Contrasting physiological strategies explain heterogeneous responses to severe drought conditions within local populations of a widespread conifer.

Understanding how trees prioritize carbon gain at the cost of drought vulnerability under severe drought conditions is crucial for predicting which genetic groups and individuals will be resilient to future climate conditions. In this study, we investigated variations in growth, tree-ring anatomy as well as carbon and oxygen isotope ratios to assess the sensitivity and the xylem formation process in response to an episode of severe drought in 29 mature white spruce (Picea glauca [Moench] Voss) families grown in a common garden trial. During the drought episode, the majority of families displayed decreased growth and exhibited either sustained or increased intrinsic water-use efficiency (iWUE), which was largely influenced by reduced stomatal conductance as revealed by the dual carbon­oxygen isotope approach. Different water-use strategies were detected within white spruce populations in response to drought conditions. Our results revealed intraspecific variation in the prevailing physiological mechanisms underlying drought response within and among populations of Picea glauca. The presence of different genetic groups reflecting diverse water-use strategies within this largely-distributed conifer is likely to lessen the negative effects of drought and decrease the overall forest ecosystems' sensitivity to it.

Increasing genomic prediction accuracy for unphenotyped full-sib families by modeling additive and dominance effects with large datasets in white spruce.

Introduction: Genomic selection is becoming a standard technique in plant breeding and is now being introduced into forest tree breeding. Despite promising results to predict the genetic merit of superior material based on their additive breeding values, many studies and operational programs still neglect non-additive effects and their potential for enhancing genetic gains. Methods: Using two large comprehensive datasets totaling 4,066 trees from 146 full-sib families of white spruce (Picea glauca (Moench) Voss), we evaluated the effect of the inclusion of dominance on the precision of genetic parameter estimates and on the accuracy of conventional pedigree-based (ABLUP-AD) and genomic-based (GBLUP-AD) models. Results: While wood quality traits were mostly additively inherited, considerable non-additive effects and lower heritabilities were detected for growth traits. For growth, GBLUP-AD better partitioned the additive and dominance effects into roughly equal variances, while ABLUP-AD strongly overestimated dominance. The predictive abilities of breeding and total genetic value estimates were similar between ABLUP-AD and GBLUP-AD when predicting individuals from the same families as those included in the training dataset. However, GBLUP-AD outperformed ABLUP-AD when predicting for new unphenotyped families that were not represented in the training dataset, with, on average, 22% and 53% higher predictive ability of breeding and genetic values, respectively. Resampling simulations showed that GBLUP-AD required smaller sample sizes than ABLUP-AD to produce precise estimates of genetic variances and accurate predictions of genetic values. Still, regardless of the method used, large training datasets were needed to estimate additive and non-additive genetic variances precisely. Discussion: This study highlights the different quantitative genetic architectures between growth and wood traits. Furthermore, the usefulness of genomic additive-dominance models for predicting new families should allow practicing mating allocation to maximize the total genetic values for the propagation of elite material.

The phenotypic and genetic effects of drought-induced stress on wood specific conductivity and anatomical properties in white spruce seedlings, and relationships with growth and wood density.

Drought frequency and intensity are projected to increase with climate change, thus amplifying stress on forest trees. Resilience to drought implicates physiological traits such as xylem conductivity and wood anatomical traits, which are related to growth and wood density. Integrating drought-stress response traits at the juvenile stage into breeding criteria could help promote the survival of planted seedlings under current and future climate and thus, improve plantation success. We assessed in greenhouse the influence of drought-induced stress on 600 two-year-old white spruce (Picea glauca) seedlings from 25 clonal lines after two consecutive growing seasons. Three levels of drought-induced stress were applied: control, moderate and severe. Seedlings were also planted at a 45° angle to clearly separate compression from normal wood. We looked at the phenotypic and genetic effects of drought stress on xylem specific hydraulic conductivity, lumen diameter, tracheid diameter and length, and the number of pits per tracheid in the normal wood. We detected no significant effects of drought stress except for tracheid length, which decreased with increasing drought stress. We found low to high estimates of trait heritability, which generally decreased with increasing drought stress. Genetic correlations were higher than phenotypic correlations for all treatments. Specific conductivity was genetically highly correlated positively with lumen diameter and tracheid length under all treatments. Tracheid length and diameter were always negatively correlated genetically, indicating a trade-off in resource allocation. Moderate to high genetic correlations sometimes in opposite direction were observed between physico-anatomical and productivity traits, also indicating trade-offs. A large variation was observed among clones for all physico-anatomical traits, but clonal ranks were generally stable between control and drought-induced treatments. Our results indicate the possibility of early screening of genetic material for desirable wood anatomical attributes under normal growing conditions, thus allowing to improve the drought resilience of young trees.

