High-resolution methylome analysis uncovers stress-responsive genomic hotspots and drought-sensitive TE superfamilies in the clonal Lombardy poplar.

DNA methylation is environment-sensitive and can mediate stress responses. In long-lived trees, changing environments might cumulatively shape the methylome landscape over their lifetime. However, because high-resolution methylome studies usually focus on single environmental cues, it remains unclear to what extent the methylation responses are generic or stress-specific, and how this relates to their long-term stability. Here, we studied the methylome plasticity of a Populus nigra cv. 'Italica' clone that is widespread across Europe. Adult trees from a variety of geographic locations were clonally propagated in a common garden experiment, and the ramets were exposed to cold, heat, drought, herbivory, rust infection, and salicylic acid treatments. Through comprehensive whole-genome bisulfite sequencing, we analyzed stress-induced and naturally occurring DNA methylation variants. Stress-induced methylation changes predominantly targeted transposable elements. When occurring in CG/CHG contexts, the same regions were often affected by multiple stresses, suggesting a generic response of the methylome. Drought stress caused a distinct CHH hypermethylation response in transposable elements, affecting entire TE superfamilies near drought-responsive genes. Methylation differences in CG/CHG contexts that were induced by stress treatments showed striking overlap with methylation differences observed between trees from distinct geographical locations. Thus, we revealed genomic hotspots of methylation change that are not stress-specific and that contribute to natural DNA methylation variation, and we identified specific transposable element superfamilies that respond to a specific stress with possible functional consequences. Our results underscore the importance of studying the effects of multiple stressors in a single experiment for recognizing general versus stress-specific methylome responses.

Nature 4.0: A networked sensor system for integrated biodiversity monitoring.

Ecosystem functions and services are severely threatened by unprecedented global loss in biodiversity. To counteract these trends, it is essential to develop systems to monitor changes in biodiversity for planning, evaluating, and implementing conservation and mitigation actions. However, the implementation of monitoring systems suffers from a trade-off between grain (i.e., the level of detail), extent (i.e., the number of study sites), and temporal repetition. Here, we present an applied and realized networked sensor system for integrated biodiversity monitoring in the Nature 4.0 project as a solution to these challenges, which considers plants and animals not only as targets of investigation, but also as parts of the modular sensor network by carrying sensors. Our networked sensor system consists of three main closely interlinked components with a modular structure: sensors, data transmission, and data storage, which are integrated into pipelines for automated biodiversity monitoring. We present our own real-world examples of applications, share our experiences in operating them, and provide our collected open data. Our flexible, low-cost, and open-source solutions can be applied for monitoring individual and multiple terrestrial plants and animals as well as their interactions. Ultimately, our system can also be applied to area-wide ecosystem mapping tasks, thereby providing an exemplary cost-efficient and powerful solution for biodiversity monitoring. Building upon our experiences in the Nature 4.0 project, we identified ten key challenges that need to be addressed to better understand and counteract the ongoing loss of biodiversity using networked sensor systems. To tackle these challenges, interdisciplinary collaboration, additional research, and practical solutions are necessary to enhance the capability and applicability of networked sensor systems for researchers and practitioners, ultimately further helping to ensure the sustainable management of ecosystems and the provision of ecosystem services.

Topographic barriers drive the pronounced genetic subdivision of a range-limited fossorial rodent.

Due to their limited dispersal ability, fossorial species with predominantly belowground activity usually show increased levels of population subdivision across relatively small spatial scales. This may be exacerbated in harsh mountain ecosystems, where landscape geomorphology limits species' dispersal ability and leads to small effective population sizes, making species relatively vulnerable to environmental change. To better understand the environmental drivers of species' population subdivision in remote mountain ecosystems, particularly in understudied high-elevation systems in Africa, we studied the giant root-rat (Tachyoryctes macrocephalus), a fossorial rodent confined to the afro-alpine ecosystem of the Bale Mountains in Ethiopia. Using mitochondrial and low-coverage nuclear genomes, we investigated 77 giant root-rat individuals sampled from nine localities across its entire ~1000 km2 range. Our data revealed a distinct division into a northern and southern group, with no signs of gene flow, and higher nuclear genetic diversity in the south. Landscape genetic analyses of the mitochondrial and nuclear genomes indicated that population subdivision was driven by slope and elevation differences of up to 500 m across escarpments separating the north and south, potentially reinforced by glaciation of the south during the Late Pleistocene (~42,000-16,000 years ago). Despite this landscape-scale subdivision between the north and south, weak geographic structuring of sampling localities within regions indicated gene flow across distances of at least 16 km at the local scale, suggesting high, aboveground mobility for relatively long distances. Our study highlights that despite the potential for local-scale gene flow in fossorial species, topographic barriers can result in pronounced genetic subdivision. These factors can reduce genetic variability, which should be considered when developing conservation strategies.

