Climatic variation allows montane willows to escape an adaptive trade-off.

Adaptive responses to climate change, based on heritable variation in stress tolerance, may be important for plant population persistence. It is unclear which populations will mount the strongest future adaptive responses. It may be fruitful to identify populations that have escaped trade-offs among performance traits, which can hinder adaptation. Barring strong genetic constraints, the extent of trade-offs may depend on spatial relationships among climate variables shaping different traits. Here, we test for climate-driven ecotypic variation and trade-offs among drought and freezing sensitivity, and growth, for Lemmon's willow (Salix lemmonii) in a common garden study of 90 genotypes from 38 sites in the Sierra Nevada, USA. Salix lemmonii exhibits ecotypic variation in leaf turgor loss point, a measure of drought sensitivity, from -0.95 to -0.74 MPa along a gradient of spring snowpack. We also find variation in spring freezing sensitivity with minimum May temperature. However, we find no trade-off, as the climatic gradients shaping these traits are spatially uncorrelated in our study region, despite being negatively correlated across the Sierra Nevada. Species may escape adaptive trade-offs in geographic regions where climate variables are spatially decoupled. These regions may represent valuable reservoirs of heritable adaptive phenotypic variation.

Weak local adaptation to drought in seedlings of a widespread conifer.

Tree seedlings from populations native to drier regions are often assumed to be more drought tolerant than those from wetter provenances. However, intraspecific variation in drought tolerance has not been well-characterized despite being critical for developing climate change mitigation and adaptation strategies, and for predicting the effects of drought on forests. We used a large-scale common garden drought-to-death experiment to assess range-wide variation in drought tolerance, measured by decline of photosynthetic efficiency, growth, and plastic responses to extreme summer drought in seedlings of 73 natural populations of the two main varieties of Douglas-fir (Pseudotsuga menziesii var. menziesii and var. glauca). Local adaptation to drought was weak in var. glauca and nearly absent in menziesii. Var. glauca showed higher tolerance to drought but slower growth than var. menziesii. Clinal variation in drought tolerance and growth species-wide was mainly associated with temperature rather than precipitation. A higher degree of plasticity for growth was observed in var. menziesii in response to extreme drought. Genetic variation for drought tolerance in seedlings within varieties is maintained primarily within populations. Selective breeding within populations may facilitate adaptation to drought more than assisted gene flow.

Genomic data revealed inbreeding despite a geographically connected stable effective population size since the Holocene in the protected Formosan Long-Arm Scarab beetle, Cheirotonus formosanus.

Biodiversity conservation is a top priority in the face of global environmental change, and the practical restoration of biodiversity has emerged as a key objective. Nevertheless, the question of how to effectively contribute to biodiversity restoration and identify suitable systems for such efforts continues to present major challenges. By using genome-wide SNP data, our study revealed that populations from different mountain ranges of the Formosan Long-Arm Scarab beetle, a flagship species that receives strict protection, exhibited a single genetic cluster with no subdivision. Additionally, our result implied an association between the demographic history and historical fluctuations in climate and environmental conditions. Furthermore, we showed that, despite a stable and moderately sized effective population over recent history, all the individuals we studied exhibited signs of genetic inbreeding. We argued that the current practice of protecting the species as one evolutionarily significant unit remains the best conservation plan and that recent habitat change may have led to the pattern of significant inbreeding. We closed by emphasizing the importance of conservation genetic studies in guiding policy decisions and highlighting the potential of genomic data for identifying ideal empirical systems for genetic rescue, or assisted gene flow studies.

Assisted gene flow using cryopreserved sperm in critically endangered coral.

Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao-Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.

Reforestation of high elevation pines: Direct seeding success depends on seed source and sowing environment.