Breeding for adaptation to climate change: genomic selection for drought response in a white spruce multi-site polycross test.

With climate change, increasingly intense and frequent drought episodes will be affecting water availability for boreal tree species, prompting tree breeders and forest managers to consider adaptation to drought stress as a priority in their reforestation efforts. We used a 19-year-old polycross progeny test of the model conifer white spruce (Picea glauca) replicated on two sites affected by distinct drought episodes at different ages to estimate the genetic control and the potential for improvement of drought response in addition to conventional cumulative growth and wood quality traits. Drought response components were measured from dendrochronological signatures matching drought episodes in wood ring increment cores. We found that trees with more vigorous growth during their lifespan resisted better during the current year of a drought episode when the drought had more severe effects. Phenotypic data were also analyzed using genomic prediction (GBLUP) relying on the genomic relationship matrix of multi-locus gene SNP marker information, and conventional analysis (ABLUP) based on validated pedigree information. The accuracy of predicted breeding values for drought response components was marginally lower than that for conventional traits and comparable between GBLUP and ABLUP. Genetic correlations were generally low and nonsignificant between drought response components and conventional traits, except for resistance which was positively correlated to tree height. Heritability estimates for the components of drought response were slightly lower than for conventional traits, but similar single-trait genetic gains could be obtained. Multi-trait genomic selection simulations indicated that it was possible to improve simultaneously for all traits on both sites while sacrificing little on gain in tree height. In a context of rapid climate change, our results suggest that with careful phenotypic assessment, drought response may be considered in multi-trait improvement of white spruce, with accelerated screening of large numbers of candidates and selection at young age with genomic selection.

Connecting tree-ring phenotypes, genetic associations and transcriptomics to decipher the genomic architecture of drought adaptation in a widespread conifer.

As boreal forests face significant threats from climate change, understanding evolutionary trajectories of coniferous species has become fundamental to adapting management and conservation to a drying climate. We examined the genomic architecture underlying adaptive variation related to drought tolerance in 43 populations of a widespread boreal conifer, white spruce (Picea glauca [Moench] Voss), by combining genotype-environment associations, genotype-phenotype associations, and transcriptomics. Adaptive genetic variation was identified by correlating allele frequencies for 6,153 single nucleotide polymorphisms from 2,606 candidate genes with temperature, precipitation and aridity gradients, and testing for significant associations between genotypes and 11 dendrometric and drought-related traits (i.e., anatomical, growth response and climate-sensitivity traits) using a polygenic model. We identified a set of 285 genes significantly associated with a climatic factor or a phenotypic trait, including 110 that were differentially expressed in response to drought under greenhouse-controlled conditions. The interlinked phenotype-genotype-environment network revealed eight high-confidence genes involved in white spruce adaptation to drought, of which four were drought-responsive in the expression analysis. Our findings represent a significant step toward the characterization of the genomic basis of drought tolerance and adaptation to climate in conifers, which is essential to enable the establishment of resilient forests in view of new climate conditions.

Genomic selection for resistance to spruce budworm in white spruce and relationships with growth and wood quality traits.