Molecular phylogeny of mega-diverse Carabus attests late Miocene evolution of alpine environments in the Himalayan-Tibetan Orogen.

The timing, sequence, and scale of uplift of the Himalayan-Tibetan Orogen (HTO) are controversially debated. Many geoscientific studies assume paleoelevations close to present-day elevations and the existence of alpine environments across the HTO already in the late Paleogene, contradicting fossil data. Using molecular genetic data of ground beetles, we aim to reconstruct the paleoenvironmental history of the HTO, focusing on its southern margin (Himalayas, South Tibet). Based on a comprehensive sampling of extratropical Carabus, and ~ 10,000 bp of mitochondrial and nuclear DNA we applied Bayesian and Maximum likelihood methods to infer the phylogenetic relationships. We show that Carabus arrived in the HTO at the Oligocene-Miocene boundary. During the early Miocene, five lineages diversified in different parts of the HTO, initially in its southern center and on its eastern margin. Evolution of alpine taxa occurred during the late Miocene. There were apparently no habitats for Carabus before the late Oligocene. Until the Late Oligocene elevations must have been low throughout the HTO. Temperate forests emerged in South Tibet in the late Oligocene at the earliest. Alpine environments developed in the HTO from the late Miocene and, in large scale, during the Pliocene-Quaternary. Findings are consistent with fossil records but contrast with uplift models recovered from stable isotope paleoaltimetry.

Ground and tiger beetles (Coleoptera: Carabidae, Cicindelidae) of the Federal Democratic Republic of Ethiopia: a provisional faunistic checklist based on literature data.

  A provisional checklist and a synopsis of published records and localities (occurrence data) in Ethiopia for ground and tiger beetles are presented. The checklist comprises 878 species, of which 313 (ca. 36%) are endemic or potentially endemic (i.e., so far not recorded from elsewhere) to Ethiopia. In addition, 36 Ethiopian endemic subspecies are listed. The known distribution of each species and subspecies is shown in grid cell-based distributional maps. An annotated gazetteer of included collection localities is provided with the respective synonymic names and variant spellings used in the literature.

Genetic basis of growth reaction to drought stress differs in contrasting high-latitude treeline ecotones of a widespread conifer.

Climate change is increasing the frequency and intensity of drought events in many boreal forests. Trees are sessile organisms with a long generation time, which makes them vulnerable to fast climate change and hinders fast adaptations. Therefore, it is important to know how forests cope with drought stress and to explore the genetic basis of these reactions. We investigated three natural populations of white spruce (Picea glauca) in Alaska, located at one drought-limited and two cold-limited treelines with a paired plot design of one forest and one treeline plot. We obtained individual increment cores from 458 trees and climate data to assess dendrophenotypes, in particular the growth reaction to drought stress. To explore the genetic basis of these dendrophenotypes, we genotyped the individual trees at 3000 single nucleotide polymorphisms in candidate genes and performed genotype-phenotype association analysis using linear mixed models and Bayesian sparse linear mixed models. Growth reaction to drought stress differed in contrasting treeline populations. Therefore, the populations are likely to be unevenly affected by climate change. We identified 40 genes associated with dendrophenotypic traits that differed among the treeline populations. Most genes were identified in the drought-limited site, indicating comparatively strong selection pressure of drought-tolerant phenotypes. Contrasting patterns of drought-associated genes among sampled sites and in comparison to Canadian populations in a previous study suggest that drought adaptation acts on a local scale. Our results highlight genes that are associated with wood traits which in turn are critical for the establishment and persistence of future forests under climate change.

The EpiDiverse Plant Epigenome-Wide Association Studies (EWAS) Pipeline.