Forest persistence in regions impacted by increasing water and temperature stress will depend upon species' ability to either rapidly adjust to novel conditions or migrate to track ecological niches. Predicted, rapid climate change is likely to outpace the adaptive and migratory capacity of long-lived isolated tree species, and reforestation may be critical to species' persistence. Facilitating persistence both within and beyond a species' range requires identification of seed lots best adapted to the current and future conditions predicted with rapid climate change. We evaluate variation in emergent seedling performance that leads to differential survival among species and populations for three high elevation five-needle pines. We paired a fully reciprocal field common garden experiment with a greenhouse common garden study to (1) quantify variation in seedling emergence and functional traits, (2) ask how functional traits affect performance under different establishment conditions, and (3) evaluate whether trait and performance variation demonstrates local adaptation and plasticity. Among study species-limber, Great Basin bristlecone, and whitebark pines-we found divergence in emergence and functional traits, though soil moisture was the strongest driver of seedling emergence and abundance across all species. Generalist limber pine had a clear emergence advantage as well as traits associated with drought adaptation, while edaphic specialist bristlecone pine was characterized by low emergence yet high early survival once established. Despite evidence for edaphic specialization, soil characteristics alone did not explain bristlecone success. Across species, trait-environment relationships provided some evidence for local adaptation in drought-adapted traits, but we found no evidence of local adaptation in emergence or survival at this early life stage. For managers looking to promote persistence, sourcing seed from drier environments is likely to impart greater drought resistance into reforestation efforts through strategies such as greater root investment, increasing the probability of early seedling survival. This research demonstrates, through a rigorous reciprocal transplant experimental design, that it may be possible to select climate- and soil-appropriate seed sources for reforestation. However, planting success will ultimately rely on a suitable establishment environment, requiring careful consideration of interannual climate variability for management interventions in these climate and disturbance-impacted tree species.

Estimating the potential for coral adaptation to global warming across the Indo-West Pacific.

The potential of reef-building corals to adapt to increasing sea-surface temperatures is often debated but has rarely been comprehensively modeled on a region-wide scale. We used individual-based simulations to model adaptation to warming in a coral metapopulation comprising 680 reefs and representing the whole of the Central Indo-West Pacific. Encouragingly, some reefs-most notably Vietnam, Japan, Taiwan, New Caledonia and the southern half of the Great Barrier Reef-exhibited high capacity for adaptation and, in our model, maintained coral cover even under a rapid "business-as-usual" warming scenario throughout the modeled period (200 years). Higher resilience of these reefs was observed under all tested parameter settings except the models prohibiting selection and/or migration during warming. At the same time, the majority of reefs in the region tended to collapse within the first 100 years of warming. The adaptive potential (odds of maintaining high coral cover) of a given reef could be predicted based on two metrics: the reef's present-day temperature, and the proportion of recruits immigrating from warmer locations. The latter metric explains the most variation in adaptive potential, and significantly correlates with actual coral cover changes observed throughout the region between the 1970s and the early 2000s. These findings will help prioritize coral conservation efforts and plan assisted gene flow interventions to boost the adaptive potential of specific coral populations.

How many and when? Optimising targeted gene flow for a step change in the environment.

Targeted gene flow is an emerging conservation strategy that involves introducing individuals with particular traits to places where these traits are of benefit. One obvious application is to adapt a recipient population to a known threat, but questions remain as to how best to achieve this. Here, we vary timing and size of the introduction to maximise our objective - survival of the recipient population's genome. We explore a generic population model as well as a specific example - the northern quoll, an Australian marsupial predator threatened by the toxic cane toad. We reveal a trade-off between preserving the recipient genome and reducing population extinction risk, but key management levers can often optimise this so that nearly 100% of the recipient population's genome is preserved. Any action was better than none but the size of the benefit was sensitive to outbreeding depression, recombination rate, and the timing and size of the introduction.

Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic.

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self-sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first-generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef-building corals facing a rapidly changing environment.

Targeted gene flow for conservation.