With climate change, the pressure on tree breeding to provide varieties with improved resilience to biotic and abiotic stress is increasing. As such, pest resistance is of high priority but has been neglected in most tree breeding programs, given the complexity of phenotyping for these traits and delays to assess mature trees. In addition, the existing genetic variation of resistance and its relationship with productivity should be better understood for their consideration in multitrait breeding. In this study, we evaluated the prospects for genetic improvement of the levels of acetophenone aglycones (AAs) in white spruce needles, which have been shown to be tightly linked to resistance to spruce budworm. Furthermore, we estimated the accuracy of genomic selection (GS) for these traits, allowing selection at a very early stage to accelerate breeding. A total of 1,516 progeny trees established on five sites and belonging to 136 full-sib families from a mature breeding population in New Brunswick were measured for height growth and genotyped for 4,148 high-quality SNPs belonging to as many genes along the white spruce genome. In addition, 598 trees were assessed for levels of AAs piceol and pungenol in needles, and 578 for wood stiffness. GS models were developed with the phenotyped trees and then applied to predict the trait values of unphenotyped trees. AAs were under moderate-to-high genetic control (h 2: 0.43-0.57) with null or marginally negative genetic correlations with other traits. The prediction accuracy of GS models (GBLUP) for AAs was high (PAAC: 0.63-0.67) and comparable or slightly higher than pedigree-based (ABLUP) or BayesCπ models. We show that AA traits can be improved and that GS speeds up the selection of improved trees for insect resistance and for growth and wood quality traits. Various selection strategies were tested to optimize multitrait gains.

Adaptive genetic variation to drought in a widely distributed conifer suggests a potential for increasing forest resilience in a drying climate.

Drought intensity and frequency are increasing under global warming, with soil water availability now being a major factor limiting tree growth in circumboreal forests. Still, the adaptive capacity of trees in the face of future climatic regimes remains poorly documented. Using 1481 annually resolved tree-ring series from 29-yr-old trees, we evaluated the drought sensitivity of 43 white spruce (Picea glauca (Moench) Voss) populations established in a common garden experiment. We show that genetic variation among populations in response to drought plays a significant role in growth resilience. Local genetic adaptation allowed populations from drier geographical origins to grow better, as indicated by higher resilience to extreme drought events, compared with populations from more humid geographical origins. The substantial genetic variation found for growth resilience highlights the possibility of selecting for drought resilience in boreal conifers. As a major research outcome, we showed that adaptive genetic variation in response to changing local conditions can shape drought vulnerability at the intraspecific level. Our findings have wide implications for forest ecosystem management and conservation.

Genomic prediction for hastening and improving efficiency of forward selection in conifer polycross mating designs: an example from white spruce.

Genomic selection (GS) has a large potential for improving the prediction accuracy of breeding values and significantly reducing the length of breeding cycles. In this context, the choice of mating designs becomes critical to improve the efficiency of breeding operations and to obtain the largest genetic gains per time unit. Polycross mating designs have been traditionally used in tree and plant breeding to perform backward selection of the female parents. The possibility to use genetic markers for paternity identification and for building genomic prediction models should allow for a broader use of polycross tests in forward selection schemes. We compared the accuracies of genomic predictions of offspring's breeding values from a polycross and a full-sib (partial diallel) mating design with similar genetic background in white spruce (Picea glauca). Trees were phenotyped for growth and wood quality traits, and genotyped for 4092 SNPs representing as many gene loci distributed across the 12 spruce chromosomes. For the polycross progeny test, heritability estimates were smaller, but more precise using the genomic BLUP (GBLUP) model as compared with pedigree-based models accounting for the maternal pedigree or for the reconstructed full pedigree. Cross-validations showed that GBLUP predictions were 22-52% more accurate than predictions based on the maternal pedigree, and 5-7% more accurate than predictions using the reconstructed full pedigree. The accuracies of GBLUP predictions were high and in the same range for most traits between the polycross (0.61-0.70) and full-sib progeny tests (0.61-0.74). However, higher genetic gains per time unit were expected from the polycross mating design given the shorter time needed to conduct crosses. Considering the operational advantages of the polycross design in terms of easier handling of crosses and lower associated costs for test establishment, we believe that this mating scheme offers great opportunities for the development and operational application of forward GS.

