bioRxiv Science⌕ Search

Biology subjects

Opgenoorth, L.

Publications and source records attributed to Opgenoorth, L..

14 recordsLinked to original sources

Early establishment acts as a selective filter shaping climate-associated genomic variation in European beech

Climate change is increasing drought and heat stress in European forests, raising concerns about the capacity of long-lived tree species to respond to rapidly changing environmental conditions. While local adaptation has been documented in many forest trees, it remains unclear whether newly established seedlings, which form the forests of the future, are able to persist and adapt to these new climatic conditions. Here, we investigated genomic differences between naturally regenerated seedlings and trees of European beech (Fagus sylvatica) across the three regions of the German Biodiversity Exploratories using low-coverage whole-genome sequencing (5x) of 1,032 individuals. Population structure was primarily driven by geographic region, whereas genetic diversity was similar across life stages. Despite this genome-wide similarity, we detected allele frequency shifts between trees and seedlings, concentrated in narrow genomic windows. These shifts were strongest in surviving seedlings, suggesting that environmental filtering during early establishment may contribute to shaping the genetic composition of regenerating populations. The strongest signals were observed within the Swabian Alb, where sampled seedlings were 2-years old and had experienced a longer period of potential filtering prior to sampling. Genotype - environment association analyses identified loci associated with climatic variables, and subsequent GO enrichment analyses of genes linked to these loci revealed significantly more enriched GO terms in seedlings than in trees, suggesting stronger environmental filtering by the current climate in seedlings. In particular, we found associations with maximum air temperature, relative humidity, soil moisture, and precipitation, affecting genes involved in stress responses, growth, metabolism, and developmental processes. Together, our results demonstrate that young cohorts of European beech differ genetically from trees and reveal genomic patterns consistent with life-stage-dependent environmental filtering. These findings suggest that the genetic composition of early life-stages is already altered by current environmental conditions, possibly contributing to adaptation to new climatic conditions.

ecology↗

Intra-individual variation in leaf microbiota matches within-crown environmental heterogeneity and promotes tree performance

Plant-associated microbial communities exhibit pronounced specificity across biological and spatial scales. While the patterns and accompanied functions have been well documented across and within plant species, the functional importance of intra-individual variation remains underexplored. Particularly in trees that experience strong environmental gradients within single crowns, stratum-specific microbiota may significantly contribute to plant performance. We experimentally tested whether variation in microbiota within the crown of Quercus robur is related to host performance. In mesocosm experiments, we transferred microbial communities derived from sun and shade leaves to germ-reduced clonal individuals of the same species and applied UV radiation simulating conditions that matched or mismatched the origin of the microbial inoculum (environmental matching). Our results demonstrate that matching microbiota-environment combinations increased plant performance compared to mismatching combinations. We infer that pronounced intra-individual variation of leaf-associated microbial communities not only reflects environmental heterogeneity along canopy strata but is functionally relevant for the plant host.

ecology↗

Recurrent hybridization and gene flow shaped Norway and Siberian spruce evolutionary history over multiple glacial cycles

Over the last decades, extensive genome-wide resequencing studies have highlighted the extent of hybridization and introgression between closely related species. Animal and plant species went through cycles of contractions and expansions as a result of glacial cycles. These repeated sequences of reproductive isolation and admixture at continental scales have led to the accumulation over time of an ancient, deep-seated and complex genetic structure. This structure was blurred by extensive gene flow, or reinforced by strong local adaptation. This already multi-layered structure has often been further enhanced by hybridization. We investigated this complexity in Norway spruce (Picea abies) and Siberian spruce (P. obovata), two closely related species dominating Eurasian boreal forests and forming a vast hybrid zone. Here, we genotyped 542 individuals of both species and their hybrids at 480K SNPs. Individuals came from 55 populations, extending from western Europe to Siberia with a focus on the main hybrid zone. Despite extensive gene flow and a clear Isolation-by-Distance pattern at the continental scale, distinct genetic clusters emerged, indicating barriers and corridors to migration. Coalescent-based demographic inferences revealed that Norway and Siberian spruce repeatedly hybridized during the Pleistocene with introgression pattern varying depending on the latitude. In northern ranges, P. obovata expanded into P. abies while P. abies expanded into P. obovata in the southern parts. Two cryptic refugia located in the large hybrid zone played a critical role in shaping the current distribution of the two species. Our study highlights the importance of considering the whole species complex instead of separate entities to shed light on their complex demographic histories.

