Sally Aitken

As rapid climate change intensifies threats to forests, evaluating the strength, scale, and drivers of local adaptation to climate, as well as intraspecific genetic variation of climate adaptive traits, can improve predictions of forest responses and evaluating management strategies such as assisted migration. Additionally, assessing how tree breeding for growth affects climate adaptation could help mitigate potential impacts on forest health and productivity. I investigated local adaptation to climate in western larch (Larix occidentalis Nutt.) by combining extensive phenotyping from a seedling common garden experiment with 52 natural populations and genomic data from targeted exome-capture (pooled sequencing) of 44 populations from an adult provenance trial. I assessed adaptive and breeding potential by quantifying genetic variation and trait correlations at population and family levels under contrasting soil moisture conditions. I also evaluated the relative contributions of climate, geography, and neutral genetic structure to patterns of landscape genomic variation. Finally, I examined the effects of breeding for growth on climate adaptive traits by comparing 29 selectively-bred families and 23 natural populations from two breeding zones in British Columbia.Phenotypic and genomic evidence of local adaptation to climate was weak. Population differentiation was low for most traits, with weak clines associated with longitude and elevation rather than climatic variables expected to drive local adaptation. Partitioning of landscape genomic variation indicated that neutral genetic structure explained most of the genetic variance among populations, with climate and geography explaining little additional genetic variance. Genetic variation and heritability for drought resistance was limited, and genetic variation declined in growth and phenology under drought, indicating constraints to drought adaptation. Breeding for growth had minimal effects on climate adaptive traits, indicating that breeding has not likely altered risks associated with assisted migration. Overall, weak local adaptation suggests that assisted gene flow among populations may have limited benefits and risks for western larch. Combined with recent projected reductions in climatic suitability within the current range and expansion beyond the range based on climate niche models, these findings indicate that assisted migration beyond the natural range will likely be an important management strategy for western larch forests under future climates.

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There is an urgent need to better understand how populations of trees will respond to changes in climate and the intensification of extreme weather events. Characterizing the amount of genetic variation and genetic architecture of climate-adaptive traits is important for developing management approaches that mitigate the effects of climate change on forests. In this dissertation, I combined three large-scale common garden experiments (~6,000 seedlings) with population genomic approaches to investigate phenotypic and genomic variation across the natural ranges of the two main varieties of Douglas-fir (Pseudotsuga menziesii var. menziesii and var. glauca), as well as within breeding zones in British Columbia. Seedlings from 74 natural and 14 selected breeding populations were assessed for drought tolerance, cold hardiness, growth, phenology, and plastic responses to drought. I also used a case-control genome-wide association approach to identify single nucleotide polymorphisms (SNPs) associated with drought tolerance and cold hardiness within populations, and tested for repeated evolution between varieties, pleiotropy between traits, and allelic clines along environmental gradients. Finally, I tested the effects of selection for growth in tree breeding programs on climate adaptive phenotypes, and on the frequency of SNPs associated with cold hardiness and drought tolerance, by comparing selected seedlots with their wild counterparts. Signals of local adaptation to drought were weak within var. glauca and nearly absent within var. menziesii. Genetic variation for drought tolerance in seedlings is maintained primarily within rather than among populations. The complex polygenic architectures and genomic redundancy controlling climate adaptation make it challenging to use genomic information in management of Douglas-fir. Selection for faster growth reduced cold hardiness in var. menziesii, but had weaker effects in var. glauca. Drought tolerance was not affected by selection for faster growth. There is potential to increase drought tolerance through selection within breeding populations. These results collectively can inform adjustments to assisted gene flow in Douglas-fir.

