of various resistance types: moderately resistant, moderately susceptible and highly susceptible. We observed a direct proportional relationship between cultivar resistance and the aggressiveness of P. teres populations collected in both growth phases of the host plant. The isolates collected at an early stage of host plant development have a large difference in aggressiveness criteria: colony growth rate, sporulation intensity, latency period, plant damage degree, and the number of identified races. At the BBCH 30 growth stage, the growth rate of fungus colonies selected from a resistant cultivar is 1.2 times higher than that of a susceptible cultivar. The growth rate of colonies selected from resistant and susceptible cultivars in the earlier BBCH 30 stage is 1.04 times higher than the growth rate of colonies selected from the later phase. The sporulation intensity of fungal populations selected from a resistant cultivar is higher than that of populations selected from a susceptible cultivar (for BBCH 30–5.4 times, for BBCH 47–4.0 times); and it is 1.3 times higher in an earlier phase of plant development. Correlation between colony growth rate and spore formation rate in the BBCH 30 is r = 0.4. A high correlation level (r = 0.9) and notable difference between the variants were revealed when studying the duration of the latent period. The average value of plant damage by the P. teres from resistant cultivar is 4 times higher than from the susceptible cultivar in the BBCH 30 stage; and 12 times – in the BBCH 47 stage. There is a moderate negative correlation between the plant damage degree and the number of races identified from the fungal population, r = ?0.59 for the BBCH 30, r = ?0.8 for the BBCH 47. The number of races identified from P. teres populations collected in the late phase of plant growth was one third less. Our study helped to acquire new knowledge about intrapopulation processes under the influence of various factors – plant growth stage and cultivar genotype. The results obtained are the basis for the development of adaptive-integrated techniques for managing populations of the hemibiotrophic pathogen, barley net blotch.     

Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction

The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale-Melampsora lini plant-pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross-inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host-pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.