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Future climate change has been predicted to disrupt local adaptation in many perennial plants, such as forest trees, but the magnitude and location of these effects are thus far poorly understood. Here, we assess local adaptation to current climate in European aspen (Populus tremula) by using environmental association analyses to identify genetic variants associated with two representative climate variables describing current day variation in temperature and precipitation. We also analysed patterns of genetic differentiation between southern and northern populations and observe that regions of high genetic differentiation are enriched for SNPs that are significantly associated with climate. Using variants associated with climate, we examined patterns of isolation by distance and environment and used spatial modelling to predict the geographic distribution of genomic variation in response to two scenarios of future climate change. We show that climate conditions at a northern reference site will correspond to climate conditions experienced by current day populations located 4–8 latitude degrees further south. By assessing the relationship between phenotypic traits and vegetative fitness, we also demonstrate that southern populations harbour genetic variation that likely would be adaptive further north under both climate change scenarios. Current day populations at the lagging edge of the distribution in Sweden can therefore serve as sources for introducing adaptive alleles onto northern populations, but the likelihood of this largely depends on naturally occurring levels of gene flow.

Although hundreds of plant lineages have independently evolved dioecy (that is, separation of the sexes), the underlying genetic basis remains largely elusive 1 . Here we show that diverse poplar species carry partial duplicates of the ARABIDOPSIS RESPONSE REGULATOR 17 ( ARR17 ) orthologue in the male-specific region of the Y chromosome. These duplicates give rise to small RNAs apparently causing male-specific DNA methylation and silencing of the ARR17 gene. CRISPR–Cas9-induced mutations demonstrate that ARR17 functions as a sex switch, triggering female development when on and male development when off. Despite repeated turnover events, including a transition from the XY system to a ZW system, the sex-specific regulation of ARR17 is conserved across the poplar genus and probably beyond. Our data reveal how a single-gene-based mechanism of dioecy can enable highly dynamic sex-linked regions and contribute to maintaining recombination and integrity of sex chromosomes. Populus has young sex chromosomes despite ancient dioecy. This study shows that the ARR17 gene functions as a sex switch, triggering female development when on and male development when off. This single-gene system enables dynamic evolution of poplar sex chromosomes.

Genetic diversity is a key prerequisite for adaptation to changing environments. Maintaining genetic diversity in forest trees is crucial amid climate change, given their long generation times. Forest management practices can affect the genetic diversity of forest ecosystems through selective felling or reforestation strategies following harvests. To assess how managed forests respond to climate‐driven changes, we investigated patterns of genetic diversity and local adaptation by contrasting old‐growth and recently planted stands of Norway spruce (Picea abies). We assess both neutral and adaptive genetic variation by sequencing pooled samples collected from 45 first stands across northern Sweden. Our results reveal no significant differences in overall genetic diversity between natural and planted populations, indicating that current forest management practices have not substantially reduced genetic variation. Analyses of adaptive variation demonstrate strong signatures of local adaptation in old‐growth populations, with clear correlations between genetic and environmental distances. In contrast, planted stands show weaker adaptive signals and are also at greater risk of non‐adaptiveness under future climate scenarios. While current forest management practices preserve much of the neutral genetic diversity necessary for long‐term forest health, our findings highlight the importance of conserving and promoting adaptive genetic variation available in old‐growth stands to ensure resilience against ongoing climate change.

The demographical history of France remains largely understudied despite its central role toward understanding modern population structure across Western Europe. Here, by exploring publicly available Europe-wide genotype datasets together with the genomes of 3234 present-day and six newly sequenced medieval individuals from Northern France, we found extensive fine-scale population structure across Brittany and the downstream Loire basin and increased population differentiation between the northern and southern sides of the river Loire, associated with higher proportions of steppe vs. Neolithic-related ancestry. We also found increased allele sharing between individuals from Western Brittany and those associated with the Bell Beaker complex. Our results emphasise the need for investigating local populations to better understand the distribution of rare (putatively deleterious) variants across space and the importance of common genetic legacy in understanding the sharing of disease-related alleles between Brittany and people from western Britain and Ireland.

With the rapid advancement of high throughput sequencing, large numbers of genetic markers can be readily and cheaply acquired, but most current software packages for genetic map construction cannot handle such dense input. Modern computer architectures and server farms represent untapped resources that can be used to enable higher marker densities to be processed in tractable time. Here we present a pipeline using a modified version of OneMap that parallelizes over bottleneck functions and achieves substantial speedups for producing a high density linkage map (N = 20,000). Using simulated data we show that the outcome is as accurate as the traditional pipeline. We further demonstrate that there is a direct relationship between the number of markers used and the level of deviation between true and estimated order, which in turn impacts the final size of a genetic map.