evolutionary biology↗

Temperature and day length drive local adaptation in the Patagonian foundation tree species Nothofagus pumilio

Climate change alters relationships among environmental conditions and thus has the potential to change the selection pressures acting on adaptive gene variants. Using a landscape genomic approach, we show that the southern beech species Nothofagus pumilio has notable genetic adaptations to climate along its 2000-kilometer-long range in the Andes. We screened 47,336 SNP loci in 1,632 contigs and found that high-latitude sampling sites have lower genetic diversity, likely due to greater impact of glacial oscillations at high latitudes. Using four genome scan methods, we identified 457 outlier SNPs that are either strongly differentiated among subpopulations or associated with environmental covariates related to temperature, day length, and precipitation. Temperature and day length parameters were associated with notably more outliers than precipitation (n = 133, 113, and 61 outliers, respectively), and almost half of all annotated outliers were related to stress response (n=38, 21%) or catabolism-metabolism (n=43, 24%). Our findings suggest that Nothofagus pumilio is an ideal Andean model of genetic adaptation to climate change because it is locally adapted to extant climate conditions, and shifting patterns among environmental parameters may be detrimental to its future survival and adaptation potential.

genetics↗

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 susceptible to environmental change. The giant root-rat (Tachyoryctes macrocephalus) is a highly 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 whole [~]1,000 km2 range. Our data revealed a distinct division into a northern and southern subpopulation, with no signs of gene flow, and higher nuclear genetic diversity in the south. Landscape genetic analyses of the mitochondrial genomes indicated that population subdivision was driven by steep slopes 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 to 16,000 years ago). Despite the pronounced subdivision observed at the range-wide scale, weak geographic structuring of sampling localities within subpopulations indicated gene flow across distances of at least 16 km, suggesting aboveground dispersal and high mobility for relatively long distances. Our study highlights how topographic barriers can lead to the genetic subdivision of fossorial species, despite their potential to maintain gene flow at the local scale. These factors can reduce genetic variability, which should be considered when developing conservation strategies.

evolutionary biology↗

Synchronous effective population size changes and genetic stability of forest trees through glacial cycles

The effect of past environmental changes on the demography and genetic diversity of natural populations remains a contentious issue and has rarely been investigated across multiple, phylogenetically distant species. Here, we performed comparative population genomic analyses and demographic inferences for seven widely distributed and ecologically contrasted European forest tree species based on concerted sampling of 164 populations across their natural ranges. For all seven species, the effective population size, Ne, increased or remained stable over many glacial cycles and up to 15 million years in the most extreme cases. Hence, surprisingly, the drastic environmental changes associated with the Pleistocene glacial cycles have had little impact on the level of genetic diversity of dominant forest tree species, despite major shifts in their geographic ranges. Based on their trajectories of Ne over time, the seven tree species can be divided into three major groups, highlighting the importance of life history and range size in determining synchronous variation in genetic diversity, over time. Altogether, our results indicate that forest trees were able to retain their evolutionary potential over very long periods of time despite strong environmental changes. One-Sentence SummaryPopulation genomic analyses reveal that forest trees retained their evolutionary potential over the Quaternary.

evolutionary biology↗

Epigenetic variation in the Lombardy poplar along climatic gradients is independent of genetic structure and persists across clonal reproduction

- Environmental changes can trigger phenotypic variation in plants through epigenetic mechanisms, but strong genetic influences make it difficult to isolate and study epigenetic effects. Clonal trees with low genetic variation, such as the Lombardy poplar (Populus nigra cv. Italica Duroi), offer a unique system to study epigenetic variation associated with the environment. - We collected cuttings (ramets) of Lombardy poplar along a wide geographical range in Europe. We performed whole-genome-bisulfite sequencing of 164 ramets grown in a common garden and of a subset of 35 of the original parental individuals. Using historical bioclimatic data, we tested the relationship between DNA methylation and climatic gradients. - We found that average methylation levels in TEs and promoter regions correlate with biologically relevant climatic variables. Furthermore, we observed that DNA methylation was transmitted to the next clonal generation, but a fraction of the methylome changed relatively fast when comparing the parental individuals with the clonal offspring. - Our results suggest that the poplar methylome is a dynamic layer of information that can be transmitted to the clonal offspring and potentially affect how poplars acclimate to new environmental conditions.

