bioRxiv Science⌕ Search

Biology subjects

Scotti, I.

Publications and source records attributed to Scotti, I..

11 recordsLinked to original sources

Rapid evolutionary responses to climate change in maritime pine (Pinus pinaster Ait.) despite widespread adaptive lag

Climate change is profoundly affecting species worldwide and poses a major threat to their long-term persistence. Although trees may have the potential for rapid adaptation to changing climates, empirical evidence remains limited, and whether these long-lived organisms can adapt quickly enough to keep pace with ongoing climate change is still an open question. To investigate real-time responses to contemporary climate change, we combined genomic data from 82 range-wide populations of the widespread tree Pinus pinaster Ait. with intensive sampling of two successive cohorts from two natural populations. Using an original genotype-environment association (GEA) approach to quantify climate (mal)adaptation, we found that most individuals from both target populations showed evidence of an adaptive lag to current climatic conditions, and are predicted to face substantial risk of maladaptation under future climates. Importantly, changes in genomic composition at climate-associated loci between cohorts were consistent with rapid evolutionary responses to ongoing climate change and could not be explained by neutral demographic processes alone, as supported by forward-time genetic simulations. We also observed a lower realised genetic load in the younger cohort, suggesting that the dynamics of deleterious mutations may change with climatic pressure. Our work provides evidence suggesting genetic responses to contemporary climate change within a single generation, including signals of rapid evolutionary changes in genomic composition at climate-associated loci and signatures of purifying selection, despite widespread adaptive lag to current climates. These findings challenge the view that trees only respond slowly to environmental change and highlight the need to integrate evolutionary dynamics into predictive models of species persistence under future climates.

genomics↗

Multiscale intraspecific variation and coordination of hydraulic traits in silver fir

O_LIIntraspecific variability in hydraulic and morphological traits may alter projections of forest vulnerability to climate change. Recognizing multiscale nature is essential, as trait relationships within populations may not reflect those across the species range. C_LIO_LIWe assessed variability in 11 traits in 10 natural populations of Abies alba across environmental and phylogeographic gradients to evaluate potential impacts on drought vulnerability. We quantified trait variation within and among populations, tested effects of climate, phylogeny and local factors, and evaluated trait coordination across scales. C_LIO_LIHydraulic safety traits and wood density showed low variability, indicating strong constraints. In contrast, water-use and efficiency traits were highly variable. Aridity influenced several traits, but reduced variance was detected only for leaf residual conductance and succulence consisted with stabilising selection. Trait coordination was weak within populations than among populations. C_LIO_LIOverall, A. alba combines constrained hydraulic safety traits with variable water use traits. This may buffer drought impacts but limits shifts in hydraulic safety margins, potentially increasing risks of hydraulic failure, especially in humid environments where populations lack the capacity to tolerate prolonged dry periods. Thus, our findings highlight the need to account for scale-dependent trait variability, coordination, and their underlying drivers when predicting species adaptive capacity to drought. C_LI

plant biology↗

The FORGENIUS genomic resources: new genotyping tools and genomic data for 23 forest tree species and their Genetic Conservation Units

Genetic diversity is a critical but often overlooked component of biological diversity. The European H2020 FORGENIUS project is precisely aimed at increasing the quality and quantity of genetic data to start monitoring the European network of forest Genetic Conservation Units (GCUs). A first step in this direction was developing standardized genomic resources for 23 forest tree species, spanning from rare and scattered (e.g., Abies nebrodensis and Torminalis glaberrima) to widespread, economically relevant ones (e.g., Fagus sylvatica, Picea abies and Pinus sylvestris). Here, we describe the development and application of targeted genotyping tools, primarily based on Single Primer Enrichment Technology (SPET), along with existing SNP arrays for the selected species. The SPET panels developed in FORGENIUS were designed to capture {square}10,000 loci per species, balancing species-specific and randomly distributed regions to ensure broad genome coverage and minimize ascertainment bias. Across 7,192 genotyped trees, we identified over 1.8 million single nucleotide polymorphisms (SNPs) covering approximately 50 Mb of DNA sequence. SPET panels demonstrated high genotyping efficiency and cross-species transferability, especially within genera such as Quercus and Abies. They represent a cost-effective, flexible, and scalable solution for population-level genetic assessments across diverse taxa, enabling standardized, genome-wide characterization of the GCU network. These resources not only promote the establishment of genetic monitoring, support genetically informed conservation strategies and improve our understanding of adaptive responses in European forests, but also enhance species delimitation and hybrid detection, and enable the characterization of phylogenetically related but previously underexplored species.

genomics↗

Genomic signatures of climate-driven (mal)adaptation in an iconic conifer, the English yew (Taxus baccata L.)