Bisulfite sequencing is a widely used technique for determining DNA methylation and its relationship with epigenetics, genetics, and environmental parameters. Various techniques were implemented for epigenome-wide association studies (EWAS) to reveal meaningful associations; however, there are only very few plant studies available to date. Here, we developed the EpiDiverse EWAS pipeline and tested it using two plant datasets, from P. abies (Norway spruce) and Q. lobata (valley oak). Hence, we present an EWAS implementation tested for non-model plant species and describe its use.

Rewinding the molecular clock in the genus Carabus (Coleoptera: Carabidae) in light of fossil evidence and the Gondwana split: A reanalysis.

Molecular clocks have become powerful tools given increasing sequencing and fossil resources. However, calibration analyses outcomes depend on the choice of priors. Here, we revisited the seminal dating study published by Andújar and coworkers of the genus Carabus proposing that prior choices need re-evaluation. We hypothesized that reflecting fossil evidence and the Gondwanan split properly significantly rewinds the molecular clock. We re-used the dataset including five mitochondrial and four nuclear DNA fragments with a total length of 7888 nt. Fossil evidence for Oligocene occurrence of Calosoma was considered. Root age was set based on the fossil evidence of Harpalinae ground beetles in the Upper Cretaceous. Paleogene divergence of the outgroup taxa Ceroglossini and Pamborini is introduced as a new prior based on current paleontological and geological literature. The ultrametric time-calibrated tree of the extended nd5 dataset resulted in a median TMRCA Carabus of 53.92 Ma (HPD 95% 45.01-63.18 Ma), roughly 30 Ma older than in the Andújar study. The splits among C. rugosus and C. morbillosus (A), C. riffensis from the European Mesocarabus (B), and Eurycarabus and Nesaeocarabus (C) were dated to 17.58 (12.87-22.85), 24.14 (18.02-30.58), and 21.6 (16.44-27.43) Ma. They were decidedly older than those previously reported (7.48, 10.93, and 9.51 Ma). These changes were driven almost entirely by constraining the Carabidae time-tree root with a Harpalinae amber fossil at ~99 Ma. Utilizing the nd5 dating results of three well-supported Carabus clades as secondary calibration points for the complete MIT-NUC dataset led to a TMRCA of Carabus of 44.72 (37.54-52.22) Ma, compared with 25.16 Ma (18.41-33.04 Ma) in the previous study. Considering fossil evidence for Oligocene Calosoma and Late Cretaceous Harpalini together with the Gondwanan split as a new prior, our new approach supports the origin of genus Carabus in the Eocene. Our results are preliminary because of the heavy reliance on the nd5 gene, and thus will have to be tested with a sufficient set of nuclear markers. Additionally, uncertainties due to dating root age of the tree based on a single fossil and outgroup taxon affect the results. Improvement of the fossil database, particularly in the supertribe Carabitae, is needed to reduce these uncertainties in dating Carabus phylogeny.

Evolutionary history of two rare endemic conifer species from the eastern Qinghai-Tibet Plateau.

BACKGROUND AND AIMS: Understanding the population genetics and evolutionary history of endangered species is urgently needed in an era of accelerated biodiversity loss. This knowledge is most important for regions with high endemism that are ecologically vulnerable, such as the Qinghai-Tibet Plateau (QTP). METHODS: The genetic variation of 84 juniper trees from six populations of Juniperus microsperma and one population of Juniperus erectopatens, two narrow-endemic junipers from the QTP that are sister to each other, was surveyed using RNA-sequencing data. Coalescent-based analyses were used to test speciation, migration and demographic scenarios. Furthermore, positively selected and climate-associated genes were identified, and the genetic load was assessed for both species. KEY RESULTS: Analyses of 149 052 single nucleotide polymorphisms showed that the two species are well differentiated and monophyletic. They diverged around the late Pliocene, but interspecific gene flow continued until the Last Glacial Maximum. Demographic reconstruction by Stairway Plot detected two severe bottlenecks for J. microsperma but only one for J. erectopatens. The identified positively selected genes and climate-associated genes revealed habitat adaptation of the two species. Furthermore, although J. microsperma had a much wider geographical distribution than J. erectopatens, the former possesses lower genetic diversity and a higher genetic load than the latter. CONCLUSIONS: This study sheds light on the evolution of two endemic juniper species from the QTP and their responses to Quaternary climate fluctuations. Our findings emphasize the importance of speciation and demographic history reconstructions in understanding the current distribution pattern and genetic diversity of threatened species in mountainous regions.