ecology↗

High-resolution methylome analysis in the clonal Populus nigra cv. 'Italica' reveals environmentally sensitive hotspots and drought-responsive TE superfamilies

ABSTRACT/SUMMARYO_LIDNA methylation is environment-sensitive and can mediate plant 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 environments, it remains unclear to what extent the methylation responses are generic or stress-specific, and how this relates to their long-term stability. C_LIO_LIHere, we studied the methylome plasticity of a single poplar genotype, Populus nigra cv. Italica. Adult poplar trees with diverse environmental histories were clonally propagated, and the ramets exposed to experimental cold, heat, drought, herbivory, rust infection and salicylic acid treatments. Then, we identified and compared stress-induced vs. naturally occurring DNA methylation changes using whole genome bisulfite sequencing data. C_LIO_LIMethylation changes mainly targeted transposable elements and when occurring in CG/CHG contexts, the same regions were often affected by multiple stresses, indicating a generic response. Drought triggered a unique CHH hypermethylation response in transposable elements, affecting entire superfamilies and often occurring near drought-responsive genes. Stress-induced methylation variation in CG/CHG contexts showed striking overlap with methylation differences observed between trees from distinct geographical locations. C_LIO_LIAltogether, our results indicate that generic methylome stress responses can persist as epialleles in nature while some environments trigger more transient but large and specific responses, with possible functional consequences. C_LI

genomics↗

An uncommon garden experiment: microenvironment has stronger influence on phenotypic variation than epigenetic memory in the clonal Lombardy poplar

Environmental changes can trigger phenotypic variation in plants through epigenetic mechanisms, but strong genetic influences on epigenetic variation and phenotypes make it difficult to isolate and study these effects. We investigated phenotypic plasticity using the Lombardy poplar (Populus nigra cv. Italica Duroi), a globaly distributed clonal tree. We surveyed 14 functional traits related to tree growth, ecophysiological and phenological processes in poplar ramets collected along a wide geographical range in Europe and planted under common garden conditions. We investigated whether phenotypic variation was related to geography and historical bioclimatic data of the ramets sites of origin using linear mixed effect models. We found significant differences in among ramets from different geographic origins in tree height, number of stems per ramet and duration of bud flush. However, microenvironmental variation in the common garden, captured via block effects, had an even bigger impact on phenotypic variation than the environmental conditions at the sites of origin. Our results show that phenotypic variation in the ramets might be associated to the climate origin from different climates, suggesting possible epigenetic memory. However, such legacy effects might be quickly outweighed by new environmental conditions.

ecology↗

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, 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 (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 modeling revealed that elevation and, to a lesser extent, post-glacial colonization history, but not climatic and habitat variables, were the best predictors of FGSG across populations. These results may 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 complementary information about demographic history and could be used for defining conservation priorities.

evolutionary biology↗

Rewinding the molecular clock in the genus Carabus (Coleoptera: Carabidae): Revisiting Andujar et al. in light of new fossil evidence and the Gondwana split

1BackgroundMolecular clocks have become powerful tools given increasing sequencing and fossil resources. However, outcome of calibration analyses depend on choosing priors. Here we revisit a seminal dating study of the genus Carabus by Andujar et al. proposing that their prior choices need re-evaluation with the hypothesis that reflecting fossil evidence and the Gondwanan split properly rewinds the molecular clock significantly. We used the same dataset including five mitochondrial and four nuclear DNA fragments with 7888 nt total length. We set the root age based on the fossil evidence of Harpalinae ground beetles in the Upper Cretaceous and introduce the Paleogene divergence of the outgroup taxa Ceroglossus (endemic to South-America) and Pamborus + Maoripamborus (Australia, New Zealand) as a new prior based on current paleontological and geological literature. ResultsThe ultrametric time-calibrated tree of the extended nd5 dataset resulted in a median TMRCA Carabus age of 58.48 Ma (HPD95% 46.61-72.04), roughly 35 Ma older than in the Andujar study. The splits between C. rugosus and C. morbillosus (A), between C. riffensis from the European Mesocarabus (B), and between Eurycarabus and Nesaeocarabus (C) were dated to 19.19 (13.54-25.87), 25.95 (18.8-34.62), and 23.98 (17.28-31.47) Ma and were thus decidedly older than previously reported (7.48, 10.93, and 9.51 Ma). These changes were driven solely by constraining the Carabidae time tree root with Harpalinae amber fossils at [~]99 Ma. Utilizing the nd5 dating results of three well supported Carabus clades as secondary calibration points for the complete MIT-NUC data set lead to a TMRCA of Carabus of 53.56 (41.25-67.05) Ma compared to 25.16 (18.41-33.04) in Andujars study. ConclusionTaking into account the Gondwanan split as a new prior, together with the fossil evidence of the outgroup taxon Harpalini in the Late Cretaceous, our new approach supports an origin of the genus Carabus in the Paleocene-Early Eocene. Our results are preliminary due to the heavy reliance on the nd5 gene and thus will have to be tested with sufficient set of nuclear markers. In addition, uncertainties arise from dating the root age of the tree based on a single fossil and outgroup taxon which has a major effect on the results. Improvement of the fossil data base particularly in the supertribe Carabitae is thus strongly needed to reduce the currently large uncertainties in dating Carabus phylogeny.

