Dr. Katalin Csillery

We propose a long-overdue subgeneric classification of Fagus and revision of its western Eurasian taxa based on population-level sampling of morphological and molecular data. The molecular sequence data bolstering this classification derive from nuclear-encoded genetic markers. Fagus subg. Fagus comprises twelve species, of which two occur in North America, four in western Eurasia, and six in East Asia. Fagus subg. Englerianae Denk & G. W. Grimm comprises three East Asian species. Application of a new species concept using fine-scale data justifies the recognition of previously overlooked cryptic taxa. Beech trees from western Eurasia are currently treated as one species, F. sylvatica L., with two subspecies. Despite this, several previous studies pointed out distinct differences between beech populations from Europe, Turkey, the Caucasus region, and the Hyrcanian forest region including the Talysh Mountains of Azerbaijan and the forests south of the Caspian Sea in Iran. All newly generated data indicate that the various Oriental beeches reflect divergences and speciation processes predating the split between the European beech and its eastern siblings. Therefore, based on morphological and molecular differences, we recognize four species in western Eurasia, the European F. sylvatica L., the chiefly northwestern Turkish F. orientalis Lipsky, the Caucasian F. hohenackeriana Palib., and the Hyrcanian F. caspica Denk & G. W. Grimm. Diagnostic genotypic characteristics are included in the descriptions.

Climate change-related extreme drought events already have a significant impact on the productivity and mortality of Central European forests. European beech (Fagus sylvatica ssp. sylvatica), one of the most important European broadleaved species, has responded to such drought periods with increasing mortality and reduced volume increment. This has raised concerns about its suitability and adaptive capacity in relation to future climatic conditions and motivated the search for alternative tree species that are suitable for assisted migration into European beech forests. One of the candidates is the Oriental beech species complex (F. sylvatica ssp. orientalis), whose range extends from the Balkan to Iran and, at least in some parts of its range, grows under a warmer and drier climate. In order to evaluate whether Oriental beech is more drought tolerant, we compared the radial growth response to droughts between 1920 and 2018 of a total of 138 European and 122 Oriental beeches growing under identical site conditions in eight different locations in Germany and France. The species identity of all analysed trees was verified by microsatellite analyses, and the origin of the introduced Oriental beech was traced to the Greater Caucasus (7 stands) and the Black Sea coast (1 stand). The drought responses of radial growth were quantified using the indices resistance, resilience, and recovery as suggested by Lloret et al. (2011) and growth recovery time (GRT) (Thurm et al., 2016) and used as response variables in generalized linear mixed effect models. Considering only the average radial growth response to severe and extreme drought events, both the different Lloret indices and the GRT did not show prominent difference between Oriental and European beech. However, the mixed model analyses, which also included interaction terms, revealed interspecific differences in drought tolerance, depending on the intensity and timing of the drought. In extreme summer drought years, values of resistance predicted by the mixed-effect models were significantly higher in Oriental beech than in European beech, whereas its resilience was only slightly better than in European beech, regardless of drought intensities. In contrast, Oriental beech was much more susceptible to spring drought with significantly weaker growth recovery and distinctly longer growth recovery times. Based on these results, Oriental beech provenances from the Caucasus do not appear to be sufficiently more drought tolerant than European beech to justify an assisted migration approach to adapt Central European forests to climate change. To analyse the drought tolerance of Oriental beech more comprehensively, introduced trees representing other genetic clusters need to be analysed, as well as the effects of repeated drought events on growth and mortality.

European beech (Fagus sylvatica L.) forests have recently experienced severe diebacks that are expected to increase in future. Oriental beech (Fagus sylvatica spp. orientalis (Lipsky) Greut. & Burd) is a potential candidate for assisted migration (AM) in European forests due to its greater genetic diversity and potentially higher drought resistance. Yet AM entails not only benefits, but also risks, and it is therefore important to monitor the progression of introduced (sub)species. Here, we demonstrate the potential of leaf spectroscopy to replace resource-intensive genetic analysis and field phenotyping for the discrimination and characterization of these two beech subspecies.
We studied two European beech forests, one in France and one in Switzerland, where Oriental beech from the Greater Caucasus was introduced over 100 years ago. During two summers (2021, 2022), we measured leaf spectral reflectance, leaf morphological and biochemical traits from genotyped adult trees. Subspecies prediction models were developed separately for top-of-canopy leaves (amenable to remote sensing) and bottom-of-canopy leaves (easier to harvest) using partial least squares discriminant analysis (PLS-DA) and different sets of spectral predictors.
Morphological, biochemical and spectra-derived leaf traits indicated that Oriental beech trees at the sites studied were characterized by higher lignin and nitrogen per unit leaf area than European beech, suggesting more protein-rich leaves on a per-area basis. The model based on top-of-canopy leaf reflectance spectra in the short-wave-infrared region (SWIR I: 1450-1750 nm) most accurately distinguished Oriental from European beech (BA = 0.86 ± 0.08, k = 0.72 ± 0.15), closely followed by models based on SWIR II, and on spectra-derived traits (BA ≥ 0.84, k ≥ 0.67).
This study provides a proof-of-principle for the development of spectroscopy-based approaches when monitoring introduced species, subspecies or provenances. Our findings hold promise for upscaling to large forest areas using airborne remote sensing.