Fine-scale spatial genetic structure across the species range reflects recent colonization of high elevation habitats in silver fir (Abies alba Mill.).

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 1,368 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 (FCT = 0.148) was an order of magnitude greater than between elevations within sites (FSC = 0.031), nevertheless high elevation populations consistently exhibited a stronger FSGS. Structural equation modelling 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.

Adaptive responses to temperature and precipitation variation at the early-life stages of Pinus sylvestris.

Early-stage fitness variation has been seldom evaluated at broad scales in forest tree species, despite the long tradition of studying climate-driven intraspecific genetic variation. In this study, we evaluated the role of climate in driving patterns of population differentiation at early-life stages in Pinus sylvestris and explored the fitness and growth consequences of seed transfer within the species range. We monitored seedling emergence, survival and growth over a 2-yr period in a multi-site common garden experiment which included 18 European populations and spanned 25° in latitude and 1700 m in elevation. Climate-fitness functions showed that populations exhibited higher seedling survival and growth at temperatures similar to their home environment, which is consistent with local adaptation. Northern populations experienced lower survival and growth at warmer sites, contrary to previous studies on later life stages. Seed mass was higher in populations from warmer areas and was positively associated with survival and growth at more southern sites. Finally, we did not detect a survival-growth trade-off; on the contrary, bigger seedlings exhibited higher survival probabilities under most climatic conditions. In conclusion, our results reveal that contrasting temperature regimes have played an important role in driving the divergent evolution of P. sylvestris populations at early-life stages.

Complete mitochondrial genome of the giant root-rat (Tachyoryctes macrocephalus).

The endangered giant root-rat (Tachyoryctes macrocephalus, also known as giant mole rat) is a fossorial rodent endemic to the afro-alpine grasslands of the Bale Mountains in Ethiopia. The species is an important ecosystem engineer with the majority of the global population found within 1000 km2. Here, we present the first complete mitochondrial genome of the giant root-rat and the genus Tachyoryctes, recovered using shotgun sequencing and iterative mapping. A phylogenetic analysis including 15 other representatives of the family Spalacidae placed Tachyoryctes as sister genus to Rhizomys with high support. This position is in accordance with a recent study revealing the topology of the Spalacidae family. The full mitochondrial genome of the giant root-rat presents an important resource for further population genetic studies.

Tackling the challenges of evolutionary forest research with multidata approaches.

Many forest tree species have characteristics that make the study of their evolutionary ecology complex. For example, they are long-lived and thus have long generation times, and their often large, complex genomes have hampered establishing genomic resources. One way to tackle this challenge is to access multiple complementary data sources and analytical approaches when attempting to infer patterns of adaptive evolution. In the cover article of this issue of Molecular Ecology, Depardieu et al. (2021) combine large amounts of environmental, genomic, dendrochronological, and gene expression data in a common garden to explore the polygenic basis of drought resistance in white spruce (Picea glauca), a long-lived conifer. They identify candidate genes involved in growth and resistance to extreme drought events and show how multiple data sets may deliver complementary evidence to circumvent the manifold challenges of the research field.

The GenTree Platform: growth traits and tree-level environmental data in 12 European forest tree species.

BACKGROUND: Progress in the field of evolutionary forest ecology has been hampered by the huge challenge of phenotyping trees across their ranges in their natural environments, and the limitation in high-resolution environmental information. FINDINGS: The GenTree Platform contains phenotypic and environmental data from 4,959 trees from 12 ecologically and economically important European forest tree species: Abies alba Mill. (silver fir), Betula pendula Roth. (silver birch), Fagus sylvatica L. (European beech), Picea abies (L.) H. Karst (Norway spruce), Pinus cembra L. (Swiss stone pine), Pinus halepensis Mill. (Aleppo pine), Pinus nigra Arnold (European black pine), Pinus pinaster Aiton (maritime pine), Pinus sylvestris L. (Scots pine), Populus nigra L. (European black poplar), Taxus baccata L. (English yew), and Quercus petraea (Matt.) Liebl. (sessile oak). Phenotypic (height, diameter at breast height, crown size, bark thickness, biomass, straightness, forking, branch angle, fructification), regeneration, environmental in situ measurements (soil depth, vegetation cover, competition indices), and environmental modeling data extracted by using bilinear interpolation accounting for surrounding conditions of each tree (precipitation, temperature, insolation, drought indices) were obtained from trees in 194 sites covering the species' geographic ranges and reflecting local environmental gradients. CONCLUSION: The GenTree Platform is a new resource for investigating ecological and evolutionary processes in forest trees. The coherent phenotyping and environmental characterization across 12 species in their European ranges allow for a wide range of analyses from forest ecologists, conservationists, and macro-ecologists. Also, the data here presented can be linked to the GenTree Dendroecological collection, the GenTree Leaf Trait collection, and the GenTree Genomic collection presented elsewhere, which together build the largest evolutionary forest ecology data collection available.

