Coping with Environmental Constraints: Geographically Divergent Adaptive Evolution and Germination Plasticity in the Transcontinental \u3cem\u3ePopulus tremuloides\u3c/em\u3e

Societal Impact Statement Syntheses clearly show that global warming is affecting ecosystems and biodiversity around the world. New methods and measures are needed to predict the climate resilience of plant species critical to ecosystem stability, to improve ecological management and to support habitat restoration and human well-being. Widespread keystone species such as aspen are important targets in the study of resilience to future climate conditions because they play a crucial role in maintaining various ecosystem functions and may contain genetic material with untapped adaptive potential. Here, we present a new framework in support of climate-resilient revegetation based on comprehensively understood patterns of genetic variation in aspen. Summary Elucidating species\u27 genetic makeup and seed germination plasticity is essential to inform tree conservation efforts in the face of climate change. Populus tremuloides Michx. (aspen) occurs across diverse landscapes and reaches from Alaska to central Mexico, thus representing an early-successional model for ecological genomics. Within drought-affected regions, aspen shows ploidy changes and/or shifts from sexual to clonal reproduction, and reduced diversity and dieback have already been observed. We genotyped over 1000 individuals, covering aspen\u27s entire range, for approximately 44,000 single-nucleotide polymorphisms (SNPs) to assess large-scale and fine-scale genetic structure, variability in reproductive type (sexual/clonal), polyploidy and genomic regions under selection. We developed and implemented a rapid and reliable analysis pipeline (FastPloidy) to assess the presence of polyploidy. To gain insights into plastic responses, we contrasted seed germination from western US and eastern Canadian natural populations under elevated temperature and water stress. Four major genetic clusters were identified range wide; a preponderance of triploids and clonemates was found within western and southern North American regions, respectively. Genomic regions involving approximately 1000 SNPs under selection were identified with association to temperature and precipitation variation. Under drought stress, western US genotypes exhibited significantly lower germination rates compared with those from eastern North America, a finding that was unrelated to differences in mutation load (ploidy). This study provided new insights into the adaptive evolution of a key indicator tree that provisions crucial ecosystem services across North America, but whose presence is steadily declining within its western distribution. We uncovered untapped adaptive potential across the species\u27 range which can form the basis for climate-resilient revegetation

De chercheurs à détectives : au bouleau! : une approche multicritère pour comprendre le succès d'un syngaméon de bouleaux arbustifs d'Amérique du Nord face aux changements climatiques en régions subarctiques

Thèse ou mémoire avec insertion d’articlesLes bouleaux sont une composante importante du paysage forestier de l'hémisphère nord. Les bouleaux arbustifs, contribuant actuellement au verdissement de la toundra, sont des témoins privilégiés des changements climatiques (CC) en régionssubarctiques. À ce jour, ces espèces demeurent peu étudiées sur le plan génétique et des incertitudes persistent quant à leur taxonomie et leurs liens phylogénétiques. Le développement de connaissances sur la diversité génétique des espèces végétales nordiques et leur capacité d'adaptation aux CC sera essentiel pour mettre en place des mesures de conservation. L'objectif de l'étude était d'analyser la biogéographie et la diversité génétique du bouleau glanduleux (Betula glandulosa), un arbuste de la toundra nord-américaine. Un échantillonnage, à l'échelle de son aire de répartition en Amérique du Nord, a été réalisé. Une approche multicritère, basée sur la détermination du niveau de ploïdie, la génomique (échantillonnage des régions de l'ADN nucléaire et chloroplastique) et la morphologie, a été utilisée pour distinguer les individus de B. glandulosa des autres espèces de bouleaux, en raison des difficultés liées à la validation taxonomique des échantillons. Les résultats ont révélé la présence de trois espèces distinctes et leurs hybrides parmi les échantillons. L'analyse des polymorphismes nucléotidiques (« single nucleotide polymorphisms », SNP) nucléaires et chloroplastiques a mis en évidence une longue histoire d'échanges de gènes entre les différentes espèces et groupes génétiques. L'ensemble des résultats porte à croire que B. glandulosa fait partie d'un syngaméon de bouleaux arbustifs nord-américains avec B. pumila, B. nana et B. occidentalis. À l'échelle intraspécifique, deux groupes génétiques issus probablement de deux lignées glaciaires ont été détectés chez B. glandulosa en Amérique du Nord. L'étude souligne l'importance d'une approche multicritère pour décrire la diversité génétique intraspécifique lorsque les limites taxonomiques sont floues et l'importance de prendre en compte l'impact évolutif des espèces apparentées pour préserver la diversité génétique et la capacité d'adaptation dans un contexte de CC.Birches are an important component of the northern hemisphere forest landscape. Shrub birches, currently contributing to tundra greening, are an indicator of climate change in subarctic regions. To date, these species remain poorly studied genetically and uncertainties persist regarding their taxonomy and phylogenetic relationships. The development of knowledge on the genetic diversity of northern plant species and their ability to adapt to CC will be essential to implement conservation measures. This study aimed to analyze the biogeography and genetic diversity of dwarf birch (Betula glandulosa), a shrub of the North American tundra. Sampling was conducted throughout its North American range. A multicriteria approach, based on ploidy level assessment, genomics (sampling of nuclear and chloroplast DNA regions) and morphology, was used to distinguish individuals of B. glandulosa from other birch species, due to the difficulties associated with taxonomic validation of the samples. The results revealed the presence of three distinct species and their hybrids among the samples. Analysis of nuclear and chloroplast single nucleotide polymorphisms (SNPs) revealed a long history of gene exchange between the different species and genetic clusters. Taken together, the results suggest that B. glandulosa is part of a North American shrub birch syngameon with B. pumila, B. nana, and B. occidentalis. At the intraspecific level, two genetic clusters were detected within B. glandulosa in North America originating probably from two glacial lineages. The study highlights the importance of a multicriteria approach to describe intraspecific genetic diversity when taxonomic boundaries are blurred and to consider the evolutionary impact of related species to preserve genetic diversity and adaptive capacity in a climate change context

A cryptic syngameon within Betula shrubs revealed: Implications for conservation in changing subarctic environments

Abstract Arctic and subarctic ecosystems are rapidly transforming due to global warming, emphasizing the need to understand the genetic diversity and adaptive strategies of northern plant species for effective conservation. This study focuses on Betula glandulosa, a native North American tundra shrub known as dwarf birch, which demonstrates an apparent capacity to adapt to changing climate conditions. To address the taxonomic challenges associated with shrub birches and logistical complexities of sampling in the northernmost areas where species' ranges overlap, we adopted a multicriteria approach. Incorporating molecular data, ploidy level assessment and leaf morphology, we aimed to distinguish B. glandulosa individuals from other shrub birch species sampled. Our results revealed three distinct species and their hybrids within the 537 collected samples, suggesting the existence of a shrub birch syngameon, a reproductive network of interconnected species. Additionally, we identified two discrete genetic clusters within the core species, B. glandulosa, that likely correspond to two different glacial lineages. A comparison between the nuclear and chloroplast SNP data emphasizes a long history of gene exchange between different birch species and genetic clusters. Furthermore, our results highlight the significance of incorporating interfertile congeneric species in conservation strategies and underscores the need for a holistic approach to conservation in the context of climate change, considering the complex dynamics of species interactions. While further research will be needed to describe this shrub birches syngameon and its constituents, this study is a first step in recognizing its existence and disseminating awareness among ecologists and conservation practitioners. This biological phenomenon, which offers evolutionary flexibility and resilience beyond what its constituent species can achieve individually, may have significant ecological implications