The benefits and risks of human-aided translocation of individuals within the species range, assisted gene flow (AGF), depend on the genetic divergence, on the rate and direction of hybridization, and on the climate transfer distance between the host and donor populations. In this study, we explored the use of Oriental beech (Fagus sylvatica subsp. orientalis), growing from Iran to the Balkans, for AGF into European beech populations (F. sylvatica subsp. sylvatica) that increasingly suffer from climate warming. Using samples from natural populations of Oriental and European beech and microsatellite loci, we identified 5 distinct genetic clusters in Oriental beech with a divergence (F_ST) of 0.15 to 0.25 from European beech. Using this knowledge, we traced the origin of 11 Oriental beech stands in Western Europe established during the 20th century. In two stands of Greater Caucasus origin, we found evidence for extensive hybridization, with 18% and 41% of the offspring having hybrid status. Climate data revealed higher seasonality with warmer and drier summers across the native Oriental beech sites in comparison to the planting sites in Western Europe. Accordingly, we found that bud burst of Oriental beech occurred four days earlier than in European beech. Overall, our results suggest that AGF of Oriental beech could increase the genetic diversity of European beech stands and may foster introgression of variants adapted to expected future climatic conditions. Our study showcases the evaluation of the benefits and risks of AGF and call for similar studies on other native tree species.

Genetic diversity influences the evolutionary potential of forest trees under changing environmental conditions, thus indirectly the ecosystem services that forests provide. European beech (Fagus sylvatica L.) is a dominant European forest tree species that increasingly suffers from climate change-related die-back. Here, we conducted a systematic literature review of neutral genetic diversity in European beech and created a meta-data set of expected heterozygosity (He) from all past studies providing nuclear microsatellite data. We propose a novel approach, based on population genetic theory and a min–max scaling to make past studies comparable. Using a new microsatellite data set with unprecedented geographic coverage and various re-sampling schemes to mimic common sampling biases, we show the potential and limitations of the scaling approach. The scaled meta-dataset reveals the expected trend of decreasing genetic diversity from glacial refugia across the species range and also supports the hypothesis that different lineages met and admixed north of the European mountain ranges. As a result, we present a map of genetic diversity across the range of European beech which could help to identify seed source populations harboring greater diversity and guide sampling strategies for future genome-wide and functional investigations of genetic variation. Our approach illustrates how to combine information from several nuclear microsatellite data sets to describe patterns of genetic diversity extending beyond the geographic scale or mean number of loci used in each individual study, and thus is a proof-of-concept for synthesizing knowledge from existing studies also in other species.

Abies alba has a high potential for mitigating climate change in European mountain forests, yet, its natural regeneration is severely limited by ungulate browsing. Here, we simulated browsing in a common garden experiment to study growth and physiological traits, measured from bulk needles, using a randomized block design with two levels of browsing severity and seedlings originating from 19 populations across Switzerland. Genetic factors explained most variation in growth (on average, 51.5%) and physiological traits (10.2%) under control conditions, while heavy browsing considerably reduced the genetic effects on growth (to 30%), but doubled those on physiological traits related to C storage. While browsing reduced seedling height, it also lowered seedling water use efficiency (decreased δ¹³C) and increased their δ¹⁵N. Different populations reacted differently to browsing stress, and for seedling height, starch concentration and δ¹⁵N, population differences appeared to be the result of natural selection. First, we found that populations originating from the warmest regions recovered the fastest from browsing stress, and they did so by mobilizing starch from their needles, which suggests a genetic underpinning for a growth-storage trade-off across populations. Second, we found that seedlings originating from mountain populations growing on steep slopes had a higher δ¹⁵N in the common garden than those originating from flat areas, indicating that they have been selected to grow on N poor, potentially drained, soils. This finding was corroborated by the fact that N concentration in adult needles was lower on steep slopes than on flat ground, strongly indicating that steep slopes are the most N poor environments. These results suggest that adaptation to climate and soil N availability, as well as ungulate browsing pressure co-determine the regeneration and range limit of silver fir.