A Chromosome-Level Genome Assembly of the European Beech (Fagus sylvatica) Reveals Anomalies for Organelle DNA Integration, Repeat Content and Distribution of SNPs.

The European Beech is the dominant climax tree in most regions of Central Europe and valued for its ecological versatility and hardwood timber. Even though a draft genome has been published recently, higher resolution is required for studying aspects of genome architecture and recombination. Here, we present a chromosome-level assembly of the more than 300 year-old reference individual, Bhaga, from the Kellerwald-Edersee National Park (Germany). Its nuclear genome of 541 Mb was resolved into 12 chromosomes varying in length between 28 and 73 Mb. Multiple nuclear insertions of parts of the chloroplast genome were observed, with one region on chromosome 11 spanning more than 2 Mb which fragments up to 54,784 bp long and covering the whole chloroplast genome were inserted randomly. Unlike in Arabidopsis thaliana, ribosomal cistrons are present in Fagus sylvatica only in four major regions, in line with FISH studies. On most assembled chromosomes, telomeric repeats were found at both ends, while centromeric repeats were found to be scattered throughout the genome apart from their main occurrence per chromosome. The genome-wide distribution of SNPs was evaluated using a second individual from Jamy Nature Reserve (Poland). SNPs, repeat elements and duplicated genes were unevenly distributed in the genomes, with one major anomaly on chromosome 4. The genome presented here adds to the available highly resolved plant genomes and we hope it will serve as a valuable basis for future research on genome architecture and for understanding the past and future of European Beech populations in a changing climate.

Selection patterns on early-life phenotypic traits in Pinus sylvestris are associated with precipitation and temperature along a climatic gradient in Europe.

Understanding the dynamics of selection is key to predicting the response of tree species to new environmental conditions in the current context of climate change. However, selection patterns acting on early recruitment stages and their climatic drivers remain largely unknown in most tree species, despite being a critical period of their life cycle. We measured phenotypic selection on Pinus sylvestris seed mass, emergence time and early growth rate over 2 yr in four common garden experiments established along the latitudinal gradient of the species in Europe. Significant phenotypic plasticity and among-population genetic variation were found for all measured phenotypic traits. Heat and drought negatively affected fitness in the southern sites, but heavy rainfalls also decreased early survival in middle latitudes. Climate-driven directional selection was found for higher seed mass and earlier emergence time, while the form of selection on seedling growth rates differed among sites and populations. Evidence of adaptive and maladaptive phenotypic plasticity was found for emergence time and early growth rate, respectively. Seed mass, emergence time and early growth rate have an adaptive role in the early stages of P. sylvestris and climate strongly influences the patterns of selection on these fitness-related traits.

Genetic variation in early fitness traits across European populations of silver birch (Betula pendula).

Given that the ecological niche of tree species is typically narrower for earlier life stages, intraspecific genetic variation at early fitness traits may greatly influence the adaptive response of tree populations to changing environmental conditions. In this study, we evaluated genetic variation in early fitness traits among 12 populations of Betula pendula from a wide latitudinal range in Europe (41-55°N). We first conducted a chamber experiment to test for population differences in germination and the effect of pre-chilling treatment on seed dormancy release. We then established three common gardens spread across the species latitudinal range in order to evaluate levels of quantitative genetic variation and genotype-by-environment interaction at different early life traits. Our results showed significant variation in chamber germination rates among populations (0-60 %), with southern populations exhibiting lower germination. Pre-chilling treatments did not generally improve germination success. Population seedling emergence rates in the field were correlated with chamber germination rates, though being an order of magnitude lower, with an average ranging from 0 to 1.3 % across gardens. Highly significant variation was found in field emergence rates among populations, and between seed-crop years within populations, but not among families within populations. Populations differed in seedling height, diameter, slenderness and budburst date, with significant among-family variation. Population latitude was positively associated with chamber germination rate and with seedling emergence rate in one of the central field sites. Overall, genetic, environmental and demographic factors seem to influence the observed high levels of variation in early fitness traits among B. pendula populations. Our results suggest limited regeneration capacity for the study species under drier conditions, but further field trials with sufficient replication over environments and seed crops will improve our understanding of its vulnerability to climate change.