Anthropogenic threats often impose strong selection on affected populations, causing rapid evolutionary responses. Unfortunately, these adaptive responses are rarely harnessed for conservation. We suggest that conservation managers pay close attention to adaptive processes and geographic variation, with an eye to using them for conservation goals. Translocating pre-adapted individuals into recipient populations is currently considered a potentially important management tool in the face of climate change. Targeted gene flow, which involves moving individuals with favorable traits to areas where these traits would have a conservation benefit, could have a much broader application in conservation. Across a species' range there may be long-standing geographic variation in traits or variation may have rapidly developed in response to a threatening process. Targeted gene flow could be used to promote natural resistance to threats to increase species resilience. We suggest that targeted gene flow is a currently underappreciated strategy in conservation that has applications ranging from the management of invasive species and their impacts to controlling the impact and virulence of pathogens.

Planting long-lived trees in a warming climate: Theory shows the importance of stage-dependent climatic tolerance.

Climate change poses a particular threat to long-lived trees, which may not adapt or migrate fast enough to keep up with rising temperatures. Assisted gene flow could facilitate adaptation of populations to future climates by using managed translocation of seeds from a warmer location (provenance) within the current range of a species. Finding the provenance that will perform best in terms of survival or growth is complicated by a trade-off. Because trees face a rapidly changing climate during their long lives, the alleles that confer optimal performance may vary across their lifespan. For instance, trees from warmer provenances could be well adapted as adults but suffer from colder temperatures while juvenile. Here we use a stage-structured model, using both analytical predictions and numerical simulations, to determine which provenance would maximize the survival of a cohort of long-lived trees in a changing climate. We parameterize our simulations using empirically estimated demographic transition matrices for 20 long-lived tree species. Unable to find reliable quantitative estimates of how climatic tolerance changes across stages in these same species, we varied this parameter to study its effect. Both our mathematical model and simulations predict that the best provenance depends strongly on how fast the climate changes and also how climatic tolerance varies across the lifespan of a tree. We thus call for increased empirical efforts to measure how climate tolerance changes over life in long-lived species, as our model suggests that it should strongly influence the best provenance for assisted gene flow.

Small-scale genetic structure of coral populations in Palau based on whole mitochondrial genomes: Implications for future coral resilience.

The ability of local populations to adapt to future climate conditions is facilitated by a balance between short range dispersal allowing local buildup of adaptively beneficial alleles, and longer dispersal moving these alleles throughout the species range. Reef building corals have relatively low dispersal larvae, but most population genetic studies show differentiation only over 100s of km. Here, we report full mitochondrial genome sequences from 284 tabletop corals (Acropora hyacinthus) from 39 patch reefs in Palau, and show two signals of genetic structure across reef scales from 1 to 55 km. First, divergent mitochondrial DNA haplotypes exist in different proportions from reef to reef, causing PhiST values of 0.02 (p = 0.02). Second, closely related sequences of mitochondrial Haplogroups are more likely to be co-located on the same reefs than expected by chance alone. We also compared these sequences to prior data on 155 colonies from American Samoa. In these comparisons, many Haplogroups in Palau were disproportionately represented or absent in American Samoa, and inter-regional PhiST = 0.259. However, we saw three instances of identical mitochondrial genomes between locations. Together, these data sets suggest two features of coral dispersal revealed by occurrence patterns in highly similar mitochondrial genomes. First, the Palau-American Samoa data suggest that long distance dispersal in corals is rare, as expected, but that it is common enough to deliver identical mitochondrial genomes across the Pacific. Second, higher than expected co-occurrence of Haplogroups on the same Palau reefs suggests greater retention of coral larvae on local reefs than predicted by many current oceanographic models of larval movement. Increased attention to local scales of coral genetic structure, dispersal, and selection may help increase the accuracy of models of future adaptation of corals and of assisted migration as a reef resilience intervention.

Facilitated Adaptation as A Conservation Tool in the Present Climate Change Context: A Methodological Guide.

