Ecological and evolutionary implications of spatial heterogeneity during the off-season for a wild plant pathogen

•While recent studies have elucidated many of the factors driving parasite dynamics during the growing season, the ecological and evolutionary dynamics during the off-season (i.e. the period between growing seasons) remain largely unexplored. •We combine large-scale surveys and detailed experiments to investigate the overwintering success of the specialist plant pathogen Podosphaera plantaginis on its patchily distributed host plant Plantago lanceolata on the Åland Islands. •Twelve years of epidemiological data establish the off-season as a crucial stage in pathogen metapopulation dynamics, with approximately forty percent of the populations going extinct during the off-season. At the end of the growing season, we observed environmentally-mediated variation in the production of resting structures, with major consequences for spring infection at spatial scales ranging from single individuals to populations within a metapopulation. Reciprocal transplant experiments further demonstrated that pathogen population of origin and overwintering site jointly shaped infection intensity in spring, with a weak signal of parasite adaptation to the local off-season environment. •We conclude that environmentally-mediated changes in the distribution and evolution of parasites during the off-season are crucial for our understanding of host-parasite dynamics, with applied implications for combating parasites and diseases in agriculture, wildlife and human disease systems.Peer reviewe

The impact of spatial scale and habitat configuration on patterns of trait variation and local adaptation in a wild plant parasite

Peer reviewe

Herbivory in a changing climate-Effects of plant genotype and experimentally induced variation in plant phenology on two summer-active lepidopteran herbivores and one fungal pathogen

With climate change, spring warming tends to advance plant leaf-out. While the timing of leaf-out has been shown to affect the quality of leaves for herbivores in spring, it is unclear whether such effects extend to herbivores active in summer. In this study, we first examined how spring and autumn phenology of seven Quercus robur genotypes responded to elevated temperatures in spring. We then tested whether the performance of two summer-active insect herbivores (Orthosia gothica and Polia nebulosa) and infection by a pathogen (Erysiphe alphitoides) were influenced by plant phenology, traits associated with genotype or the interaction between these two. Warm spring temperatures advanced both bud development and leaf senescence in Q. robur. Plants of different genotype differed in terms of both spring and autumn phenology. Plant phenology did not influence the performance of two insect herbivores and a pathogen, while traits associated with oak genotype had an effect on herbivore performance. Weight gain for O. gothica and ingestion for P. nebulosa differed by a factor of 4.38 and 2.23 among genotypes, respectively. Herbivore species active in summer were influenced by traits associated with plant genotype but not by phenology. This suggest that plant attackers active in summer may prove tolerant to shifts in host plant phenology-a pattern contrasting with previously documented effects on plant attackers active in spring and autumn

Different spatial structure of plant-associated fungal communities above- and belowground

The distribution and community assembly of above- and belowground microbial communities associated with individual plants remain poorly understood, despite its consequences for plant-microbe interactions and plant health. Depending on how microbial communities are structured, we can expect different effects of the microbial community on the health of individual plants and on ecosystem processes. Importantly, the relative role of different factors will likely differ with the scale examined. Here, we address the driving factors at a landscape level, where each individual unit (oak trees) is accessible to a joint species pool. This allowed to quantify the relative effect of environmental factors and dispersal on the distribution of two types of fungal communities: those associated with the leaves and those associated with the soil of Quercus robur trees in a landscape in southwestern Finland. Within each community type, we compared the role of microclimatic, phenological, and spatial variables, and across community types, we examined the degree of association between the respective communities. Most of the variation in the foliar fungal community was found within trees, whereas soil fungal community composition showed positive spatial autocorrelation up to 50 m. Microclimate, tree phenology, and tree spatial connectivity explained little variation in the foliar and soil fungal communities. Foliar and soil fungal communities differed strongly in community structure, with no significant concordance detected between them. We provide evidence that foliar and soil fungal communities assemble independent of each other and are structured by different ecological processes

Genetic diversity and connectivity shape herbivore load within an oak population at its range limit