Multi-trait genomic selection for weevil resistance, growth, and wood quality in Norway spruce.

Plantation-grown trees have to cope with an increasing pressure of pest and disease in the context of climate change, and breeding approaches using genomics may offer efficient and flexible tools to face this pressure. In the present study, we targeted genetic improvement of resistance of an introduced conifer species in Canada, Norway spruce (Picea abies (L.) Karst.), to the native white pine weevil (Pissodes strobi Peck). We developed single- and multi-trait genomic selection (GS) models and selection indices considering the relationships between weevil resistance, intrinsic wood quality, and growth traits. Weevil resistance, acoustic velocity as a proxy for mechanical wood stiffness, and average wood density showed moderate-to-high heritability and low genotype-by-environment interactions. Weevil resistance was genetically positively correlated with tree height, height-to-diameter at breast height (DBH) ratio, and acoustic velocity. The accuracy of the different GS models tested (GBLUP, threshold GBLUP, Bayesian ridge regression, BayesCπ) was high and did not differ among each other. Multi-trait models performed similarly as single-trait models when all trees were phenotyped. However, when weevil attack data were not available for all trees, weevil resistance was more accurately predicted by integrating genetically correlated growth traits into multi-trait GS models. A GS index that corresponded to the breeders' priorities achieved near maximum gains for weevil resistance, acoustic velocity, and height growth, but a small decrease for DBH. The results of this study indicate that it is possible to breed for high-quality, weevil-resistant Norway spruce reforestation stock with high accuracy achieved from single-trait or multi-trait GS.

The impact of reconstructed soils following oil sands exploitation on aspen and its associated belowground microbiome.

The objective of this study was to investigate the impact of different soil covers used to reclaim decommissioned oil sands mining sites on the genetic diversity of aspen and their associated belowground microbiota. Aspen genotyping showed that trees mostly originated from sexual reproduction on sites reclaimed with soil covers made of upland forest floor-mineral mix (FFMM) and lowland peat-mineral mix (PMM). In contrast, most individuals in mature and burned stands sampled as benchmarks for natural disturbances originated from vegetative reproduction. Nonetheless, aspen populations in the FFMM and PMM sites were not genetically different from those in mature and burned stands. DNA metabarcoding of bacteria and fungi in root and soil samples revealed that the diversity of the belowground microbiota associated with aspen and the relative abundance of putative symbiotic taxa in PMM were significantly lower than for FFMM and naturally disturbed sites. Despite similar aspen genetic diversity between FFMM and PMM sites, trees were not associated with the same belowground microbiota. Because the soil microbiome and more specifically the mycorrhizal communities are variable both in space and time, long-term monitoring is particularly important to better understand the ecological trajectory of these novel ecosystems.

Tree rings provide a new class of phenotypes for genetic associations that foster insights into adaptation of conifers to climate change.

Local adaptation in tree species has been documented through a long history of common garden experiments where functional traits (height, bud phenology) are used as proxies for fitness. However, the ability to identify genes or genomic regions related to adaptation to climate requires the evaluation of traits that precisely reflect how and when climate exerts selective constraints. We combine dendroecology with association genetics to establish a link between genotypes, phenotypes and interannual climatic fluctuations. We illustrate this approach by examining individual tree responses embedded in the annual rings of 233 Pinus strobus trees growing in a common garden experiment representing 38 populations from the majority of its range. We found that interannual variability in growth was affected by low temperatures during spring and autumn, and by summer heat and drought. Among-population variation in climatic sensitivity was significantly correlated with the mean annual temperature of the provenance, suggesting local adaptation. Genotype-phenotype associations using these new tree-ring phenotypes validated nine candidate genes identified in a previous genetic-environment association study. Combining dendroecology with association genetics allowed us to assess tree vulnerability to past climate at fine temporal scales and provides avenues for future genomic studies on functional adaptation in forest trees.