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The interior spruce of western Canada comprises complex hybrids of white spruce (Picea glauca) and Engelmann spruce (Picea engelmannii). These trees are a keystone of their ecosystems and are economically important to forestry in western Canada. As rapid climate change is a particular threat to long-lived forest trees, understanding climate adaptation in this species complex is critical to anticipate and mitigate impacts to our forests.Using an existing dataset of genotyped seedlings representing 254 provenances throughout British Columbia and Alberta, I assessed the role of hybridization in climate adaptation within this species complex. Using a novel climatic similarity index, I determined that the hybrid zone is a climatic mosaic of its parent species’ ranges, with a precipitation regime more similar to white spruce and a winter temperature regime more similar to Engelmann spruce.I identified SNPs with an excess of alleles from one parent species across a broad range of hybrids. SNPs with a bias towards Engelmann spruce alleles tended to be strongly correlated with temperature variables, while SNPs with higher white spruce allele frequencies were more correlated with precipitation variables, suggesting that favorable parental alleles efficiently introgress into hybrids and allow them to adapt to novel climates.Using the strong relationship between hybrid index and climate, I combined genomic and climate data with existing ecological plot data to model hybrid index throughout western Canada. These models were applied to paleoclimatic simulations which, combined with mitochondrial haplotypes, allowed me to infer the colonization history of spruce in western Canada following deglaciation. I also used these hybrid index models to estimate the impacts of contemporary and future climate change on the hybrid zone, predicting large shifts in species ranges and large genomic shifts in areas where spruce persists.Together, these results demonstrate that hybridization has greatly contributed to local climate adaptation in interior spruce, and that climate change poses an existential threat to forests in the finely tuned adaptive landscape of this hybrid zone. This knowledge of local adaptation can inform our reforestation practices, as human intervention will be necessary to align genotypes to climates over the coming decades.

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Amphibian populations are declining worldwide due to many threats including habitat destruction, disease, non-native species and climate change, and are in dire need of informed conservation strategies. Island populations are particularly at risk. Invasive species are a major threat to amphibians on islands, along with habitat destruction and reduced genetic diversity in island populations. Additionally, species’ ranges are naturally shifting due to climate change, bringing the definition of a non-native species into flux. In this thesis, I aimed to improve the understanding of population-level dynamics and provide insights for conservation of amphibians using tools from invasion biology, experimental ecology, population genomics and conservation biology. I focussed on two amphibians of conservation concern in British Columbia (BC), Canada - the Northern Red-legged Frog (Rana aurora; NRLF), introduced to the Haida Gwaii Archipelago but native to southwest BC, and the Western Toad (Anaxyrus boreas boreas, called Hlk’yáan Ḵ’ust’áan in the X̱aad Kíl dialect of the Haida language (X̱aad Kíl Née; Haida Language Council), native to both areas.I modelled the distribution of the NRLF under current and future climate, conducted a mesocosm experiment examining the effect of co-occurrence history and naïveté on competition between the Western Toad and NRLF using populations from Haida Gwaii and southwest BC, and conducted genomic analyses of diversity and divergence of 27 Western Toad (hereafter “toad”) populations on Haida Gwaii and southwest BC.Together, my research suggests that: 1) the introduced NRLF has spread since its discovery on Haida Gwaii in 2002, and will likely spread further on Haida Gwaii, especially with climate change; 2) Haida Gwaii toad tadpoles are weaker competitors with the introduced NRLF compared to southwest BC toad tadpoles, likely due to their short history of co-occurrence (but it is unknown whether competition with NRLFs affects toad population persistence); and finally, 3) Haida Gwaii toad populations are genetically distinct and less diverse compared to southwest BC toad populations. The observed toad genetic patterns could be due to a historical population bottleneck or founder effect as well as contemporary small effective population size. This thesis provides knowledge that can be used to help conserve amphibians.