Host genetic diversity and genotypic identity have been reported to affect the abundance, species richness and species diversity of associated herbivore communities. Recent work, however, suggests that these effects are highly context-dependent and that the magnitude and direction of the effects may vary with e.g., spatial factors and the amount of genetic variation present in the host population. Here, we use observational data on a Finnish oak (Quercus robur) population to examine whether low genetic diversity within peripheral populations reduces the impact of host genotype on associated herbivore communities. We first compared measures of genetic variation within Finnish oak populations with those recorded in more central parts of the species' range, confirming that genetic variation within the Finnish populations is comparatively low. Despite this result, we found consistent imprints of host genetic diversity on herbivore communities: herbivore load, but not the species richness, increased with host genetic diversity in both years and both spatial scales examined. Spatial connectivity of hosts increased herbivore diversity as well as abundance. While the similarity of herbivore communities increased with the genetic similarity among hosts, the effect of geographic distance was stronger. Overall, our findings identify a major role for spatial context in structuring oak-associated herbivore communities-but we still trace detectable imprints of host genotype at multiple spatial scales even in this peripheral, genetically impoverished oak population.Peer reviewe

Community phenology of insects on oak:Local differentiation along a climatic gradient

Climate change is advancing the onset of phenological events, with the rate of advance varying among species and trophic levels. In addition, local populations of the same species may show genetic differences in their response to seasonal cues. If populations of interacting species differ in their response, then climate change may result in geographically varying shifts in the community-level distribution of interaction strength. We explored the magnitude of trophic- and species-level responses to temperature in a tritrophic system comprising pedunculate oak, insect herbivores, and their associated parasitoids. We sampled local realizations of this community at five sites along a transect spanning fifteen degrees of latitude. Samples from each trophic level at each site were exposed to the same set of five climatic regimes during overwintering in climate chambers. We then recorded the number of days and degree-days required for oak acorns to develop and insects to emerge. In terms of dates of events, phenology differed among populations. In terms of degree-days, we found that for two species pairs, the heat sum required to develop in spring differed by an additional similar to 500 degree-days between trophic levels when overwintering at the highest temperature. For three species, within-population variation in the number of degree-days required for emergence was higher at warmer temperatures. Our findings suggest that changing temperatures can modify interactions within a community by altering the relative phenology of interacting species and that some interactions are more vulnerable than others to a shift in temperature. The geographic variation in the phenological response of a species suggests that there is a genetic component in determining the phenology of local populations. Such local variation blended with interspecific differences in responses makes it complex to understand how communities will respond to warmer temperatures

Niche differentiation within a cryptic pathogen complex: climatic drivers and hyperparasitism at multiple spatial scales

Pathogens are embedded in multi-trophic food webs, which often include co-occurring cryptic species within the same pathogen complex. Nonetheless, we still lack an understanding of what dimensions of the ecological niche might allow these cryptic species to coexist. We explored the role of climate, host characteristics (tree autumn phenology) and attack by the fungal hyperparasite Ampelomyces (a group of fungi attacking plant pathogens) in defining the niches of three powdery mildew species (Erysiphe alphitoides, E. hypophylla and E. quercicola) within a cryptic pathogen complex on the pedunculate oak Quercus robur at the continental (Europe), national (Sweden and France) and landscape scales (a 5 km(2) island in southwestern Finland). Previous studies have shown that climate separated the niches of three powdery mildew species (E. alphitoides, E. hypophylla and E. quercicola) in Europe and two species (E. alphitoides and E. quercicola) in France. In our study, we did not detect a significant relationship between temperature or precipitation and the distribution of E. alphitoides and E. hypophylla present in Sweden, while at the landscape scale, temperature, but not relative humidity, negatively affected disease incidence of E. alphitoides in an exceptionally warm year. Tree variation in autumn phenology did not influence disease incidence of powdery mildew species, and hyperparasite presence did not differ among powdery mildew species at the continental, national and landscape scale. Climate did not affect the distribution of the hyperparasite at the continental scale and at the national scale in Sweden. However, climate affected the hyperparasite distribution in France, with a negative relationship between non-growing season temperature and presence of the hyperparasite. Overall, our findings, in combination with earlier evidence, suggest that climatic factors are more important than species interactions in defining the niches of cryptic species within a pathogen complex on oak