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines.

Accurately detecting signatures of local adaptation using genetic-environment associations (GEAs) requires controlling for neutral patterns of population structure to reduce the risk of false positives. However, a high degree of collinearity between climatic gradients and neutral population structure can greatly reduce power, and the performance of GEA methods in such case is rarely evaluated in empirical studies. In this study, we attempted to disentangle the effects of local adaptation and isolation by environment (IBE) from those of isolation by distance (IBD) and isolation by colonization from glacial refugia (IBC) using range-wide samples in two white pine species. For this, SNPs from 168 genes, including 52 candidate genes for growth and phenology, were genotyped in 133 and 61 populations of Pinus strobus and P. monticola, respectively. For P. strobus and using all 153 SNPs, climate (IBE) did not significantly explained among-population variation when controlling for IBD and IBC in redundancy analyses (RDAs). However, 26 SNPs were significantly associated with climate in single-locus GEA analyses (Bayenv2 and LFMM), suggesting that local adaptation took place in the presence of high gene flow. For P. monticola, we found no evidence of IBE using RDAs and weaker signatures of local adaptation using GEA and FST outlier tests, consistent with adaptation via phenotypic plasticity. In both species, the majority of the explained among-population variation (69 to 96%) could not be partitioned between the effects of IBE, IBD, and IBC. GEA methods can account differently for this confounded variation, and this could explain the small overlap of SNPs detected between Bayenv2 and LFMM. Our study illustrates the inherent difficulty of taking into account neutral structure in natural populations and the importance of sampling designs that maximize climatic variation, while minimizing collinearity between climatic gradients and neutral structure.

Convergent local adaptation to climate in distantly related conifers.

When confronted with an adaptive challenge, such as extreme temperature, closely related species frequently evolve similar phenotypes using the same genes. Although such repeated evolution is thought to be less likely in highly polygenic traits and distantly related species, this has not been tested at the genome scale. We performed a population genomic study of convergent local adaptation among two distantly related species, lodgepole pine and interior spruce. We identified a suite of 47 genes, enriched for duplicated genes, with variants associated with spatial variation in temperature or cold hardiness in both species, providing evidence of convergent local adaptation despite 140 million years of separate evolution. These results show that adaptation to climate can be genetically constrained, with certain key genes playing nonredundant roles.

Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: a comparison between eastern and western North American postglacial colonization histories.

UNLABELLED: • Premises of the study: Understanding the influence of recent glacial and postglacial periods on species' distributions is key for predicting the effects of future environmental changes. We investigated the influence of two physiographic landscapes on population structure and postglacial colonization of two white pine species of contrasting habitats: P. monticola, which occurs in the highly mountainous region of western North America, and P. strobus, which occurs in a much less mountainous area in eastern North America.• METHODS: To characterize the patterns of genetic diversity and population structure across the ranges of both species, 158 and 153 single nucleotide polymorphism (SNP) markers derived from expressed genes were genotyped on range-wide samples of 61 P. monticola and 133 P. strobus populations, respectively.• KEY RESULTS: In P. monticola, a steep latitudinal decrease in genetic diversity likely resulted from postglacial colonization involving rare long-distance dispersal (LDD) events. In contrast, no geographic patterns of diversity were detected in P. strobus, suggesting recolonization via a gradually advancing front or frequent LDD events. For each species, structure analyses identified two distinct southern and northern genetic groups that likely originated from two different glacial lineages. At a finer scale, and for the two species, smaller subgroups were detected that could be remnants of cryptic refugia.• CONCLUSION: During postglacial colonization, the western and eastern North American landscapes had different impacts on genetic signatures in P. monticola compared with P. strobus. We discuss the importance of our findings for conservation programs and predictions of species' response to climate change.