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Bossdorf, O.

Publications and source records attributed to Bossdorf, O..

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Parental environmental effects are common and strong, but unpredictable, in Arabidopsis thaliana

The phenotypes of plants can be influenced by the environmental conditions experienced by their parents. In some cases, such parental effects have been found to be adaptive, which has led to much speculation about their ecological and evolutionary significance. However, there is still much uncertainty about how common and how predictable parental environmental effects really are. We carried out a comprehensive test for parental effects of different environmental stresses in the model plant Arabidopsis thaliana. We subjected plants of three Arabidopsis genotypes to a broad range of biotic or abiotic stresses, or combinations thereof, and compared their offspring phenotypes in a common environment. The majority of environmental stresses (16 out of 24 stress treatments) caused significant parental effects, in particular on plant biomass and reproduction, with positive or negative effects ranging from -35% to +38% changes in offspring fitness. The expression of parental effects was strongly genotype-dependent, with some effects only present in some genotypes but absent, or even in the opposite direction, in others. Parental effects of multiple environmental stresses were often non-additive, and their effects can thus not be predicted from what we know about the effects of individual stresses. Intriguingly, the direction and magnitude of parental effects were unrelated to the direct effects on the parents: some stresses did not affect the parents but caused substantial effects on offspring, while for others the situation was reversed. In summary, parental environmental effects are common and often strong in A. thaliana, but they are genotype-dependent and difficult to predict. SignificanceStress experienced by plants can alter the phenotypes of their offspring. To understand the ecological and evolutionary significance of such parental effects, we must know how common and how predictable they are. In a large experiment with Arabidopsis thaliana, we show that the majority of 24 environmental stresses cause significant, and often strong, positive or negative parental effects. However, we also find that parental effects are genotype-specific and unrelated to the direct effect of individual stresses, and that multiple stresses often act in non-additive ways across generations. Thus, parental effects appear to be common and strong, but difficult to predict. Our findings have important implications for the study of plant responses to environmental change, and the design of stress experiments.

ecology↗

Environmental stress determines the colonization and impact of an endophytic fungus on invasive knotweed

O_LIThere is increasing evidence that microbes play a key role in some plant invasions. A diverse and widespread but little understood group of plant-associated microbes are the fungal root endophytes of the order Sebacinales. They are associated with exotic populations of invasive knotweed (Reynoutria ssp.) in Europe, but their effects on the invaders are unknown. C_LIO_LIWe used the recently isolated Sebacinales root endophyte Serendipita herbamans to experimentally inoculate invasive knotweed and study root colonisation and effects on knotweed growth under different environmental conditions. We verified the inoculation success and fungal colonisation through immunofluorescence microscopy and qPCR. C_LIO_LIWe found that S. herbamans strongly colonized invasive knotweed in low-nutrient and shade environments, but much less under drought or benign conditions. At low nutrients, the endophyte had a positive effect on plant growth, whereas the opposite was true under shaded conditions. C_LIO_LISynthesis. Our study demonstrates that the root endophyte S. herbamans has the potential to colonize invasive knotweed fine roots and impact its growth, and it could thus also play a role in natural populations. Our results also show that effects of fungal endophytes on plants can be strongly environment-dependent, and may only be visible under stressful environmental conditions. C_LI

ecology↗

Forest wildflowers bloom earlier as Europe warms - but not everywhere equally.

Some of the most striking biological responses to climate change are the observed shifts in the timing of life-history events of many organisms. Plants, in particular, often flower earlier in response to climate warming, and herbarium specimens are excellent witnesses of such long-term changes. However, in large-scale analyses the magnitude of phenological shifts may vary geographically, and the data are often clustered, and it is thus necessary to account for spatial correlation to avoid geographical biases and pseudoreplication. Here, we analysed herbarium specimens of 20 spring-flowering forest understory herbs to estimate how their flowering phenology shifted across Europe during the last century. Our analyses show that on average these forest wildflowers now bloom over six days earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Plants flowered on average of 3.6 days earlier per 1{degrees}C warming. However, in some parts of Europe plants flowered earlier or later than expected. This means, there was significant residual spatial variation in flowering time across Europe, even after accounting for the effects of temperature, precipitation, elevation and year. Including this spatial autocorrelation into our statistical models significantly improved model fit and reduced bias in coefficient estimates. Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change during the last century, with potential severe consequences for their associated ecological communities. It also demonstrates the power of combining herbarium data with spatial modelling when testing for long-term phenology trends across large spatial scales.