Changing ecosystem conditions and diverse socio-economical events have contributed to an ingrained presence of non-native tree species (NNTs) in the natural and cultural European landscapes. Recent research endeavors have focused on different aspects of NNTs such as legislation, benefits, and risks for forestry, emphasizing that large knowledge gaps remain. As an attempt to fulfill part of these gaps, within the PEN-CAFoRR COST Action (CA19128) network, we established an open-access questionnaire that allows both academic experts and practitioners to provide information regarding NNTs from 20 European countries. Then, we integrated the data originating from the questionnaire, related to the country-based assessment of both peer-reviewed and grey literature, with information from available datasets (EUFORGEN and EU-Forest), which gave the main structure to the study and led to a mixed approach review. Finally, our study provided important insights into the current state of knowledge regarding NNTs. In particular, we highlighted NNTs that have shown to be less commonly addressed in research, raising caution about those characterized by an invasive behavior and used for specific purposes (e.g., wood production, soil recultivation, afforestation, and reforestation). NNTs were especially explored in the context of resilient and adaptive forest management. Moreover, we emphasized the assisted and natural northward migration of NNTs as another underscored pressing issue, which needs to be addressed by joint efforts, especially in the context of the hybridization potential. This study represents an additional effort toward the knowledge enhancement of the NNTs situation in Europe, aiming for a continuously active common source deriving from interprofessional collaboration.

Klimawandel, Trockenheit, Tannensterben: Forscherinnen und Forscher debattieren über die Zukunftsaussichten der Weisstanne. Jüngste Forschungsergebnisse deuten an, dass diese Baumart grösseres Potenzial hat als oft angenommen.

MyGardenOITrees invite forestières et forestiers de toute l'Europe à participer à une expérience pratique. Un outil de prédiction sera élaboré en fin de projet. Il les aidera à choisir les provenances optimales pour des forêts résilientes au changement climatique.

MyGardenOfTrees sta testando nuove provenienze di semi per le foreste europee. Il progetto di ricerca guidato da ricercatori dell’Istituto Federale di Ricerca WSL in Svizzera si rivolge a proprietari e gestori forestali di tutta Europa e li chiama a partecipare ad un esperimento senza precedenti. Obiettivo finale è creare uno strumento per aiutare i forestali a selezionare le provenienze ottimali e creare generazioni future di foreste resistenti al clima.

A MyGardenOfTrees projekt során különbözõ származású vetõmagokat vizsgálunk több európai erdõben. Mi, a WSL szakemberei arra kérjük az erdészeket szerte Európában, hogy vegyenek részt egy egyedülálló kísérletben. A kutatási projekt eredményei alapján olyan eszközt fejlesztünk ki az erdészek számára, ami segít kiválasztani a vetõmagok optimális származási helyét, hogy az éghajlatváltozáshoz alkalmazkodni képes erdõket tudjanak kialakítani.

Spatially explicit population genetic models have long been developed, yet have rarely been used to test hypotheses about the spatial distribution of genetic diversity or the genetic divergence between populations. Here, we use spatially explicit coalescence simulations to explore the properties of the island and the two-dimensional stepping stone models under a wide range of scenarios with spatio-temporal variation in deme size. We avoid the simulation of genetic data, using the fact that under the studied models, summary statistics of genetic diversity and divergence can be approximated from coalescence times. We perform the simulations using gridCoal, a flexible spatial wrapper for the software msprime (Kelleher et al., 2016, Theoretical Population Biology, 95, 13) developed herein. In gridCoal, deme sizes can change arbitrarily across space and time, as well as migration rates between individual demes. We identify different factors that can cause a deviation from theoretical expectations, such as the simulation time in comparison to the effective deme size and the spatio-temporal autocorrelation across the grid. Our results highlight that F_ST, a measure of the strength of population structure, principally depends on recent demography, which makes it robust to temporal variation in deme size. In contrast, the amount of genetic diversity is dependent on the distant past when N_e is large, therefore longer run times are needed to estimate N_e than F_ST. Finally, we illustrate the use of gridCoal on a real-world example, the range expansion of silver fir (Abies alba Mill.) since the last glacial maximum, using different degrees of spatio-temporal variation in deme size.