Intraspecific genetic variation in foundation species such as aspen ( Populus tremuloides Michx.) shapes their impact on forest structure and function. Identifying genes underlying ecologically important traits is key to understanding that impact. Previous studies, using single‐locus genome‐wide association (GWA) analyses to identify candidate genes, have identified fewer genes than anticipated for highly heritable quantitative traits. Mounting evidence suggests that polygenic control of quantitative traits is largely responsible for this “missing heritability” phenomenon. Our research characterized the genetic architecture of 30 ecologically important traits using a common garden of aspen through genomic and transcriptomic analyses. A multilocus association model revealed that most traits displayed a highly polygenic architecture, with most variation explained by loci with small effects (likely below the detection levels of single‐locus GWA methods). Consistent with a polygenic architecture, our single‐locus GWA analyses found only 38 significant SNPs in 22 genes across 15 traits. Next, we used differential expression analysis on a subset of aspen genets with divergent concentrations of salicinoid phenolic glycosides (key defense traits). This complementary method to traditional GWA discovered 1243 differentially expressed genes for a polygenic trait. Soft clustering analysis revealed three gene clusters (241 candidate genes) involved in secondary metabolite biosynthesis and regulation. Our work reveals that ecologically important traits governing higher‐order community‐ and ecosystem‐level attributes of a foundation forest tree species have complex underlying genetic structures and will require methods beyond traditional GWA analyses to unravel.

The rate of meiotic recombination is one of the central factors determining genome-wide levels of linkage disequilibrium which has important consequences for the efficiency of natural selection and for the dissection of quantitative traits. Here we present a new, high-resolution linkage map for Populus tremula that we use to anchor approximately two thirds of the P. tremula draft genome assembly on to the expected 19 chromosomes, providing us with the first chromosome-scale assembly for P. tremula (Table 2). We then use this resource to estimate variation in recombination rates across the P. tremula genome and compare these results to recombination rates based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with a number of genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identifies a number of genomic regions with very high recombination rates that the map-based method fails to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome. Recombination rates are positively correlated with gene density and negatively correlated with repeat density and methylation levels, suggesting that recombination is largely directed toward gene regions in P. tremula.

Norway spruce (Picea abies (L.) Karst.) is a conifer species of substanital economic and ecological importance. In common with most conifers, the P. abies genome is very large (∼20 Gbp) and contains a high fraction of repetitive DNA. The current P. abies genome assembly (v1.0) covers approximately 60% of the total genome size but is highly fragmented, consisting of >10 million scaffolds. The genome annotation contains 66,632 gene models that are at least partially validated (www.congenie.org), however, the fragmented nature of the assembly means that there is currently little information available on how these genes are physically distributed over the 12 P. abies chromosomes. By creating an ultra-dense genetic linkage map, we anchored and ordered scaffolds into linkage groups, which complements the fine-scale information available in assembly contigs. Our ultra-dense haploid consensus genetic map consists of 21,056 markers derived from 14,336 scaffolds that contain 17,079 gene models (25.6% of the validated gene models) that we have anchored to the 12 linkage groups. We used data from three independent component maps, as well as comparisons with previously published Picea maps to evaluate the accuracy and marker ordering of the linkage groups. We demonstrate that approximately 3.8% of the anchored scaffolds and 1.6% of the gene models covered by the consensus map have likely assembly errors as they contain genetic markers that map to different regions within or between linkage groups. We further evaluate the utility of the genetic map for the conifer research community by using an independent data set of unrelated individuals to assess genome-wide variation in genetic diversity using the genomic regions anchored to linkage groups. The results show that our map is sufficiently dense to enable detailed evolutionary analyses across the P. abies genome.

Owing to their long life span and ecological dominance in many communities, forest trees are subject to attack from a diverse array of herbivores throughout their range, and have therefore developed a large number of both constitutive and inducible defenses. We used molecular population genetics methods to examine the evolution of eight genes in European aspen, Populus tremula, that are all associated with defensive responses against pests and/or pathogens, and have earlier been shown to become strongly up-regulated in poplars as a response to wounding and insect herbivory. Our results show that the majority of these defense genes show patterns of intraspecific polymorphism and site-frequency spectra that are consistent with a neutral model of evolution. However, two of the genes, both belonging to a small gene family of polyphenol oxidases, show multiple deviations from the neutral model. The gene PPO1 has a 600 bp region with a highly elevated K(A)/K(S) ratio and reduced synonymous diversity. PPO1 also shows a skew toward intermediate frequency variants in the SFS, and a pronounced fixation of non-synonymous mutations, all pointing to the fact that PPO1 has been subjected to recurrent selective sweeps. The gene PPO2 shows a marked excess of high frequency, derived variants and shows many of the same trends as PPO1 does, even though the pattern is less pronounced, suggesting that PPO2 might have been the target of a recent selective sweep. Our results supports data from both Populus and other species which have found that the the majority of defense-associated genes show few signs of selection but that a number of genes involved in mediating defense against herbivores show signs of adaptive evolution.

With the rapid advancement of high throughput sequencing, large numbers of genetic markers can be readily and cheaply acquired, but most current software packages for genetic map construction cannot handle such dense input. Modern computer architectures and server farms represent untapped resources that can be used to enable higher marker densities to be processed in tractable time. Here we present a pipeline using a modified version of OneMap that parallelizes over bottleneck functions and achieves substantial speedups for producing a high density linkage map (N = 20,000). Using simulated data we show that the outcome is as accurate as the traditional pipeline. We further demonstrate that there is a direct relationship between the number of markers used and the level of deviation between true and estimated order, which in turn impacts the final size of a genetic map.