Climate change poses a novel threat to biodiversity that urgently requires the development of adequate conservation strategies. Living organisms respond to environmental change by migrating to locations where their ecological niche is preserved or by adapting to the new environment. While the first response has been used to develop, discuss and implement the strategy of assisted migration, facilitated adaptation is only beginning to be considered as a potential approach. Here, we present a review of the conceptual framework for facilitated adaptation, integrating advances and methodologies from different disciplines. Briefly, facilitated adaptation involves a population reinforcement that introduces beneficial alleles to enable the evolutionary adaptation of a focal population to pressing environmental conditions. To this purpose, we propose two methodological approaches. The first one (called pre-existing adaptation approach) is based on using pre-adapted genotypes existing in the focal population, in other populations, or even in closely related species. The second approach (called de novo adaptation approach) aims to generate new pre-adapted genotypes from the diversity present in the species through artificial selection. For each approach, we present a stage-by-stage procedure, with some techniques that can be used for its implementation. The associated risks and difficulties of each approach are also discussed.

Applying genomics in assisted migration under climate change: Framework, empirical applications, and case studies.

The rate of global climate change is projected to outpace the ability of many natural populations and species to adapt. Assisted migration (AM), which is defined as the managed movement of climate-adapted individuals within or outside the species ranges, is a conservation option to improve species' adaptive capacity and facilitate persistence. Although conservation biologists have long been using genetic tools to increase or maintain diversity of natural populations, genomic techniques could add extra benefit in AM that include selectively neutral and adaptive regions of the genome. In this review, we first propose a framework along with detailed procedures to aid collaboration among scientists, agencies, and local and regional managers during the decision-making process of genomics-guided AM. We then summarize the genomic approaches for applying AM, followed by a literature search of existing incorporation of genomics in AM across taxa. Our literature search initially identified 729 publications, but after filtering returned only 50 empirical studies that were either directly applied or considered genomics in AM related to climate change across taxa of plants, terrestrial animals, and aquatic animals; 42 studies were in plants. This demonstrated limited application of genomic methods in AM in organisms other than plants, so we provide further case studies as two examples to demonstrate the negative impact of climate change on non-model species and how genomics could be applied in AM. With the rapidly developing sequencing technology and accumulating genomic data, we expect to see more successful applications of genomics in AM, and more broadly, in the conservation of biodiversity.

Do marginal plant populations enhance the fitness of larger core units under ongoing climate change? Empirical insights from a rare carnation.

Assisted gene flow (AGF) can restore fitness in small plant populations. Due to climate change, current fitness patterns could vary in the future ecological scenario, as highly performant lineages can undergo maladaptation under the new climatic contexts. Peripheral populations have been argued to represent a potential source of species adaptation against climate change, but experimental evidence is poor. This paper considers the consequences of within- and between-population mating between a large core population and the southernmost population, the rare Dianthus guliae, to evaluate optimal AGF design under current and future conditions. We performed experimental self-pollinations and within- and between-population cross-pollinations to generate seed material and test its adaptive value to aridity. Seed germination, seedling growth and survival were measured under current and expected aridity. Effects of population type, pollination treatment and stress treatment on fitness components were analysed by generalized linear models. Relative measures of inbreeding depression and heterosis were taken under different stress treatments. Self-pollination reduced fitness for all the considered traits compared to within- and between-population cross-pollination. Under current aridity regime, the core population expressed higher fitness, and a larger magnitude of inbreeding depression. This indicated the core unit is close to its fitness optimum and could allow for restoring the fitness of the small peripheral population. Contrarily, under increased aridity, the fitness of outbred core lineages decreased, suggesting the rise of maladaptation. In this scenario, AGF from the small peripheral population enhanced the fitness of the core unit, whereas AGF from the core population promoted a fitness loss in the peripheral population. Hence, the small peripheral population could improve fitness of large core units versus climate change, while the contrary could be not true. Integrating reciprocal breeding programmes and fitness analyses under current and predicted ecological conditions can support optimal AGF design in a long-term perspective.

Evaluating genomic data for management of local adaptation in a changing climate: A lodgepole pine case study.