Variation in genetic diversity across species ranges has long been recognized as highly informative for assessing populations’ resilience and adaptive potential. The spatial distribution of genetic diversity within populations, referred to as fine-scale spatial genetic structure (FSGS), also carries information about recent demographic changes, yet it has rarely been connected to range scale processes. We studied eight silver fir (Abies alba Mill.) population pairs (sites), growing at high and low elevations, representative of the main genetic lineages of the species. A total of 1368 adult trees and 540 seedlings were genotyped using 137 and 116 single nucleotide polymorphisms (SNPs), respectively. Sites revealed a clear east-west isolation-by-distance pattern consistent with the post-glacial colonization history of the species. Genetic differentiation among sites (F_CT=0.148) was an order of magnitude greater than between elevations within sites (F_SC=0.031), nevertheless high elevation populations consistently exhibited a stronger FSGS. Structural equation modeling revealed that elevation and, to a lesser extent, post-glacial colonization history, but not climatic and habitat variables, were the best predictors of FSGS across populations. These results suggest that high elevation habitats have been colonized more recently across the species range. Additionally, paternity analysis revealed a high reproductive skew among adults and a stronger FSGS in seedlings than in adults, suggesting that FSGS may conserve the signature of demographic changes for several generations. Our results emphasize that spatial patterns of genetic diversity within populations provide information about demographic history complementary to non-spatial statistics, and could be used for genetic diversity monitoring, especially in forest trees.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or - in the particular case where it favours correlations between interacting traits - correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

Drought is one of the most important selection pressures for forest trees in the context of climate change. Yet, the different evolutionary mechanisms, and their environmental drivers, by which certain populations become more drought tolerant than others is still little understood. We studied adaptation to drought in 16 silver fir (Abies alba Mill.) populations from the French Mediterranean Alps by combining observations on seedlings from a greenhouse experiment (N = 8,199) and on adult tress in situ (N = 315). In the greenhouse, we followed half-sib families for four growing seasons for growth and phenology traits, and tested their water stress response in a "drought until death" experiment. Adult trees in the field were assessed for δ¹³C, a proxy for water use efficiency, and genotyped at 357 SNP loci. SNP data was used to generate a null expectation for seedling trait divergence between populations in order to detect the signature of selection, and 31 environmental variables were used to identify the selective environment. We found that seedlings originating from populations with low soil water capacity grew more slowly, attained a smaller stature, and resisted water stress for a longer period of time in the greenhouse. Additionally, adult trees of these populations exhibited a higher water use efficiency as evidenced by their δ¹³C. These results suggest a correlated evolution of the growth-drought tolerance trait complex. Population divergence in bud break phenology was adaptive only in the second growing season, and evolved independently from the growth-drought tolerance trait complex. Adaptive divergence in bud break phenology was principally driven by the inter- and intra-annual variation in temperature at the geographic origin of the population. Our results illustrate the different evolutionary strategies used by populations to cope with drought stress at the range limits across a highly heterogeneous landscape, and can be used to inform assisted migration programs.

Heterogeneous environments, such as mountainous landscapes, create spatially varying selection pressure that potentially affects several traits simultaneously across different life stages, yet little is known about the general patterns and drivers of adaptation in such complex settings. We studied silver fir (Abies alba Mill.) populations across Switzerland and characterized its mountainous landscape using downscaled historical climate data. We sampled 387 trees from 19 populations and genotyped them at 374 single-nucleotide polymorphisms (SNPs) to estimate their demographic distances. Seedling morphology, growth and phenology traits were recorded in a common garden, and a proxy for water use efficiency was estimated for adult trees. We tested whether populations have more strongly diverged at quantitative traits than expected based on genetic drift alone in a multi-trait framework, and identified potential environmental drivers of selection. We found two main responses to selection: (i) populations from warmer and more thermally stable locations have evolved towards a taller stature, and (ii) the growth timing of populations evolved towards two extreme strategies, 'start early and grow slowly' or 'start late and grow fast', driven by precipitation seasonality. Populations following the 'start early and grow slowly' strategy had higher water use efficiency and came from inner Alpine valleys characterized by pronounced summer droughts. Our results suggest that contrasting adaptive life-history strategies exist in silver fir across different life stages (seedling to adult), and that some of the characterized populations may provide suitable seed sources for tree growth under future climatic conditions.

