Gene copy number variations involved in balsam poplar (Populus balsamifera L.) adaptive variations

Gene copy number variations (CNVs) involved in phenotypic variations have already been shown in plants, but genomewide testing of CNVs for adaptive variation was not doable until recent technological developments. Thus, reports of the genomic architecture of adaptation involving CNVs remain scarce to date. Here, we investigated F₁ progenies of an intraprovenance cross (north–north cross, 58th parallel) and an interprovenances cross (north–south cross, 58th/49th parallels) for CNVs using comparative genomic hybridization on arrays of probes targeting gene sequences in balsam poplar (Populus balsamifera L.), a widespread North American forest tree. A total of 1,721 genes were found in varying copy numbers over the set of 19,823 tested genes. These gene CNVs presented an estimated average size of 8.3 kb and were distributed over poplar's 19 chromosomes including 22 hotspot regions. Gene CNVs number was higher for the interprovenance progeny in accordance with an expected higher genetic diversity related to the composite origin of this family. Regression analyses between gene CNVs and seven adaptive trait variations resulted in 23 significant links; among these adaptive gene CNVs, 30% were located in hotspots. One‐to‐five gene CNVs were found related to each of the measured adaptive traits and annotated for both biotic and abiotic stress responses. These annotations can be related to the occurrence of a higher pathogenic pressure in the southern parts of balsam poplar's distribution, and higher photosynthetic assimilation rates and water‐use efficiency at high latitudes. Overall, our findings suggest that gene CNVs typically having higher mutation rates than SNPs may in fact represent efficient adaptive variations against fast‐evolving pathogens.     

Timing of photoperiodic competency causes phenological mismatch in balsam poplar (Populus balsamifera L.)

Plant phenology is expected to be sensitive to climate warming. In boreal trees, spring flush is primarily temperature driven, whereas height growth cessation and autumn leaf senescence are predominantly controlled by photoperiod. Cuttings of 525 genotypes from the full range of balsam poplar were planted into two common gardens (Vancouver and Indian Head, Canada) at similar latitudes, but with differing winter temperatures and growing seasons. There was clinal variation in spring and, particularly, summer and fall phenology. Bud flush and, despite milder climate, bud set and leaf drop were earlier at Vancouver than at Indian Head by 44, 28 and 7 d, respectively. Although newly flushed growth is insensitive to photoperiod, many genotypes at both sites became competent before the summer solstice. At Vancouver, high‐latitude genotypes set dormant terminal buds in mid‐spring. Most other genotypes grew until midsummer or set bud temporarily and then experienced a second flush. In both gardens and in a growth chamber experiment, earlier bud set was associated with reduced height growth and higher root/shoot ratios. Shoots attained competency ～5 weeks after flushing, which would normally prevent dormancy induction before the solstice, but may be insufficient if spring advances by more than a few weeks.     

Clonal constitution and sex ratio in northern populations of balsam poplar Populus balsamifera

Isozyme analyses performed on balsam poplar stands in subarctic northern Québec indicated polyclonal predominance (76%). This suggests that seed sources were adequate for colonization of new habitats. High variance at the clone and the stand levels did not permit, however, the use of morphological traits for clonal partitioning. A non-random sex distribution related to habitat conditions was found both at the regional and the local scales, although there is an equal male-female ratio in the study area. Female stands predominate in regions subject to a maritime climate (1:5) and in fertile and humid habitats (1:7).     

Genetic consequences of glacial survival: the late Quaternary history of balsam poplar (Populus balsamifera L.) in North America

Aim Beringia, the unglaciated region encompassing the former Bering land bridge, as well as the land between the Lena and Mackenzie rivers, is recognized as an important refugium for arctic plants during the last ice age. Compelling palaeobotanical evidence also supports the presence of small populations of boreal trees within Beringia during the Last Glacial Maximum. The occurrence of balsam poplar (Populus balsamifera) in Beringia provides a unique opportunity to assess the implications of persistence in a refugium on present‐day genetic diversity for this boreal tree species. Location North America. Methods We sequenced three variable non‐coding regions of the chloroplast genome (cpDNA) from 40 widely distributed populations of balsam poplar across its North American range. We assessed patterns of genetic diversity, geographic structure and historical demography between glaciated and unglaciated regions of the balsam poplar’s range. We also utilized a coalescent model to test for divergence between regions. Results Levels of genetic diversity were consistently greater for populations at the southern margin (θ_W = 0.00122) than in the central (θ_W = 0.00086) or northern (θ_W = 0.00034) regions of the current distribution of balsam poplar, and diversity decreased with increasing latitude (R² = 0.49, P < 0.01). We detected low, but significant, structure (F_CT = 0.05, P = 0.05), among regions of P. balsamifera’s distribution. The cpDNA genealogy was shallow, however, showing an absence of highly differentiated chloroplast haplotypes. Coalescent analyses supported a model of divergence between the southern ice margin and the northern unglaciated region of balsam poplar’s distribution, but analyses of other regional comparisons did not converge. Main conclusions The palaeobotanical record supports the presence of a Beringian refugium for balsam poplar, but we were unable to definitively identify the presence of known refugial populations based on genetic data alone. Balsam poplar populations from Beringia are not a significant reservoir of cpDNA diversity today. Unique alleles that may have been present in the small, isolated populations that survived within Beringia were probably lost through genetic drift or swamped by post‐glacial, northward migration from populations south of the ice sheets.     