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The emergence of locally unfamiliar climates due to anthropogenic global warming is compelling scientists and resource managers to seek ecological data and management strategies from non-local climates, known as climate analogs. In this context, novel climates—emerging conditions with no analog in the observational record—represent widening gaps in the ecological knowledge base. Identification of novel climates is essential to climate change adaptation. However, methods to detect novel climates have not kept pace with this necessity. The goal of this dissertation is to advance methods for detection of novel climates in the context of ecology and forest management. I develop a multivariate metric for climatic novelty, sigma dissimilarity, that uses the local historical range of interannual climatic variability as a scale for measuring the ecological significance of climatic differences. I apply this metric at three scales—continental, jurisdictional, and local—each of which offers a distinct perspective on the implications of climatic novelty. At the continental scale, I assess the emergence of novel climates in North America, where they are an important source of extrapolation error in ecological modeling. I demonstrate the potential for novel climates to emerge throughout the continent, particularly at low topographic positions. At the jurisdictional scale, I assess the emergence of novel climates that are not represented in a structured knowledge system for forest management—the Biogeoclimatic Ecosystem Classification for British Columbia. A parallel novelty assessment using sigma dissimilarity and random forest classification indicates a robust pattern of novel climates in BC, for which analogs from outside BC must be identified. At the local scale, I demonstrate that dependencies among climate variables can produce larger and earlier departures from natural variability than is detectable in individual variables. This multivariate departure intensification effect—evident in distinct regions of the planet in global climate models—indicates adaptive challenges for ecological and human communities as their local climates become unfamiliar. The identification of locally unfamiliar and regionally novel climates is an important step in anticipating and adapting to climate change. Further, the challenges presented by novel climates are yet another basis to advocate for global emissions reductions.

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Anthropogenic climate change is shifting species ranges and exerting high selection pressures on populations of all taxa, including trees. Temperate tree species of the northern hemisphere share a history of large-scale postglacial colonization during the Quaternary, providing a natural laboratory for the study of evolutionary responses to climate fluctuations. This dissertation aims at improving our understanding of the mutual influences of demography and evolutionary patterns during range expansions in trees using Picea sitchensis (Sitka spruce) as a focal species.I first focused on the most recent P. sitchensis expansion event in south-central Alaska to study the interplay between demography and population genetics by combining neutral genetic markers and tree ring data. This multidisciplinary approach allowed me to assess the pace of neutral evolution across five centuries of colonization. Allelic richness was efficiently recovered in the colonizing population by early, open-grown colonizers on the Kodiak Archipelago during a long phase of low population growth. However, heterozygosity remains low compared with the nearest mainland populations. These results highlight the long-term importance of early colonizing genotypes in genetics of populations and the influence of pollen dispersal in maintaining standing genetic variation during forest expansion.Local hybridization of P. sitchensis colonizers with foreign pollen from white spruce (Picea glauca) populations occurred repeatedly during the early colonization period. However, introgression was suppressed in subsequent generations growing under a closed canopy. As the two species occupy separate climatic niches, selection against hybrids, intensified by competition, might explain this pattern. Spring precipitation tended to affect hybrid growth more negatively than pure P. sitchensis genotypes, but this effect was nonsignificant.I finally assessed the extent to which demographic parameters of range expansion can be estimated from genomic data through simulations using the approximate Bayesian computation framework. Simple 3-parameter models could be successfully estimated with genetic markers developed from reduced-representation methods currently available for nonmodel species. Models of higher complexity presented challenges, especially when ongoing migration after expansion was considered, and the accuracy of results depended on the time of expansion. The demic expansion models examined here were inadequate to infer the colonization history of P. sitchensis.

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Climate change is disrupting local adaptation in temperate and boreal tree species. As climates shift, tree breeding zones are becoming dissociated from their historical climatic optima and no longer represent optimal seed deployment zones. Assisted gene flow (AGF) policies that match reforestation seedlots with future climates require accurate knowledge of genetic variation in climatically adaptive traits in breeding populations. In this thesis I evaluate the effects of selective breeding on climatic adaptation in the two most planted species in western Canada, lodgepole pine (Pinus contorta) and interior spruce (Picea glauca, P. engelmanii and their hybrids), to inform provincial AGF prescriptions. I compared natural stand seedlots (n = 105 pine, 154 spruce) with selectively bred seedlots (n = 20 pine, 18 spruce) from across Alberta and British Columbia in common garden experiments. Phenotypic variation among breeding zones was assessed for growth, phenology and cold hardiness in relation to climate. For both species, phenotypic differences between natural and selected seedlings in growth traits were substantial. Height gains resulted from increased growth rate and delayed growth cessation, but autumn cold hardiness was not substantially reduced. Seedlings were also genotyped for ~30,000 candidate single nucleotide polymorphisms for growth and adaptive traits. Selection for growth has shifted interior spruce hybrid ancestry in some breeding populations, but these effects are not consistent across zones. A genome-wide association study of pine identified many trait-associated SNPs. Positive effect allele frequencies among pine breeding zones were strongly associated with climatic variation. Selection has resulted in small increases in the frequency of positive effect alleles in breeding populations. Associations among cold hardiness phenotypes, genotypes and climate dominated signals of local adaptation were preserved in breeding populations. Selection, breeding and progeny testing combined have produced taller pine and spruce seedlings without compromising climatic adaptation. Strong phenotype-genotype-climate associations suggest AGF will be necessary to match breeding populations with future climates, but selectively bred and natural seedlots can be safely redeployed using the same AGF prescriptions. Multi-locus genomic profiles of adaptive traits associated with climate provide an accurate, rapid method to assess climatic adaptation that is independent from long-term provenance trials.