We evaluate genomic data, relative to phenotypic and climatic data, as a basis for assisted gene flow and genetic conservation. Using a seedling common garden trial of 281 lodgepole pine (Pinus contorta) populations from across western Canada, we compare genomic data to phenotypic and climatic data to assess their effectiveness in characterizing the climatic drivers and spatial scale of local adaptation in this species. We find that phenotype-associated loci are equivalent or slightly superior to climate data for describing local adaptation in seedling traits, but that climate data are superior to genomic data that have not been selected for phenotypic associations. We also find agreement between the climate variables associated with genomic variation and with 20-year heights from a long-term provenance trial, suggesting that genomic data may be a viable option for identifying climatic drivers of local adaptation where phenotypic data are unavailable. Genetic clines associated with the experimental traits occur at broad spatial scales, suggesting that standing variation of adaptive alleles for this and similar species does not require management at scales finer than those indicated by phenotypic data. This study demonstrates that genomic data are most useful when paired with phenotypic data, but can also fill some of the traditional roles of phenotypic data in management of species for which phenotypic trials are not feasible.

Modern Strategies to Assess and Breed Forest Tree Adaptation to Changing Climate.

Studying the genetics of adaptation to new environments in ecologically and industrially important tree species is currently a major research line in the fields of plant science and genetic improvement for tolerance to abiotic stress. Specifically, exploring the genomic basis of local adaptation is imperative for assessing the conditions under which trees will successfully adapt in situ to global climate change. However, this knowledge has scarcely been used in conservation and forest tree improvement because woody perennials face major research limitations such as their outcrossing reproductive systems, long juvenile phase, and huge genome sizes. Therefore, in this review we discuss predictive genomic approaches that promise increasing adaptive selection accuracy and shortening generation intervals. They may also assist the detection of novel allelic variants from tree germplasm, and disclose the genomic potential of adaptation to different environments. For instance, natural populations of tree species invite using tools from the population genomics field to study the signatures of local adaptation. Conventional genetic markers and whole genome sequencing both help identifying genes and markers that diverge between local populations more than expected under neutrality, and that exhibit unique signatures of diversity indicative of "selective sweeps." Ultimately, these efforts inform the conservation and breeding status capable of pivoting forest health, ecosystem services, and sustainable production. Key long-term perspectives include understanding how trees' phylogeographic history may affect the adaptive relevant genetic variation available for adaptation to environmental change. Encouraging "big data" approaches (machine learning-ML) capable of comprehensively merging heterogeneous genomic and ecological datasets is becoming imperative, too.

Forest genomics: Advancing climate adaptation, forest health, productivity, and conservation.

Forest ecosystems provide important ecological services and resources, from habitat for biodiversity to the production of environmentally friendly products, and play a key role in the global carbon cycle. Humanity is counting on forests to sequester and store a substantial portion of the anthropogenic carbon dioxide produced globally. However, the unprecedented rate of climate change, deforestation, and accidental importation of invasive insects and diseases are threatening the health and productivity of forests, and their capacity to provide these services. Knowledge of genetic diversity, local adaptation, and genetic control of key traits is required to predict the adaptive capacity of tree populations, inform forest management and conservation decisions, and improve breeding for productive trees that will withstand the challenges of the 21st century. Genomic approaches have well accelerated the generation of knowledge of the genetic and evolutionary underpinnings of nonmodel tree species, and advanced their applications to address these challenges. This special issue of Evolutionary Applications features 14 papers that demonstrate the value of a wide range of genomic approaches that can be used to better understand the biology of forest trees, including species that are widespread and managed for timber production, and others that are threatened or endangered, or serve important ecological roles. We highlight some of the major advances, ranging from understanding the evolution of genomes since the period when gymnosperms separated from angiosperms 300 million years ago to using genomic selection to accelerate breeding for tree health and productivity. We also discuss some of the challenges and future directions for applying genomic tools to address long-standing questions about forest trees.

Genomic assessment of local adaptation in dwarf birch to inform assisted gene flow.