evolutionary biology↗

The Kobresia pygmaea ecosystem of the Tibetan highlands – origin, functioning and degradation of the world’s largest pastoral alpine ecosystem

Kobresia pastures in the eastern Tibetan highlands occupy 450000 km2 and form the worlds largest pastoral alpine ecosystem. The main constituent is an endemic dwarf sedge, Kobresia pygmaea, which forms a lawn with a durable turf cover anchored by a felty root mat, and occurs from 3000 m to nearly 6000 m a.s.l. The existence and functioning of this unique ecosystem and its turf cover have not yet been explained against a backdrop of natural and anthropogenic factors, and thus its origin, drivers, vulnerability or resilience remain largely unknown. Here we present a review on ecosystem diversity, reproduction and ecology of the key species, pasture health, cycles of carbon (C), water and nutrients, and on the paleo-environment. The methods employed include molecular analysis, grazing exclusion, measurements with micro-lysimeters and gas exchange chambers, 13C and 15N labelling, eddy-covariance flux measurements, remote sensing and atmospheric modelling.\n\nThe following combination of traits makes Kobresia pygmaea resilient and highly competitive: dwarf habit, predominantly below-ground allocation of photo assimilates, mixed reproduction strategy with both seed production and clonal growth, and high genetic diversity. Growth of Kobresia pastures is co-limited by low rainfall during the short growing season and livestock-mediated nutrient withdrawal. Overstocking has caused pasture degradation and soil deterioration, yet the extent remains debated. In addition, we newly describe natural autocyclic processes of turf erosion initiated through polygonal cracking of the turf cover, and accelerated by soil-dwelling endemic small mammals. The major consequences of the deterioration of the vegetation cover and its turf include: (1) the release of large amounts of C and nutrients and (2) earlier diurnal formation of clouds resulting in (3) decreased surface temperatures with (4) likely consequences for atmospheric circulation on large regional and, possibly global, scales.\n\nPaleo-environmental reconstruction, in conjunction with grazing experiments, suggests that the present grazing lawns of Kobresia pygmaea are synanthropic and may have existed since the onset of pastoralism. The traditional migratory rangeland management was sustainable over millennia and possibly still offers the best strategy to conserve, and possibly increase, the C stocks in the Kobresia turf, as well as its importance for climate regulation.

ecology↗

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↗

Linking Dendroecology And Association Genetics: Stress Responses Archived In Tree Rings Associate With SNP Genotypes In Abies alba (Mill.)

O_LIGenetic association studies in forest tress would greatly benefit from information on tree response to environmental stressors over time. Dendroecology can close this gap by providing such time series measurements. Here, we jointly analyzed dendroecological and genetic data to explore the genetic basis of resistance, recovery and resilience to episodic stress in silver fir.\nC_LIO_LIWe used individual level tree-ring data to characterize the growth patterns of surviving silver fir (Abies alba) during the forest dieback in the 1970s and 1980s in Central Europe and associated them with SNPs in candidate genes.\nC_LIO_LIMost trees at our study sites in the Bavarian Forest experienced severe growth decline from 1974 until the mid-1980s, which peaked during the drought year of 1976. Using the machine learning algorithm random forest, we identified 15 candidate genes that were associated with the variance in resistance, resilience and recovery among trees in this period.\nC_LIO_LIWith our study we show that the unique possibility of phenotypic time series archived in tree-rings are a powerful resource in genetic association studies. We call for a closer collaboration of dendroceologists and forest geneticists to focus on integrating individual tree level signals in genetic association studies in long lived trees.\nC_LI

ecology↗