Relationships between the Pathogen Erysiphe alphitoides, the Phytophagous Mite Schizotetranychus garmani (Acari: Tetranychidae) and the Predatory Mite Euseius finlandicus (Acari: Phytoseiidae) in Oak

Food webs on forest trees include plant pathogens, arthropods, and their natural ene-mies. To increase the understanding of the impact of a plant pathogen on herbivore-natural enemy interactions, we studied the powdery mildew fungus Erysiphe alphitoides, the phytophagous mite Schizotetranychus garmani, and the predatory and mycophagous mite Euseius finlandicus in peduncu-late oak (Quercus robur) leaves. In June, July and August of 2016, we assessed the severity of powdery mildew, mite population density and adult female mite size in 30 trees in three forests near Belgrade, Serbia. In August, the infection severity of E. alphitoides related positively to the population density of S. garmani and negatively to the body size of S. garmani females. Throughout the vegetative season, the infection severity of E. alphitoides related positively to the population density of E. finlandicus but not to its body size. The effect of E. alphitoides on the population density and adult size of S. gar-mani was not mediated by the population density of E. finlandicus, and vice versa. Interactions were consistent in all forests and varied with the summer month. Our findings indicate that E. alphitoides can influence the average body size and population densities of prey and predatory mites studied, irrespective of predator-prey relationships

Elevation and plant species identity jointly shape a diverse arbuscular mycorrhizal fungal community in the High Arctic

Knowledge about the distribution and local diversity patterns of arbuscular mycorrhizal (AM) fungi are limited for extreme environments such as the Arctic, where most studies have focused on spore morphology or root colonization. We here studied the joint effects of plant species identity and elevation on AM fungal distribution and diversity. We sampled roots of 19 plant species in 18 locations in Northeast Greenland, using next generation sequencing to identify AM fungi. We studied the joint effect of plant species, elevation and selected abiotic conditions on AM fungal presence, richness and composition. We identified 29 AM fungal virtual taxa (VT), of which six represent putatively new VT. Arbuscular mycorrhizal fungal presence increased with elevation, and as vegetation cover and the active soil layer decreased. Arbuscular mycorrhizal fungal composition was shaped jointly by elevation and plant species identity. We demonstrate that the Arctic harbours a relatively species-rich and nonrandomly distributed diversity of AM fungi. Given the high diversity and general lack of knowledge exposed herein, we encourage further research into the diversity, drivers and functional role of AM fungi in the Arctic. Such insight is urgently needed for an area with some of the globally highest rates of climate change.Peer reviewe

Elevation and plant species identity jointly shape a diverse arbuscular mycorrhizal fungal community in the High Arctic

Knowledge about the distribution and local diversity patterns of arbuscular mycorrhizal (AM) fungi are limited for extreme environments such as the Arctic, where most studies have focused on spore morphology or root colonization. We here studied the joint effects of plant species identity and elevation on AM fungal distribution and diversity. We sampled roots of 19 plant species in 18 locations in Northeast Greenland, using next generation sequencing to identify AM fungi. We studied the joint effect of plant species, elevation and selected abiotic conditions on AM fungal presence, richness and composition. We identified 29 AM fungal virtual taxa (VT), of which six represent putatively new VT. Arbuscular mycorrhizal fungal presence increased with elevation, and as vegetation cover and the active soil layer decreased. Arbuscular mycorrhizal fungal composition was shaped jointly by elevation and plant species identity. We demonstrate that the Arctic harbours a relatively species-rich and nonrandomly distributed diversity of AM fungi. Given the high diversity and general lack of knowledge exposed herein, we encourage further research into the diversity, drivers and functional role of AM fungi in the Arctic. Such insight is urgently needed for an area with some of the globally highest rates of climate change