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Natural hybrid zones provide a great opportunity to study the evolutionary relationshipsbetween closely related species. I have combined ten microsatellites (SSR) and 311 singlenucleotide polymorphism (SNP) markers with quantitative data to investigate the geneticstructure, interspecific gene flow and adaptation of the economically and ecologically importantPicea glauca (white spruce) x P. engelmannii (Engelmann spruce) hybrid zone in westernNorth America. Climate modelling and paleoclimate analysis was used to study the historicalevolutionary relationships between hybridizing species; and to predict future patterns of geneticvariation in the zone. This modelling suggests these species may have been in contact for aslong as 21,000 years. Current levels of admixture and introgression are extensive, assuggested by both the SSR and SNP analyses, with populations showing elevational andlatitudinal unimodal clines in admixture. Hybrids occupy intermediate environments in the zoneand show a higher genetic contribution from Engelmann spruce than from white spruce onaverage. Despite a long history of interspecific gene flow, pure species and hybrids areadapted to different environments. Results of the quantitative analysis based on long-term dataon growth and survival, as well as bud phenology and cold hardiness, indicate that the white xEngelmann spruce hybrid zone is maintained by adaptation to the length of growing seasonsand the persistence of the snowpack (exogenous selection), in which hybrids are fitter thanpure species in intermediate environments, fitting the "Bounded hybrid superiority" model of hybrid zone maintenance. I identified 12 outlier SNPs among the 311 SNPs; these were genesresponsible for carbohydrate metabolism, signal transduction and transcription factors. Theseresults have significant implications for forest management and breeding of spruce species inBritish Columbia, where this species complex is managed as one species without consideringthe complexity in population structure and adaptive differences between pure species andhybrids.

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Natural hybrid zones may be viewed as important biological systems for examining the role of selection in creating and maintaining species differences. Where ecological differences exist between hybridizing species, these zones may provide useful insight into the genetic architecture of important traits involved in adaptation. I have evaluated the genomic and phenotypic architecture of the economically and ecologically important Picea sitchensis (Sitka spruce) x P. glauca (white spruce) hybrid zone along the Nass and Skeena river valleys in northwestern British Columbia using chloroplast and mitochondrial markers, twelve microsatellite loci (SSRs), and 268 single nucleotide polymorphisms (SNPs), in combination with morphological variation, and phenotypic data from a common garden. Maternally- and paternally-inherited organelle markers, in combination with bi-parentally inherited nuclear markers, were used to estimate both the historic and contemporary direction and extent of gene flow within the hybrid zone. Sitka spruce mitotype ‘capture’ throughout the introgression zone point towards asymmetric gene flow, congruent with microsatellites and SNPs, indicating extensive long-term introgression and widespread recombination with more Sitka spruce than white spruce ancestry in hybrid populations. Significant clinal variation was observed for marker-based hybrid indices and morphological traits associated with climate and geography, while growth and cold hardiness traits evaluated in a common garden exhibited weak to non-significant clines. These results indicate extrinsic selection appears to play a strong role in the distribution and structure of this hybrid zone, which fits expectations for the environmentally-determined bounded hybrid superiority model of hybrid zone maintenance. However, intrinsic mechanisms of hybrid zone maintenance could not be ruled out. Finally, broad-scale patterns of variation, combined with fine-scale analysis of candidate SNP-specific patterns of introgression revealed a suite of candidate loci that may be targets of extrinsic or intrinsic selection. These loci may be involved in either adaptation to climate across the zone, particularly precipitation gradients, or involved in the maintenance of species barriers. These results have important implications for genetic conservation of adaptive variation, selection of seed sources for current reforestation within this ecologically transitional area, and appropriate scale and direction of seed transfer relating current genotype-climate associations to future climate predictions for this region.