ecology↗

A draft genome of Alliaria petiolata (garlic mustard) as a model system for invasion genetics

The emerging field of invasion genetics examines the genetic causes and consequences of biological invasions, but few study systems are available that integrate deep ecological knowledge with genomic tools. Here we report on the de novo assembly and annotation of a genome for the biennial herb Alliaria petiolata (M. Bieb.) Cavara & Grande (Brassicaceae), which is widespread in Eurasia and invasive across much of temperate North America. Our goal was to sequence and annotate a genome to complement resources available from hundreds of published ecological studies, a global field survey, and hundreds of genetic lines maintained in Germany and Canada. We sequenced a genotype (EFCC-3-20) collected from the native range near Venice, Italy and sequenced paired-end and mate pair libraries at ~70 x coverage. A de novo assembly resulted in a highly continuous draft genome (N50 = 121 Mb; L50 = 2) with 99.7 % of the 1.1 Gb genome mapping to scaffolds of at least 50 Kb in length. A total of 64,770 predicted genes in the annotated genome include 99 % of plant BUSCO genes and 98 % of transcriptome reads. Consistent with previous reports of (auto)hexaploidy in western Europe, we found that almost one third of BUSCO genes (390/1440) mapped to two or more scaffolds despite < 2 % genome-wide average heterozygosity. The continuity and gene space quality of our draft assembly will enable molecular and functional genomic studies of A. petiolata to address questions relevant to invasion genetics and conservation strategies.

genomics↗

Climate warming changes synchrony of plants and pollinators in Germany

Climate warming changes the phenology of many species. When interacting organisms respond differently, climate change may disrupt their interactions and affect the stability of ecosystems. Here, we used GBIF occurrence records to examine phenology trends in plants and their associated insect pollinators in Germany since the 1980s. We found strong phenological advances in plants, but differences in the extent of shifts among pollinator groups. The temporal trends in plant and insect phenologies were generally associated with interannual temperature variation, and thus likely driven by climate change. When examining the synchrony of species-level plant-pollinator interactions, their temporal trends differed among pollinator groups. Overall, plant-pollinator interactions become more synchronized, mainly since the phenology of plants responded more strongly to climate change than that of the pollinators. However, if the observed trends continue, many interactions may become more asynchronous again in the future. Our study suggests that climate change affects the phenologies of both plants and insects, and that it also influences the synchrony of plant-pollinator interactions.

ecology↗

Intraspecific variation in land use-related functional traits in Plantago lanceolata

Background and aimsIntraspecific variation in functional traits is essential for the evolutionary success of organisms. The co-variation between trait variation and environment, as well as between different traits, can help us to understand which ecological factors drive habitat adaptation, and to what extent adaptation may be constrained by trait correlations and trade-offs. In managed grasslands, plants experience a combination of competition, recurrent biomass removal and nutrient pulses. Each of these ecological challenges requires specific plant tolerances, and populations should locally adapt if intraspecific variation exists in these traits. MethodsWe studied variation in land use-related traits in the common grassland plant Plantago lanceolata. In a common environment, we quantified the competitive ability (R*), clipping tolerance and responses to a nitrogen pulse of plants from 54 populations with different land use intensities across Germany. Key resultsWe found significant population differentiation in competitive ability but there was little evidence that trait variation was related to land use intensity. There was a positive relationship between competitive ability and clipping tolerance at the population level, indicating a genetic, and possibly functional, link between these two traits. In contrast, clipping tolerance and nitrogen responses were negatively correlated at the levels of plant individuals, indicating a physiological trade-off between plant responses to these two land-use processes. ConclusionsOur results show that there is substantial intraspecific variation in some of the key functional traits for plant success in managed grasslands, and that rapid evolution and adaptation is therefore possible in these traits.