Temperature shapes liana diversity pattern along a latitudinal gradient in southern temperate rainforest

Plant Ecology - The decrease in liana diversity with increasing latitude has been indicated as the major physiognomic difference between tropical and temperate forests’ ecosystem. Despite the...     

Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.)

In outdoor common gardens, high latitude populations of deciduous tree species often display higher assimilation rates ( A ) than low latitude populations, but they accomplish less height. To test whether trends in A reflect adaptation to growing season length or, alternatively, are garden growth artefacts, we examined variation in height increment and ecophysiological traits in a range-wide collection of Populus balsamifera L. populations from 21 provenances, during unconstrained growth in a greenhouse. Rooted cuttings, maintained without resource limitation under 21 h photoperiod for 90 d, displayed increasing height growth, A , leaf mass per area and leaf N per area with latitude whereas stomatal conductance ( g _s) showed no pattern. Water-use efficiency as indicated by both gas exchange and δ ¹³C increased with latitude, whereas photosynthetic nitrogen-use efficiency decreased. Differences in δ ¹³C were less than expected based on A/g _s, suggesting coextensive variation in internal conductance ( g _m). Analysis of A – C _i curves on a subset of populations showed that high latitude genotypes had greater g _m than low-latitude genotypes. We conclude that higher peak rates of height growth in high latitude genotypes of balsam poplar are supported by higher A , achieved partly through higher g _m, to help compensate for a shorter growing season.     

Local Adaptation in the Flowering-Time Gene Network of Balsam Poplar, Populus balsamifera L

Identifying the signature and targets of local adaptation is an increasingly important goal in empirical population genetics. Using data from 443 balsam poplar Populus balsamifera trees sampled from 31 populations, we tested for evidence of geographically variable selection shaping diversity at 27 homologues of the Arabidopsis flowering-time network. These genes are implicated in the control of seasonal phenology, an important determinant of fitness. Using 335 candidate and 412 reference single nucleotide polymorphisms (SNPs), we tested for evidence of local adaptation by searching for elevated population differentiation using F(ST)-based outlier analyses implemented in BayeScan or a Hierarchical Model in Arelquin and by testing for significant associations between allele frequency and environmental variables using BAYENV. A total of 46 SNPs from 14 candidate genes had signatures of local adaptation-either significantly greater population differentiation or significant covariance with one or more environmental variable relative to reference SNP distributions. Only 11 SNPs from two genes exhibited both elevated population differentiation and covariance with one or more environmental variables. Several genes including the abscisic acid gene ABI1B and the circadian clock genes ELF3 and GI5 harbored a large number of SNPs with signatures of local adaptation-with SNPs in GI5 strongly covarying with both latitude and precipitation and SNPs in ABI1B strongly covarying with temperature. In contrast to several other systems, we find little evidence that photoreceptors, including phytochromes, play an important role in local adaptation. Our results additionally show that detecting local adaptation is sensitive to the analytical approaches used and that model-based significance thresholds should be viewed with caution.     

Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods

Temperate forest tree species that span large geographical areas and climatic gradients often have high levels of genetic variation. Such species are ideal for testing how neutral demographic factors and climate‐driven selection structure genetic variation within species, and how this genetic variation can affect ecological communities. Here, we quantified genetic variation in vegetative phenology and growth traits in narrowleaf cottonwood, Populus angustifolia, using three common gardens planted with genotypes originating from source populations spanning the species' range along the Rocky Mountains of North America (ca. 1700 km). We present three main findings. First, we found strong evidence of divergent selection (Q_ST > F_ST) on fall phenology (bud set) with adaptive consequences for frost avoidance. We also found evidence for selection on bud flush duration, tree height, and basal diameter, resulting in population differentiation. Second, we found strong associations with climate variables that were strongly correlated with latitude of origin. More strongly differentiated traits also showed stronger climate correlations, which emphasizes the role that climate has played in divergent selection throughout the range. We found population × garden interaction effects; for some traits, this accounted for more of the variance than either factor alone. Tree height was influenced by the difference in climate of the source and garden locations and declined with increasing transfer distance. Third, growth traits were correlated with dependent arthropod community diversity metrics. Synthesis. Overall, we conclude that climate has influenced genetic variation and structure in phenology and growth traits and leads to local adaptation in P. angustifolia, which can then impact dependent arthropod species. Importantly, relocation of genotypes far northward or southward often resulted in poor growth, likely due to a phenological mismatch with photoperiod, the proximate cue for fall growth cessation. Genotypes moved too far southward suffer from early growth cessation, whereas those moved too far northward are prone to fall frost and winter dieback. In the face of current and forecasted climate change, habitat restoration, forestry, and tree breeding efforts should utilize these findings to better match latitudinal and climatic source environments with management locations for optimal future outcomes.     

