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Red spruce (Picea rubens Sarg.) is a coniferous tree with a highly fragmented range in eastern North American montane forests. It serves as a foundational species for many locally rare and threatened taxa and has therefore been the focus of large-scale reforestation efforts aimed at restoring these montane ecosystems, yet genetic input guiding these efforts has been lacking. To tackle this issue, we took advantage of a common garden experiment and a whole exome sequencing dataset to investigate the impact of different population genetic parameters on early-life seedling fitness in red spruce. The level of inbreeding, genetic diversity and genetic load were assessed for 340 mother trees sampled from 65 localities across the spe- cies range and compared to different fitness traits measured on 5100 of their seedlings grown in a controlled environment. We identified an overall positive influence of genetic diversity and negative impact of genetic load and population-level inbreeding on early-life fitness. Those associations were most apparent for the highly fragmented populations in the Central and Southern Appalachians, where lower genetic diversity and higher inbreeding were associated with lower germination rate, shorter height and reduced early-life fitness of the seedlings. These results provide unprecedented information that could be used by field managers aiming to restore red spruce forests and to maximize the success of future plantations. 

Understanding the factors influencing the current distribution of genetic diversity across a species range is one of the main questions of evolutionary biology, especially given the increasing threat to biodiversity posed by climate change. Historical demographic processes such as population expansion or bottlenecks and decline are known to exert a predominant influence on past and current levels of genetic diversity, and revealing this demo‐genetic history can have immediate conservation implications. We used a whole‐exome capture sequencing approach to analyze polymorphism across the gene space of red spruce (Picea rubens Sarg.), an endemic and emblematic tree species of eastern North America high‐elevation forests that are facing the combined threat of global warming and increasing human activities. We sampled a total of 340 individuals, including populations from the current core of the range in northeastern USA and southeastern Canada and from the southern portions of its range along the Appalachian Mountains, where populations occur as highly fragmented mountaintop “sky islands.” Exome capture baits were designed from the closely relative white spruce (P. glauca Voss) transcriptome, and sequencing successfully captured most regions on or near our target genes, resulting in the generation of a new and expansive genomic resource for studying standing genetic variation in red spruce applicable to its conservation. Our results, based on over 2 million exome‐derived variants, indicate that red spruce is structured into three distinct ancestry groups that occupy different geographic regions of its highly fragmented range. Moreover, these groups show small Ne , with a temporal history of sustained population decline that has been ongoing for thousands (or even hundreds of thousands) of years. These results demonstrate the broad potential of genomic studies for revealing details of the demographic history that can inform management and conservation efforts of nonmodel species with active restoration programs, such as red spruce.