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.
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With climate change, plant-feeding insects increase their number of annual generations (voltinism). However, to what degree the emergence of a new herbivore generation affects the parasitism rate has ...not been explored. We performed a field experiment to test whether the parasitism rate differs between the first and the second generations of a specialist leaf miner (Tischeria ekebladella), both in the naturally univoltine and bivoltine parts of the leaf miner's distribution. We found an interactive effect between herbivore generation and geographical range on the parasitism rate. The parasitism rate was higher in the first compared to the second host generation in the part of the range that is naturally univoltine, whereas it did not differ between generations in the bivoltine range. Our experiment highlights that shifts in herbivore voltinism might release top-down control, with potential consequences for natural and applied systems.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Despite evidence that the microbiome extends host genetic and phenotypic traits, information on how the microbiome is transmitted and maintained across generations remains fragmented. For ...seed-bearing plants, seeds harbor a distinct microbiome and play a unique role by linking one generation to the next. Studies on microbial inheritance, a process we suggest including both vertical transmission and the subsequent migration of seed microorganisms to the new plant, thus become essential for our understanding of host evolutionary potential and host–microbiome coevolution. We propose dividing the inheritance process into three stages: (i) plant to seed, (ii) seed dormancy, and (iii) seed to seedling. We discuss the factors affecting the assembly of the microbiome during the three stages, highlight future research directions, and emphasize the implications of microbial inheritance for fundamental science and society.
The microbiome has a strong influence on its host. With evidence of microbial inheritance mounting, we might extend the concept of host evolutionary potential to include the microbiome.Seeds play a unique role in the inheritance process by linking plant generations and represent a bottleneck in the continuity of the plant microbiome.Plant microbial inheritance encompasses three stages: plant to seed, seed dormancy, and seed to seedling. Each stage is governed by different processes.Although research on the seed microbiome is still at its infancy, it has the potential of advancing our understanding of the natural world, with implication in fundamental and applied sciences and society.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
1. Plant pathogens and herbivores frequently co-occur on the same host plants. Despite this, little is known about the impact of their interactions on the structure of plant-based ecological ...communities. 2. Here, we synthesize evidence that indicates that plant pathogens may profoundly impact arthropod performance, preference, population dynamics and community structure across multiple spatial and temporal scales. 3. Intriguingly, the effects of plant—pathogen—herbivore interactions frequently cascade up and down multiple trophic levels and explain variation in the arthropod community at spatial scales ranging from patterns within single host plants to entire landscapes. 4. This review indicates that knowledge on pathogen—herbivore interactions may be crucial for understanding the dynamics of terrestrial communities.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Although insect herbivores and fungal pathogens frequently share the same individual host plant, we lack general insights in how fungal infection affects insect preference and performance. We ...addressed this question in a meta-analysis of 1,113 case studies gathered from 101 primary papers that compared preference or performance of insect herbivores on control vs. fungus challenged plants. Generally, insects preferred, and performed better on, not challenged plants, regardless of experimental conditions. Insect response to fungus infection significantly differed according to fungus lifestyle, insect feeding guild, and the spatial scale of the interaction (local/distant). Insect performance was reduced on plants challenged by biotrophic pathogens or endophytes but not by necrotrophic pathogens. For both chewing and piercing-sucking insects, performance was reduced on challenged plants when interactions occurred locally but not distantly. In plants challenged by biotrophic pathogens, both preference and performance of herbivores were negatively impacted, whereas infection by necrotrophic pathogens reduced herbivore preference more than performance and endophyte infection reduced only herbivore performance. Our study demonstrates that fungi could be important but hitherto overlooked drivers of plant-herbivore interactions, suggesting both direct and plant-mediated effects of fungi on insect’s behavior and development.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
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 combined 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 in the land Islands. Twelve years of epidemiological data establish the off‐season as a crucial stage in pathogen metapopulation dynamics, with c. 40% 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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Summary
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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Increasing temperatures and shifting precipitation patterns have major consequences for smallholder farmers, especially in the Global South. Our study examined spatial patterns and climatic drivers ...of farmers' perceptions of climate change, and how these perceptions translated into adaptation actions. We interviewed 56 farmers in southwestern Ethiopia and analyzed ERA5-Land reanalysis climate data from 1971 to 2020. The majority of farmers perceived the recorded temperature increase as well as a decrease and shift in the timing of rainfall. Perceived climate change varied with local climate factors and not with the rate of climate change itself. Farmers' adaptation practices showed associations with local temperature, but not with farmers’ perceptions of climate change. Our findings highlight that even if farmers perceive climate change, perceptions are most common in areas where climate action is already urgent, and perceptions may not translate into adaptation. Thus, targeted and timely information and extension programs are crucial.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Seasonal life history events are often interdependent, but we know relatively little about how the relationship between different events is influenced by the abiotic and biotic environment. Such ...knowledge is important for predicting the immediate and evolutionary phenological response of populations to changing conditions. We manipulated germination timing and shade in a multi-factorial experiment to investigate the relationship between spring and autumn phenology in seedlings of the pedunculate oak,
Quercus robur
, and whether this relationship was mediated by natural colonization of leaves by specialist fungal pathogens (i.e., the oak powdery mildew complex). Each week delay in germination corresponded to about 2 days delay in autumn leaf senescence, and heavily shaded seedlings senesced 5–8 days later than seedlings in light shade or full sun. Within seedlings, leaves on primary-growth shoots senesced later than those on secondary-growth shoots in some treatments. Path analyses demonstrated that germination timing and shade affected autumn phenology both directly and indirectly via pathogen load, though the specific pattern differed among and within seedlings. Pathogen load increased with later germination and greater shade. Greater pathogen load was in turn associated with later senescence for seedlings, but with earlier senescence for individual leaves. Our findings show that relationships between seasonal events can be partly mediated by the biotic environment and suggest that these relationships may differ between the plant and leaf level. The influence of biotic interactions on phenological correlations across scales has implications for understanding phenotypic variation in phenology and for predicting how populations will respond to climatic perturbation.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Climate change is known to shift species' geographical ranges, phenologies and abundances, but less is known about other population dynamic consequences. Here, we analyse spatio-temporal dynamics of ...the Glanville fritillary butterfly (Melitaea cinxia) in a network of 4000 dry meadows during 21 years. The results demonstrate two strong, related patterns: the amplitude of year-to-year fluctuations in the size of the metapopulation as a whole has increased, though there is no long-term trend in average abundance; and there is a highly significant increase in the level of spatial synchrony in population dynamics. The increased synchrony cannot be explained by increasing within-year spatial correlation in precipitation, the key environmental driver of population change, or in per capita growth rate. On the other hand, the frequency of drought during a critical life-history stage (early larval instars) has increased over the years, which is sufficient to explain the increasing amplitude and the expanding spatial synchrony in metapopulation dynamics. Increased spatial synchrony has the general effect of reducing long-term metapopulation viability even if there is no change in average metapopulation size. This study demonstrates how temporal changes in weather conditions can lead to striking changes in spatio-temporal population dynamics.
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