Temporal dynamics within a contemporary latitudinal diversity gradient

Poleward declines in species diversity [latitudinal diversity gradients (LDG)] remain among the oldest and most widespread of macroecological patterns. However, their contemporary dynamics remain largely unexplored even though changing ecological conditions, including global change, may modify LDG and their respective ecosystems. Here, we examine temporal variation within a temperate Northwest Atlantic LDG using 31 years of annual fisheries-independent surveys and explore its dynamics in relation to a dominant climate signal [the wintertime North Atlantic Oscillation (NAO)] that varies interannually and alters the latitudinal gradient of Northwest Atlantic continental shelf bottom water temperatures. We found that the slopes of the annual LDG vary dramatically due to changes in geographic distributions of 100+ species, variations that are concealed within the cumulative, static LDG. These changes are strongly associated with changes in NAO sign and strength. This is the first illustration of temporal dynamics in a contemporary LDG and the first demonstration of the speed at which local environmental variations can alter an LDG. Our findings underscore the need to investigate factors that modify LDG separately from those that contribute to their origins.     

Root hydraulic properties and growth of balsam poplar (Populus balsamifera) mycorrhizal with Hebeloma crustuliniforme and Wilcoxina mikolae var. mikolae

The effects of an E-strain fungus (Wilcoxina mikolae var. mikolae) and an ectomycorrhizal fungus (Hebeloma crustuliniforme) on growth and water relations of balsam poplar were examined and compared in the present study. Balsam poplar roots inoculated with W. mikolae var. mikolae (Wm) exhibited structures consistent with ectendomycorrhizal (EEM) associations, including a mantle surrounding the outside of the root and an extensive Hartig net that was located between cortical cells and extended to the vascular cylinder. Roots colonized with H. crustuliniforme (Hc) developed a mantle layer, indicative of an ectomycorrhizal (ECM) association, around the outer part of the root, but no distinct Hartig net was present. Wm-colonized balsam poplar also showed increased shoot growth, stomatal conductance (g _s), and root volumes compared with non-inoculated and Hc-inoculated plants. However, Hc-inoculated plants had higher root hydraulic conductivity (L _pr) compared with non-inoculated plants and Wm-inoculated plants. These results suggest that L _pr was not a growth-limiting factor in balsam poplar and that hyphal penetration of the root cortex in itself may have little influence on root hydraulic properties.     

Scale and direction of adaptive introgression between black cottonwood (Populus trichocarpa) and balsam poplar (P. balsamifera)

Introgression can introduce novel genetic variation at a faster rate than mutation alone and result in adaptive introgression when adaptive alleles are maintained in the recipient genome over time by natural selection. A previous study from our group demonstrated adaptive introgression from Populus balsamifera into P. trichocarpa in a target genomic region. Here we expand our local ancestry analysis to the whole genome of both parents to provide a comprehensive view of introgression patterns and to identify additional candidate regions for adaptive introgression genomewide. Populus trichocarpa is a large, fast‐growing tree of mild coastal regions of the Pacific Northwest, whereas P. balsamifera is a smaller stature tree of continental and boreal regions with intense winter cold. The species hybridize where they are parapatric. We detected asymmetric patterns of introgression across the whole genome of these two poplar species adapted to contrasting environments, with stronger introgression from P. balsamifera to P. trichocarpa than vice versa. Admixed P. trichocarpa individuals contained more genomic regions with unusually high levels of introgression (19 regions) and also the largest introgressed genome fragment (1.02 Mb) compared with admixed P. balsamifera (nine regions). Our analysis also revealed numerous candidate regions for adaptive introgression with strong signals of selection, notably related to disease resistance, and enriched for genes that may play crucial roles in survival and adaptation. Furthermore, we detected a potential overrepresentation of subtelomeric regions in P. balsamifera introgressed into P. trichocarpa and possible protection of sex‐determining regions from interspecific gene flow.     

Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits

A correct timing of growth cessation and dormancy induction represents a critical ecological and evolutionary trade-off between survival and growth in most forest trees (Rehfeldt et al. 1999; Horvath et al. 2003; Howe et al. 2003). We have studied the deciduous tree European Aspen (Populus tremula) across a latitudinal gradient and compared genetic differentiation in phenology traits with molecular markers. Trees from 12 different areas covering 10 latitudinal degrees were cloned and planted in two common gardens. Several phenology traits showed strong genetic differentiation and clinal variation across the latitudinal gradient, with Q(ST) values generally exceeding 0.5. This is in stark contrast to genetic differentiation at several classes of genetic markers (18 neutral SSRs, 7 SSRs located close to phenology candidate genes and 50 SNPs from five phenology candidate genes) that all showed F(ST) values around 0.015. We thus find strong evidence for adaptive divergence in phenology traits across the latitudinal gradient. However, the strong population structure seen at the quantitative traits is not reflected in underlying candidate genes. This result fit theoretical expectations that suggest that genetic differentiation at candidate loci is better described by F(ST) at neutral loci rather than by Q(ST) at the quantitative traits themselves.