plant biology↗

Rapid evolution in managed grasslands: different land-use regimes are associated with contrasting phenotypes in Plantago lanceolata

Land-use intensification is a major driver of biodiversity declines, and it is known to decrease species numbers and alter community composition of managed grasslands. An open question is whether similar impacts occur within species, i.e. whether grassland management affects also the genetic diversity of plant populations and alters their genetic composition, possibly reflecting adaptation to land use. To address these questions, we sampled 61 populations of the common grassland herb Plantago lanceolata that covered a broad range of land use intensities in the German Biodiversity Exploratories, and we grew their offspring in a common environment to quantify variation in plant size, architecture, reproduction, and leaf economy. All measured traits harboured substantial heritable variation, and six out of nine traits showed population differentiation. Interestingly, several traits were significantly correlated with land use intensity, but with opposing trends for mowing versus grazing: Increased mowing intensity was associated with larger plant size and lower specific leaf area (SLA), which may reflect evolutionary responses to increased light competition and a lesser need for resource conservation in highly productive meadows. In contrast, increased grazing intensity tended to be associated with smaller plant size and higher SLA, a phenotype syndrome known from grazing lawns. Moreover, we found that land-use intensification also affected genetic diversity, again with opposing effects for mowing versus grazing: while increased mowing was associated with decreased levels of intrapopulation phenotypic variation, the opposite was true for increased grazing intensity. In summary, land use intensification has not only already caused rapid evolutionary changes in these grassland populations, it also affects their future evolutionary potential.

plant biology↗

High standing genetic variation in an invasive plant allows immediate evolutionary response to climate warming

AO_SCPLOWBSTRACTC_SCPLOWPredicting plant distributions under climate change is constrained by our limited understanding of potential rapid adaptive evolution. In an experimental evolution study with the invasive common ragweed, we subjected replicated populations of the same initial genetic composition to simulated climate warming. Pooled DNA sequencing of parental and offspring populations showed that warming populations experienced a greater loss of genetic diversity, and greater genetic divergence from their parents, than control populations. In a common environment, offspring from warming populations showed more convergent phenotypes in seven out of nine plant traits, with later flowering and larger biomass, than plants from control populations. For both traits, we also found a significant higher ratio of phenotypic to genetic differentiation across generations for warming than for control populations, indicating stronger selection under warming conditions. Our findings demonstrate that ragweed populations can rapidly evolve in response to climate change within a single generation.

evolutionary biology↗

Less is more! Rapid increase in plant species richness after reduced mowing of urban grasslands

Urban lawns provide space for recreation in cities, and they are an important part of urban green infrastructures. However, most lawns are intensively managed. As only few plant species can survive the frequent mowing, urban lawns typically harbor only a limited number of plant species. To improve the biodiversity of urban lawns, it is often suggested to reduce the mowing frequency. Here, we studied the plant diversity of urban grasslands that have recently undergone management changes from mowing every few weeks to mowing only once or twice per season and compared them to intensively managed lawns. Within six years after the management changes, the grasslands with reduced mowing frequency indeed hosted 30% more plant species than intensively managed lawns, and they were more heterogeneous both within and between grasslands. Additionally, the species composition of less frequently mown grasslands shifted from common mowing-tolerant lawn species to typical meadow species. Our study thus shows that the reduction of mowing is a simple and effective tool for increasing the biodiversity in urban grasslands.

ecology↗

Effects of forest management on the phenology of early-flowering understory herbs