The risk of climate maladaptation is increasing for numerous species, including trees. Developing robust methods to assess population maladaptation remains a critical challenge. Genomic offset approaches aim to predict climate maladaptation by characterising the genomic changes required for populations to maintain their fitness under changing climates. In this study, we assessed the risk of climate maladaptation in European populations of English yew (Taxus baccata), a long-lived tree with a patchy distribution across Europe, the Atlas Mountains, and the Near East, where many populations are small or threatened. We found evidence suggesting local climate adaptation by analysing 8,616 SNPs in 475 trees from 29 European T. baccata populations, with climate explaining 18.1% of genetic variance and 100 unlinked climate-associated loci identified via genotype- environment association (GEA). Then, we evaluated the deviation of populations from the overall gene-climate association to assess variability in local adaptation or different adaptation trajectories across populations and found the highest deviations in low latitude populations. Moreover, we predicted genomic offsets and successfully validated these predictions using fitness proxies assessed in plants from 26 populations grown in a comparative experiment. Finally, we integrated information from current local adaptation, genomic offset, historical genetic differentiation and effective migration rates to show that Mediterranean and high-elevation T. baccata populations face higher vulnerability to climate change than low-elevation Atlantic and continental populations. Our study demonstrates the practical use of the genomic offset framework in conservation genetics, offers insights for its further development, and highlights the need for a population-centred approach that incorporates additional statistics and data sources to credibly assess climate vulnerability in wild plant populations.

genomics↗

Beyond Proxies: Towards ecophysiological indicators of drought resistance for forest management

As drought-induced mortality increases globally in forest biomes, it becomes necessary for foresters to have access to reliable predictors of species vulnerability to drought and mortality risk under different climatic scenarios. On the one hand, there exist several "operational" indicators of drought resistance, which are based on observations, expert knowledge and species bioclimate (e.g. Ellenberg, Rameau, ClimEssences). On the other hand, as traits can now be measured at high throughput, functional traits (such as plant hydraulic traits) have been increasingly used to assess species vulnerability to hydraulic failure, a key process of tree mortality under drought. However, this mechanistic approach has never been compared to the operational approach. In this study, we review if indicators commonly used by foresters provide information on Abies species vulnerability to hydraulic failure. We measured a set of traits in a common garden experiment of closely related Mediterranean Abies species. These traits were used as inputs to the SurEau model to compute a single indicator of vulnerability (Time to Hydraulic Failure - THF) and to assess mortality risk in future climate. We found that among circum-Mediterranean firs, a high THF was mainly due to high water losses after stomatal closure. Some operational indicators are good proxies of THF, however they are not available for all species, reduce a species to a single value and have the same limitations as species distribution models. We argue that the ecophysiological approach could help foresters in species selection and in estimating the risk faced by forest tree species in a changing climate. While accounting for the variability of traits, hydraulic models can be forced with different climatic scenarios allowing hydraulic failure risk assessment by the end of the century. HighlightsO_LIIntegrating ecophysiological traits in a process-based model allows the computation of an accurate indicator of vulnerability: the Time to Hydraulic Failure (THF). C_LIO_LIFor Abies species, "operational" indicators, i.e. indicators used by foresters and land managers, are mutually consistent and can be simplified proxies of the vulnerability to hydraulic failure. C_LIO_LIMore research on intra-specific variability is needed to assess the evolutionary potential of Euro-Mediterranean Abies species. C_LI

ecology↗

Estimation of contemporary effective population size in plant populations: limitations of genomic datasets

Effective population size (Ne) is a pivotal evolutionary parameter with crucial implications in conservation practice and policy. Genetic methods to estimate Ne have been preferred over demographic methods because they rely on genetic data rather than time-consuming ecological monitoring. Methods based on linkage disequilibrium, in particular, have become popular in conservation as they require a single sampling and provide estimates that refer to recent generations. A software programme based on the linkage disequilibrium method, GONE, looks particularly promising to estimate contemporary and recent-historical Ne (up to 200 generations in the past). Genomic datasets from non-model species, especially plants, may present some constraints to the use of GONE, as linkage maps and reference genomes are seldom available, and SNP genotyping is usually based on reduced-representation methods. In this study, we use empirical datasets from four plant species to explore the limitations of plant genomic datasets when estimating Ne using the algorithm implemented in GONE, in addition to exploring some typical biological limitations that may affect Ne estimation using the linkage disequilibrium method, such as the occurrence of population structure. We show how accuracy and precision of Ne estimates potentially change with the following factors: occurrence of missing data, limited number of SNPs/individuals sampled, and lack of information about the location of SNPs on chromosomes, with the latter producing a significant bias, previously unexplored with empirical data. We finally compare the Ne estimates obtained in GONE for the last generations with the contemporary Ne estimates obtained in the programmes currentNe and NeEstimator.