When populations of a rare species are small, isolated and declining under climate change, some populations may become locally maladapted. Detecting this maladaptation may allow effective rapid conservation interventions, even if based on incomplete knowledge. Population maladaptation may be estimated by finding genome-environment associations (GEA) between allele frequencies and environmental variables across a local species range, and identifying populations whose allele frequencies do not fit with these trends. We can then design assisted gene flow strategies for maladapted populations, to adjust their allele frequencies, entailing lower levels of intervention than with undirected conservation action. Here, we investigate this strategy in Scottish populations of the montane plant dwarf birch (Betula nana). In genome-wide restriction site-associated single nucleotide polymorphism (SNP) data, we found 267 significant associations between SNP loci and environmental variables. We ranked populations by maladaptation estimated using allele frequency deviation from the general trends at these loci; this gave a different prioritization for conservation action than the Shapely Index, which seeks to preserve rare neutral variation. Populations estimated to be maladapted in their allele frequencies at loci associated with annual mean temperature were found to have reduced catkin production. Using an environmental niche modelling (ENM) approach, we found annual mean temperature (35%), and mean diurnal range (15%), to be important predictors of the dwarf birch distribution. Intriguingly, there was a significant correlation between the number of loci associated with each environmental variable in the GEA and the importance of that variable in the ENM. Together, these results suggest that the same environmental variables determine both adaptive genetic variation and species range in Scottish dwarf birch. We suggest an assisted gene flow strategy that aims to maximize the local adaptation of dwarf birch populations under climate change by matching allele frequencies to current and future environments.

Estimating the impact of divergent mating phenology between residents and migrants on the potential for gene flow.

Gene flow between populations can allow the spread of beneficial alleles and genetic diversity between populations, with importance to conservation, invasion biology, and agriculture. Levels of gene flow between populations vary not only with distance, but also with divergence in reproductive phenology. Since phenology is often locally adapted, arriving migrants may be reproductively out of synch with residents, which can depress realized gene flow. In flowering plants, the potential impact of phenological divergence on hybridization between populations can be predicted from overlap in flowering schedules-the daily count of flowers capable of pollen exchange-between a resident and migrant population. The accuracy of this prospective hybridization estimate, based on parental phenotypes, rests upon the assumptions of unbiased pollen transfer between resident and migrant active flowers. We tested the impact of phenological divergence on resident-migrant mating frequencies in experiments that mimicked a single large gene flow event. We first prospectively estimated mating frequencies two lines of Brassica rapaselected or early and late flowering. We then estimated realized mating frequencies retrospectively through progeny testing. The two estimates strongly agreed in a greenhouse experiment, where procedures ensured saturating, unbiased pollination. Under natural pollination in the field, the rate of resident-migrant mating, was lower than estimated by phenological divergence alone, although prospective and retrospective estimates were correlated. In both experiments, differences between residents and migrants in flowering schedule shape led to asymmetric hybridization. Results suggest that a prospective estimate of hybridization based on mating schedules can be a useful, although imperfect, tool for evaluating potential gene flow. They also illustrate the impact of mating phenology on the magnitude and symmetry of reproductive isolation.

Assessing the potential for assisted gene flow using past introduction of Norway spruce in southern Sweden: Local adaptation and genetic basis of quantitative traits in trees.

Norway spruce (Picea abies) is a dominant conifer species of major economic importance in northern Europe. Extensive breeding programs were established to improve phenotypic traits of economic interest. In southern Sweden, seeds used to create progeny tests were collected on about 3,000 trees of outstanding phenotype ('plus' trees) across the region. In a companion paper, we showed that some were of local origin but many were recent introductions from the rest of the natural range. The mixed origin of the trees together with partial sequencing of the exome of >1,500 of these trees and phenotypic data retrieved from the Swedish breeding program offered a unique opportunity to dissect the genetic basis of local adaptation of three quantitative traits (height, diameter and bud-burst) and assess the potential of assisted gene flow. Through a combination of multivariate analyses and genome-wide association studies, we showed that there was a very strong effect of geographical origin on growth (height and diameter) and phenology (bud-burst) with trees from southern origins outperforming local provenances. Association studies revealed that growth traits were highly polygenic and bud-burst somewhat less. Hence, our results suggest that assisted gene flow and genomic selection approaches could help to alleviate the effect of climate change on P. abies breeding programs in Sweden.