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

Spatial eco-evolutionary feedback in plant-pathogen interactions

In recent years the potential for evolutionary change to drive ecological dynamics, and vice versa, has been widely recognized. However, the convincing examples of eco-evolutionary dynamics mainly stem from highly artificial experimental systems, with conspicuously few examples contributed by field systems. While rarely considered in the eco-evolutionary literature, the gene-for-gene hypothesis inherently recognizes the tight link between evolutionary and ecological dynamics. The boom-and-bust dynamics of some agricultural pathogens are an extreme demonstration of this. In this perspective, we place plant-pathogen systems in a spatial eco-evolutionary framework, which recognizes that ecology and evolution are tightly linked, take place at the same time scale and are strongly influenced by spatial structure. Specifically, we i) exemplify how the ecological process of dispersal modifies rapid local coevolutionary dynamics and thereby shapes spatial variation in resistance, infectivity, and local adaptation; and ii) illustrate how the outcome of coevolution (spatial distribution in resistance, infectivity and local adaptation) drives ecological metapopulation processes. Overall, we conclude that both agricultural and wild pathosystems provide a unique illustration of the high relevance of spatial eco-evolutionary feedback in understanding species interactions.Peer reviewe

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

Evidence for host–microbiome co-evolution in apple

Plants evolved in association with a diverse community of microorganisms. The effect of plant phylogeny and domestication on host–microbiome co‐evolutionary dynamics are poorly understood. Here we examined the effect of domestication and plant lineage on the composition of the endophytic microbiome of 11 Malus species, representing three major groups: domesticated apple (M. domestica), wild apple progenitors, and wild Malus species. The endophytic community of M. domestica and its wild progenitors showed higher microbial diversity and abundance than wild Malus species. Heirloom and modern cultivars harbored a distinct community composition, though the difference was not significant. A community‐wide Bayesian model revealed that the endophytic microbiome of domesticated apple is an admixture of its wild progenitors, with clear evidence for microbiome introgression, especially for the bacterial community. We observed a significant correlation between the evolutionary distance of Malus species and their microbiome. This study supports co‐evolution between Malus species and their microbiome during domestication. This finding has major implications for future breeding programs and our understanding of the evolution of plants and their microbiomes

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

Higher host-plant specialization of root-associated endophytes than mycorrhizal fungi along an arctic elevational gradient

How community-level specialization differs among groups of organisms, and changes along environmental gradients, is fundamental to understanding the mechanisms influencing ecological communities. In this paper, we investigate the specialization of root-associated fungi for plant species, asking whether the level of specialization varies with elevation. For this, we applied DNA barcoding based on the ITS region to root samples of five plant species equivalently sampled along an elevational gradient at a high arctic site. To assess whether the level of specialization changed with elevation and whether the observed patterns varied between mycorrhizal and endophytic fungi, we applied a joint species distribution modeling approach. Our results show that host plant specialization is not environmentally constrained in arctic root-associated fungal communities, since there was no evidence for changing specialization with elevation, even if the composition of root-associated fungal communities changed substantially. However, the level of specialization for particular plant species differed among fungal groups, root-associated endophytic fungal communities being highly specialized on particular host species, and mycorrhizal fungi showing almost no signs of specialization. Our results suggest that plant identity affects associated mycorrhizal and endophytic fungi differently, highlighting the need of considering both endophytic and mycorrhizal fungi when studying specialization in root-associated fungal communities.Peer reviewe

Higher host-plant specialization of root-associated endophytes than mycorrhizal fungi along an arctic elevational gradient

How community-level specialization differs among groups of organisms, and changes along environmental gradients, is fundamental to understanding the mechanisms influencing ecological communities. In this paper, we investigate the specialization of root-associated fungi for plant species, asking whether the level of specialization varies with elevation. For this, we applied DNA barcoding based on the ITS region to root samples of five plant species equivalently sampled along an elevational gradient at a high arctic site. To assess whether the level of specialization changed with elevation and whether the observed patterns varied between mycorrhizal and endophytic fungi, we applied a joint species distribution modeling approach. Our results show that host plant specialization is not environmentally constrained in arctic root-associated fungal communities, since there was no evidence for changing specialization with elevation, even if the composition of root-associated fungal communities changed substantially. However, the level of specialization for particular plant species differed among fungal groups, root-associated endophytic fungal communities being highly specialized on particular host species, and mycorrhizal fungi showing almost no signs of specialization. Our results suggest that plant identity affects associated mycorrhizal and endophytic fungi differently, highlighting the need of considering both endophytic and mycorrhizal fungi when studying specialization in root-associated fungal communities.Peer reviewe