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↗

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↗

Genetic signatures of divergent selection in European beech (Fagus sylvatica L.) are associated with the variation in temperature and precipitation across its distribution range

High genetic variation and extensive gene flow may help forest trees with adapting to ongoing climate change, yet the genetic bases underlying their adaptive potential remain largely unknown. We investigated range-wide patterns of potentially adaptive genetic variation in 64 populations of European beech (Fagus sylvatica L.) using 270 SNPs from 139 candidate genes involved either in phenology or in stress responses. We inferred neutral genetic structure and processes (drift and gene flow) and performed differentiation outlier analyses and gene-environment association (GEA) analyses to detect signatures of divergent selection. Beech range-wide genetic structure was consistent with the species previously identified postglacial expansion scenario and recolonization routes. Populations showed high diversity and low differentiation along the major expansion routes. A total of 52 loci were found to be putatively under selection and 15 of them turned up in multiple GEA analyses. Temperature and precipitation related variables were equally represented in significant genotype-climate associations. Signatures of divergent selection were detected in the same proportion for stress response and phenology-related genes. The range-wide adaptive genetic structure of beech appears highly integrated, suggesting a balanced contribution of phenology and stress-related genes to local adaptation, and of temperature and precipitation regimes to genetic clines. Our results imply a best-case scenario for the maintenance of high genetic diversity during range shifts in beech (and putatively other forest trees) with a combination of gene flow maintaining within-population neutral diversity and selection maintaining between-population adaptive differentiation.

evolutionary biology↗

The genetic structure of the European black pine (Pinus nigra Arnold) is shaped by its recent Holocene demographic history.

Fragmentation acting over geological times confers wide, biogeographical scale, genetic diversity patterns to species, through demographic and natural selection processes. To test the effects of historical fragmentation on the genetic diversity and differentiation of a major European forest tree and to resolve its demographic history, we describe and model its spatial genetic structure and gene genealogy. We then test which Pleistocene event, whether recent or ancient, could explain its widespread but patchy geographic distribution using population genetic data, environmental data and realistic demographic timed scenarios. The taxon of interest is a conifer forest tree, Pinus nigra (Arnold), the European black pine, whose populations are located in the mountains of southern Europe and North Africa, most frequently at mid-elevation. We used a set of different genetic markers, both neutral and potentially adaptive, and either bi-parentally or paternally inherited, and we sampled natural populations across the entire range of the species. We analysed the data using frequentist population genetic methods as well as Bayesian inference methods to calibrate realistic, demographic timed scenarios. Species with geographically fragmented distribution areas are expected to display strong among-population genetic differentiation and low within-population genetic diversity. Contrary to these expectations, we show that the current diversity of Pinus nigra and its weak genetic spatial structure are best explained as resulting from late Pleistocene or early Holocene fragmentation of one ancestral population into seven genetic lineages, which we found to be the main biogeographical contributors of the natural black pine forests of today. Gene flow among the different lineages is strong across forests and many current populations are admixed between lineages. We propose to modify the currently accepted international nomenclature made of five subspecies and name these seven lineages using regionally accepted subspecies-level names. HighlightsO_LIThe European black pine, Pinus nigra (Arnold), has a weak spatial genetic structure. C_LIO_LIGene flow among populations is frequent and populations are often of admixed origin. Current genealogies result from recent, late Pleistocene or Holocene events. C_LIO_LISeven modern genetic lineages emerged from divergence and demographic contractions. C_LIO_LIThese seven lineages warrant a revision of subspecies taxonomic nomenclature. C_LI

ecology↗

Genomics of microgeographic adaptation in the hyperdominant Amazonian tree Eperua falcata Aubl. (Fabaceae).

Plant populations can undergo very localized adaptation, allowing widely distributed populations to adapt to divergent habitats in spite of recurrent gene flow. Neotropical trees - whose large and undisturbed populations often span a variety of environmental conditions and local habitats - are particularly good models to study this process. Here, we carried out a genome scan for selection through whole-genome sequencing of pools of populations, sampled according to a replicated sampling design, to evaluate microgeographic adaptation in the hyperdominant Amazonian tree Eperua falcata Aubl. (Fabaceae). A high-coverage genomic resource of [~]250 Mb was assembled de novo and annotated, leading to 32,789 predicted genes. 97,062 bi-allelic SNPs were detected over 25,803 contigs, and a custom Bayesian model was implemented to uncover candidate genomic targets of divergent selection. A set of 290 divergence outlier SNPs was detected at the regional scale (between study sites), while 185 SNPs located in the vicinity of 106 protein-coding genes were detected as replicated outliers between microhabitats within regions. Outlier genomic regions are involved in a variety of physiological processes, including plant responses to stress (e.g., oxidative stress, hypoxia and metal toxicity) and biotic interactions. Together with evidence suggesting microgeographic divergence in functional traits, the discovery of genomic targets of microgeographic adaptation in the Neotropics is consistent with the hypothesis that local adaptation is a key driver of ecological diversification, operating across multiple spatial scales, from large- (i.e. regional) to microgeographic- (i.e. landscape) scales.

evolutionary biology↗