Novel genomic offset metrics integrate local adaptation into habitat suitability forecasts and inform assisted migration

Abstract

Genomic data are increasingly being integrated into macroecological forecasting, offering an evolutionary perspective that has been largely missing from global change biogeography. Genomic offset, which quantifies the disruption of genotype–environment associations under environmental change, allows for the incorporation of intraspecific climate-associated genomic differentiation into forecasts of habitat suitability. Gradient Forest (GF) is a commonly used approach to estimate genomic offset; however, major hurdles in the application of GF-derived genomic offsets are (1) an inability to interpret their absolute magnitude in an ecologically meaningful way and (2) uncertainty in how their implications compare with those of species-level approaches like Ecological Niche Models (ENMs). Here, we assess the climate change vulnerability of red spruce (Picea rubens), a cool-temperate tree species endemic to eastern North America, using both ENMs and GF modeling of genomic variation along climatic gradients. To gain better insights into climate change risks, we derive and apply two new threshold-based genomic offset metrics—Donor and Recipient Importance—that quantify the transferability of propagules between donor populations and recipient localities while minimizing disruption of genotype–environment associations. We also propose and test a method for scaling genomic offsets relative to contemporary genomic variation across the landscape. In three common gardens, we found a significant negative relationship between (scaled) genomic offsets and red spruce growth and higher explanatory power for scaled offsets than climate transfer distances. However, the garden results also revealed the potential effects of spatial extrapolation and neutral genomic differentiation that can compromise the degree to which genomic offsets represent maladaptation and highlight the necessity of using common garden data to evaluate offset-based predictions. ENMs and our novel genomic offset metrics forecasted drastic northward range shifts in suitable habitats. Combining inferences from our offset-based metrics, we show that a northward shift mainly will be required for populations in the central and northern parts of red spruce's current range, whereas southern populations might persist in situ due to climate-associated variation with less offset under future climate. These new genomic offset metrics thus yield refined, region-specific prognoses for local persistence and show how management could be improved by considering assisted migration.