Many organisms respond to anthropogenic environmental change through shifts in their phenology. In plants, flowering is largely driven by temperature, and therefore affected by climate change. However, on smaller scales climatic conditions are also influenced by other factors, including habitat structure. A group of plants with a particularly distinct phenology are the understorey herbs in temperate forests. In these forests, management alters tree species composition and stand structure and, as a consequence, light conditions and microclimate. Forest management should thus also affect the phenology of understorey herbs. To test this, we recorded the flowering phenology of 20 early-flowering herbs on 100 forest plots varying in management intensity, from near-natural to intensely managed forests, in Central and Southern Germany. We found that in forest stands with a high management intensity the plants flowered on average about two weeks later than in unmanaged forests. This was largely because management also affected microclimate (e.g. spring temperatures of 5.9 {degrees}C in managed coniferous, 6.7 in managed deciduous and 7.0 {degrees}C in unmanaged deciduous plots), which in turn affected phenology, with plants flowering later on colder and moister forest stands (+4.5 days per -1{degrees}C and 2.7 days per 10 % humidity increase). Among forest characteristics, the main tree species as well as the age, overall crown projection area, structural complexity and spatial distribution of trees had the greatest influence on microclimate. Our study demonstrates that forest management alters plant phenology, with potential far-reaching consequences for the ecology and evolution of understorey communities. More generally, our study suggests that besides climate change other drivers of environmental change, too, can influence the phenology of organisms.

ecology↗

A map of climate change-driven natural selection in Arabidopsis thaliana

Through the lens of evolution, climate change is an agent of directional selection that forces populations to change and adapt, or face extinction. Current assessments of the risks associated with climate change1,2, however, do not typically take into account that natural selection can dramatically impact the genetic makeup of populations3. We made use of extensive genome information in Arabidopsis thaliana and measured how rainfall-manipulation affected the fitness of 517 natural lines grown in Spain and Germany. This allowed us to directly infer selection at the genetic level4. Natural selection was particularly strong in the hot-dry Spanish location, killing 63% of lines and significantly changing the frequency of [~]5% of all genome-wide variants. A significant proportion of this selection over variants could be predicted from climate (mis)match between experimental sites and the geographic areas of where variants are found (R2=29-52%). Field-validated predictions across the species range indicated that Mediterranean and Western Siberia populations -- at the edges of the species environmental limits -- currently experience the strongest climate-driven selection, and Central Europeans the weakest. With rapidly increasing droughts and rising temperatures in Europe5, we forecast a wave of directional selection moving North, putting many native A thaliana populations at evolutionary risk.

evolutionary biology↗

A rainfall-manipulation experiment with 517 Arabidopsis thaliana accessions

The gold standard for studying natural selection and adaptation in the wild is to quantify lifetime fitness of individuals from natural populations that have been grown together in a common garden, or that have been reciprocally transplanted. By combining fitness values with species traits and genome sequences, one can infer selection coefficients at the genetic level. Here we present a rainfall-manipulation experiment with 517 whole-genome sequenced natural accessions of the plant Arabidopsis thaliana spanning the global distribution of the species. The experiments were conducted in two field stations in contrasting climates, in the Mediterranean and in Central Europe, where we built rainout shelters and simulated high and low rainfall. Using custom image analysis we quantified fitness- and phenology-related traits for 23,154 pots, which contained about 14,500 plants growing independently, and over 310,000 plants growing in small populations (max. 30 plants). This large field experiment dataset, which associates fitness and ecologically-relevant traits with genomes, will provide an important resource to test eco-evolutionary genetic theories and to understand the potential evolutionary impacts of future climates on an important plant model species.

evolutionary biology↗

Ecological plant epigenetics: Evidence from model and non-model species, and the way forward

Growing evidence makes a strong case that epigenetic mechanisms contribute to complex traits, with implications across many fields of biology from dissecting developmental processes to understanding aspects of human health and disease. In ecology, recent studies have merged ecological experimental design with epigenetic analyses to elucidate the contribution of epigenetics to plant phenotypes, stress response, adaptation to habitat, or species range distributions. While there has been some progress in revealing the role of epigenetics in ecological processes, many studies with non-model species have so far been limited to describing broad patterns based on anonymous markers of DNA methylation. In contrast, studies with model species have benefited from powerful genomic resources, which allow for a more mechanistic understanding but have limited ecological realism. To understand the true significance of epigenetics for plant ecology and evolution, we must combine both approaches transferring knowledge and methods from model-species research to genomes of evolutionarily divergent species, and examining responses to complex natural environments at a more mechanistic level. This requires transforming genomics tools specifically for studying non-model species, which is challenging given the large and often polyploid genomes of plants. Collaboration between molecular epigeneticists, ecologists and bioinformaticians promises to enhance our understanding of the mutual links between genome function and ecological processes.

ecology↗