Silver fir (Abies alba Mill.) is a keystone conifer of European montane forest ecosystems that has experienced large fluctuations in population size during during the Quaternary and, more recently, due to land-use change. To forecast the species' future distribution and survival, it is important to investigate the genetic basis of adaptation to environmental change, notably to extreme events. For this purpose, we here provide a first draft genome assembly and annotation of the silver fir genome, established through a community-based initiative. DNA obtained from haploid megagametophyte and diploid needle tissue was used to construct and sequence Illumina paired-end and mate-pair libraries, respectively, to high depth. The assembled A. alba genome sequence accounted for over 37 million scaffolds corresponding to 18.16 Gb, with a scaffold N50 of 14,051 bp. Despite the fragmented nature of the assembly, a total of 50,757 full-length genes were functionally annotated in the nuclear genome. The chloroplast genome was also assembled into a single scaffold (120,908 bp) that shows a high collinearity with both the A. koreana and A. sibirica complete chloroplast genomes. This first genome assembly of silver fir is an important genomic resource that is now publicly available in support of a new generation of research. By genome-enabling this important conifer, this resource will open the gate for new research and more precise genetic monitoring of European silver fir forests.

Over the last decade, the genomic revolution has offered the possibility to generate tremendous amounts of data that contain valuable information on the genetic basis of phenotypic traits, such as those linked to human diseases or those that allow for species to adapt to a changing environment. Most ecologically relevant traits are controlled by a large number of genes with small individual effects on trait variation, but that are connected with one another through complex developmental, metabolic and biochemical networks. As a result, it has recently been suggested that most adaptation events in natural populations are reached via correlated changes at multiple genes at a time, for which the name polygenic adaptation has been coined. The current challenge is to develop methods to extract the relevant information from genomic data to detect the signature of polygenic evolutionary change. The symposium entitled "Detecting the Genomic Signal of Polygenic Adaptation and the Role of Epistasis in Evolution" held in 2017 at the University of Zürich aimed at reviewing our current state of knowledge. In this review, we use the talks of the invited speakers to summarize some of the most recent developments in this field.

Damage due to wind-storms and droughts is increasing in many temperate forests, yet little is known about the long-term roles of these key climatic factors in forest dynamics and in the carbon budget. The objective of this study was to estimate individual and coupled effects of droughts and wind-storms on adult tree mortality across a 31-year period in 115 managed, mixed coniferous forest stands from the Western Alps and the Jura mountains. For each stand, yearly mortality was inferred from management records, yearly drought from interpolated fields of monthly temperature, precipitation and soil water holding capacity, and wind-storms from interpolated fields of daily maximum wind speed. We performed a thorough model selection based on a leave-one-out cross-validation of the time series. We compared different critical wind speeds (CWSs) for damage, wind-storm, and stand variables and statistical models. We found that a model including stand characteristics, drought, and storm strength using a CWS of 25 ms^-1 performed the best across most stands. Using this best model, we found that drought increased damage risk only in the most southerly forests, and its effect is generally maintained for up to 2 years. Storm strength increased damage risk in all forests in a relatively uniform way. In some stands, we found positive interaction between drought and storm strength most likely because drought weakens trees, and they became more prone to stem breakage under wind-loading. In other stands, we found negative interaction between drought and storm strength, where excessive rain likely leads to soil water saturation making trees more susceptible to overturning in a wind-storm. Our results stress that temporal data are essential to make valid inferences about ecological impacts of disturbance events, and that making inferences about disturbance agents separately can be of limited validity. Under projected future climatic conditions, the direction and strength of these ecological interactions could also change.

Quantitative genetic theory provides a means of estimating the evolutionary potential of natural populations. However, this approach was previously only feasible in systems where the genetic relatedness between individuals could be inferred from pedigrees or experimental crosses. The genomic revolution opened up the possibility of obtaining the realized proportion of genome shared among individuals in natural populations of virtually any species, which could promise (more) accurate estimates of quantitative genetic parameters in virtually any species. Such a 'genomic' quantitative genetics approach relies on fewer assumptions, offers a greater methodological flexibility, and is thus expected to greatly enhance our understanding of evolution in natural populations, for example, in the context of adaptation to environmental change, eco-evolutionary dynamics, and biodiversity conservation.