Molecular Phylogeography and Evolutionary History of the Endemic Species Corydalis hendersonii (Papaveraceae) on the Tibetan Plateau Inferred From Chloroplast DNA and ITS Sequence Variation.

In response to past climatic changes, the species with different habits or adaptive traits likely have experienced very different evolutionary histories, especially for species that restricted to high mountain areas. In order to trace how Quaternary climatic oscillations affected range distributions and intraspecific divergence of such alpine plants on the Tibetan Plateau, here, we investigated maternally inherited chloroplast DNA (cpDNA) markers and biparentally inherited nuclear ribosomal internal transcribed spacer (ITS) DNA variations and aimed to explore the phylogeographic history of the endemic alpine species Corydalis hendersonii Hemsl. (Papaveraceae). We sequenced four cpDNA fragments (trnS-trnG, trnT-trnL, atpH-atpI, and psbE-petL) and also the nuclear (ITS) region in 368 individuals from 30 populations across the species' range. The network and phylogenetic analysis based on cpDNA variations identified 15 chlorotypes that cluster into three distinct clades. However, our nuclear DNA results demonstrated that there were four genetic/geographical groups within C. hendersonii. Some common and highly divergent cpDNA and ITS haplotypes were distributed in the populations of central and northeastern Tibetan Plateau, and the highest nucleotide diversity and genetic differentiation were detected in the central region. Demographic tests further indicated that the populations of southwestern and western Tibet may have experienced recent range expansion, which most likely occurred during the last glacial maximum (LGM) and continued its expansion after the beginning of the Holocene. These two different groups of this species may have derived from potential refugia that existed in the central and/or northeastern regions of Tibet during recent interglacial periods. In addition, our AMOVA analyses detected high genetic differentiation along with the whole sampling range. Also, distinct phylogeographic structures were detected among populations of C. hendersonii based on both of cpDNA and ITS variation. These findings shed new light on the importance of climatic oscillations during Quaternary and complex local topography as causes of intraspecific diversification and demographic changes within cold-tolerant herbs in the Tibetan Plateau biodiversity hotspot.

Author Correction: The GenTree Dendroecological Collection, tree-ring and wood density data from seven tree species across Europe.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Individual reproductive success in Norway spruce natural populations depends on growth rate, age and sensitivity to temperature.

Quantifying the individual reproductive success and understanding its determinants is a central issue in evolutionary research for the major consequences that the transmission of genetic variation from parents to offspring has on the adaptive potential of populations. Here, we propose to distil the myriad of information embedded in tree-ring time series into a set of tree-ring-based phenotypic traits to be investigated as potential drivers of reproductive success in forest trees. By using a cross-disciplinary approach that combines parentage analysis and a thorough dendrophenotypic characterisation of putative parents, we assessed sex-specific relationships between such dendrophenotypic traits (i.e., age, growth rate and parameters describing sensitivity to climate and to extreme climatic events) and reproductive success in Norway spruce. We applied a full probability method for reconstructing parent-offspring relationships between 604 seedlings and 518 adult trees sampled within five populations from southern and central Europe. We found that individual female and male reproductive success was positively associated with tree growth rate and age. Female reproductive success was also positively influenced by the correlation between growth and the mean temperature of the previous vegetative season. Overall, our results showed that Norway spruce individuals with the highest fitness are those who are able to keep high-growth rates despite potential growth limitations caused by reproductive costs and climatic limiting conditions. Identifying such functional links between the individual ecophysiological behaviour and its evolutionary gain would increase our understanding on how natural selection shapes the genetic composition of forest tree populations over time.