Coping with environmental constraints: Geographically divergent adaptive evolution and germination plasticity in the transcontinental Populus tremuloides

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. Elucidating species' 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's 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' range which can form the basis for climate-resilient revegetation.

Automated summary

This study investigates the genetic structure, reproductive type, and adaptive responses of aspen populations. The findings reveal the patterns of genetic variation as well as the selection responses to temperature and precipitation variations. The study uncovers the untapped adaptive potential of aspen populations, providing a basis for climate-resilient revegetation.