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Climate change will affect the regeneration, growth, survival and distribution of trees. Here, I use common gardens to empirically test establishment, growth and the potential for persistence, adaptation and migration for two iconic North American trees, whitebark pine (Pinus albicaulis) and lodgepole pine (Pinus contorta ssp. latifolia). Whitebark pine is of conservation concern due to range-wide diebacks, while lodgepole pine is critical to forest productivity and carbon sequestration. Whitebark seeds were planted north of the current range in areas predicted to be climatically suitable through the 2050s; these germinated and survived in varying proportions at all locations. Establishment and growth were positively affected by moderate snow-cover durations, heavier seed weights, and warmer provenance temperatures. Whitebark pine seedlings grown from seeds sown in growth chambers spanning current and predicted-future temperatures demonstrated positive responses to warmer growing seasons. Lodgepole pine seedlings in the same chambers outgrew the whitebark pine seedlings at all but the coldest temperatures. Together, these results suggest that whitebark pine may lose its competitive advantage to other species within its narrow alpine-treeline niche as the climate warms, but that it is capable of establishing in climatically-suitable areas north of its current range. Using tree-ring data from long-term lodgepole pine common garden trials, I built universal growth-trend response functions to forecast future growth trends relative to genetics, climate and tree age. The models predict growth reductions for all populations by the end of the 21st century based on middle-of-the-road climate models, except in far northern areas near and within Yukon, Canada. Analogous models built using summer and winter climate indices indicate that the growth declines are primarily caused by warmer summers, and may be offset by growth increases resulting from warmer winters. I found that populations are most sensitive to annual temperatures and summer aridity, but that sensitivity to climate varies due to local adaptation. Overall, my research will help forest professionals and conservationists forecast changes in forest productivity and species growth and survival under warming temperatures.

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Genecological studies in widely distributed tree species have revealed steep genetic clines along environmental gradients for traits related to adaptation to local climate. In the face of a changing climate, the ecological and economic importance of conifers necessitates an appraisal of how molecular genetic variation shapes quantitative trait variation. I have combined transcript profiling with association mapping to better understand the genomic architecture of adaptation to local climate in conifers, using Sitka spruce (Picea sitchensis) as a model. A microarray study during the fall hardening period revealed wholesale remodeling of the transcriptome within a population originating in the centre of the species range, and substantial variation in the autumn transcriptome was observed when populations from the northern and southern limits of the range were compared. Based on these data, a suite of candidate genes was selected and screened for single nucleotide polymorphisms (SNPs) in a panel of 24 individuals. A diverse array of biological processes were represented among the candidate genes, including stress response, carbohydrate, lipid and phenylpropanoid metabolism, light signal transduction, and transcriptional and posttranscriptional regulation. Nucleotide diversity in Sitka spruce was approximately average for a conifer (π = 3.49 x 10⁻³), and linkage disequilibrium decayed rapidly. Tests of selective neutrality suggest widespread purifying selection within these candidate genes, though evidence for positive selection was detected within a few. In addition, I observed evidence for diversifying selection in 8% of the studied genes, which exhibited high population differentiation relative to the genome-wide average FST of 0.12. To identify genetic determinants of phenotypic variation in locally adaptive traits, an Illumina GoldenGate assay was used to genotype 768 SNPs in a mapping population comprised of 410 individuals from 12 geographical populations collected from across the species range. After correcting for population structure and relative kinship, associations were detected in 28 of the candidate genes, which cumulatively explained 28% and 34% of the phenotypic variance in cold hardiness and budset, respectively. Most notable among these associations were five genes putatively involved in light signal transduction, the key pathway regulating autumn growth cessation in perennials. This study represents a significant step toward the goal of characterizing the genomic underpinnings of adaptation to local climate in conifers, and provides a substantial resource for breeding and conservation genetics in a changing climate.

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